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The Gametophyte-Sporophyte Junction in Land Plants
The Gametophyte-Sporophyte Junction in Land Plants
ROBERTO LIGRONE Dipartimento di Biologiu Vegetule, Universita di Napoli, Viu Foria 223, 1-80139 Nupoli, Italy JEFFREY G. DUCKETT School of Biological Sciences, Queen Mary and Westjield College, University of London, Mile End Road, London E l 4 N S , U K
and KAREN S. RENZAGLIA School of Biological Sciences, Box 23590A, East Tennessee State University, Johnson City, TN 37614, USA
I.
Introduction
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234 235 253 275
111.
The Taxonomic Significance of the Placenta in Bryophytes and Implications for Phylogeny . . . . . . . . . . . . . . . .
283
IV.
Pteridophytes . . . . . . . . . . . . . . . . . . . . . . .
295
V.
Seedplants . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . .
301 306 307
11.
Bryophytes . . . . . . . . . . . . . A. Mosses (Bryopsida) . . . . . . B. Liverworts (Hepatopsida) . . . C. Anthocerotes (Anthocerotopsida)
232
Advances in Botanical Research Vol. 19 ISBN (b12-00.5919-3
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Copyright 01993Academic Press Limited All rights of reproduction in any form reserved
232
R. LIGRONE ef a / .
I. INTRODUCTION The life-cycle of land plants characteristically involves an embryonic phase during which the sporophyte is associated with the parental gametophyte and has no direct contact with the substratum (Graham, 1985; Duckett and Renzaglia, 1988a). This phase is very short in lower tracheophytes, where the young sporophyte rapidly breaks free from the confines of the gametophyte and develops a root and an aerial photosynthetic system, thus becoming independent. Likewise, seed plants have a relatively short embryonic phase that terminates with seed germination after a dormant period of variable duration. By contrast, the sporophyte of bryophytes is permanently associated with the gametophyte and therefore retains structural if not functional dependence on the latter throughout its life-span. During development the embryo utilizes conspicuous amounts of organic compounds for growth and respiration. Moreover, in most cases, the embryo accumulates abundant reserves, mostly in the form of starch, proteins and lipids, that are utilized later in development. It is widely maintained that the bulk of these substances are of exogenous origin, the embryo being barely able to produce them autonomously. There is abundant evidence from physiological studies (Proctor, 1977; Courtice et a [ . , 1978;Thomas et af.,1978,1979; Browning and Gunning, 1979a,b,c; Caussin et a f . , 1983; Renault et al., 1989) that the sporophyte of bryophytes needs organic nutrients from the gametophyte for normal growth and development, although it contains chlorophyll and, notably in mosses and anthocerotes, may have well-organized photosynthetic tissues (Duckett and Renzaglia, 1988b). The same is presumably true for the embryos of pteridophytes, although no direct evidence is presently available (DeMaggio, 1963; Sheffield and Bell, 1987; Bell, 1989). The situation is more complex in seed plants, as here the reduced gametophyte grows and is fertilized within the parental sporophyte. The embryo is nourished by the gametophyte for a short time, thereafter it starts taking up nutrients directly from the old sporophyte. The dependence of the embryo on exogenously supplied nutrients is reflected by a series of morphological specializations that presumably serve to facilitate nutrient translocation. In bryophytes and most pteridophytes the embryo forms a basal or lateral organ, the foot, that penetrates the gametophyte tissue and is thought to be active in nutrient uptake. In addition, pteridophytes and seed plants possess a suspensor that orientates and keeps the embryo in intimate contact with the nutritive tissue of the gametophyte (Gifford and Foster, 1989). The suspensor is generally small and short-lived in pteridophytes. Conversely, the embryo of seed plants has a relatively large and long-lived suspensor but never forms a foot (Wardlaw, 1965; Gifford and Foster, 1989). At very early stages in development the
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
233
embryo of mosses and most liverworts forms a suspensor-like basal structure. Most frequently this consists of one or few cells and collapses with the subsequent development of the foot. The interface between the sporophyte foot and parental gametophyte in bryophytes and pteridophytes is commonly referred to as the placenta (Pate and Gunning, 1972; Gunning and Pate, 1974; Ligrone and Gambardella, 1988a,b). Generally placental cells have dense cytoplasm rich in mitochondria, endoplasmic reticulum and ribosomes. Most frequently they present a wall-membrane apparatus typical of transfer cells (Pate and Gunning, 1972; Gunning and Pate, 1974). A true placenta is lacking in seed plants, as the embryo does not form a foot, but transfer cells may be found in several different sites such as the interface between the gametophyte and its parental sporophyte, as well as in the suspensor, cotyledons, endosperm and integumentary endothelium (Gunning and Pate, 1969a, 1974; Pate and Gunning, 1972; Gunning, 1977). The formation of an embryo has been widely recognized as one of the most distinctive features of land plants, unknown in chlorophyll a bcontaining algae, with the possible exception of Coleochaete (Graham et al., 1991). Red algae are the only other group in which post-fertilization development may produce an intercalated multicellular diploid phase, the carposporophyte, that remains associated with the gametophyte by means of highly specialized placental structures (Bold and Wynne, 1985). There is no doubt, however, that red algae and land plants have but a very remote common ancestry and similarities in their life-cycles must be due to parallel evolution. The term embryophytes for land plants has therefore received increasing favour in the last years (Mishler and Churchill, 1984, 1985; Bremer, 1985; Crane, 1985; Bremer et al., 1987), although it is still debated whether, in a cladistic context, embryophytes may be considered a monophyletic group (Sluiman, 1985). The placenta has a critical role in the life-cycle of land plants as it connects and integrates two organisms subject to different environmental and genetic constraints. Regardless of whether the land plant sporophyte and its nutritional and developmental association with the gametophyte originated de novo, through a delay in zygotic meiosis (Bower, 1908), or secondarily from a free-living organism (Fritsch, 1945), one of the very first steps must have been the evolution of a placental tissue. Since then the placenta has been evolving over millions of years under the selective pressures that have produced all the extant, and extinct, groups of land plants. This review presents a comparative analysis of the placenta in land plants, including the first detailed systematic survey of bryophytes encompassing several groups not studied before, together with comments on pteridophytes, where comparative data are virtually non-existent, and on placental analogues in seed plants. Far from exhaustive, this is primarily an attempt to
+
234
R. LIGRONE
et a1
draw the attention of plant morphologists, physiologists and taxonomists to a topic of considerable relevance to the phylogeny, taxonomy and functional biology of land plants.
11.
BRYOPHYTES
The bryophytes present a particularly conspicuous placental region, probably as a consequence of the inability of their sporophyte to become autonomous. The nutrient relationships of the two generations have been reviewed recently (Ligrone and Gambardella, 1988a) and will not be discussed in detail here. Ultrastructural studies performed in recent years have revealed remarkable diversity in the organization of the placenta (Ligrone and Gambardella, 1988b). Unfortunately, the paucity of comparative data and in particular a complete absence of information for several major groups, notably the Andreaeidae and Tetraphidales among the mosses and the Jungermanniales and Metzgeriales among the liverworts, have hitherto prevented any wide-ranging conclusions. The most clear-cut feature that distinguishes the sporophytegametophyte junction in different bryophyte groups is the presence or absence of wall labyrinths in the placental cells of each generation (Tables I, I11 and V). Further distinctive attributes are the cell wall structure, notably the shape and arrangement of wall ingrowths, and certain cytoplasmic features of placental cells such as plastid morphology (Tables 11, IV and VI). Some of these characteristics may undergo changes during sporophyte development. For example, in mature sporophytes the wall labyrinth of placental transfer cells is partially or completely obliterated by deposition of new wall material (Browning and Gunning, 1979a; Gambardella, 1987; Gambardella and Ligrone, 1987). It is therefore important that different developmental stages be examined and corresponding stages be considered when comparing different species or groups. This is not an easy task; the sporophytes develop at different times of the year, according to the species, and in liverworts the phase of active sporophyte growth is usually very short. Moreover, attempts to obtain sporophytes under laboratory conditions have been successful only in a very limited number of species. In this account two main stages of sporophyte development are distinguished. Stage 1, pre-meiotic, is characterized by proliferative activity in the sporangial tissue. Stage 2, post-meiotic, is characterized by the presence of maturing spores in the still intact sporangium. The highest demand for exogenous nutrients by the sporophyte, presumably associated with maximum activity of the placenta, has been observed during the first stage of development (Proctor, 1977; Browning and Gunning, 1979b). When not otherwise indicated, the ultrastructural observations reported here refer to that stage. The new information presented in this review encompasses 17 species of mosses, 26 of liverworts and 9 of anthocerotes, with representatives from all the major orders of bryophytes (Tables I-VI).
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
235
Nomenclature for genera and species follows Corley et a f .(1981) for mosses, Grolle (1983) for liverworts, and Stotler and Crandall-Stotler (1977) or Hasegawa (1988) for anthocerotes. A. MOSSES (Bryopsida)
The first division of the zygote within the archegonium is transverse and produces an upper, epibasal cell and a lower, hypobasal cell. According to Roth (1969), in all mosses, except Sphagnum, the epibasal cell generates an elongate flattened embryo with a lenticular apical cell, whereas the hypobasal cell undergoes a few randomly orientated divisions producing a small mass of cells. Subsequently the embryo forms an intercalary meristem which is responsible for the development basipetally of the foot and the lowermost part of the seta, whereas cells differentiating acropetally from the meristem produce the upper seta and the capsule base (Crandall-Stotler, 1984). In Sphagnum the embryo does not form an intercalary meristem. As a consequence, the seta is lacking and the foot is entirely derived from the activity of the hypobasal cell (Roth, 1969). In some bryalean genera, e.g. Archidium and Ephemerum (Crandall-Stotler, 1984), the seta meristem is functional for only a few division cycles and consequently a very small foot and short seta are developed. In most cases the hypobasally derived cells usually degenerate at an early stage of sporophyte development and either disappear or in a few moss genera (Table I) form a small necrotic appendage visible at the tip of the foot (Roth, 1969; HCbant, 1975; Ligrone and Gambardella, 1988a). 1 . Andreaeidae This subclass consists of the genus Andreaea, with 50 to 100 species (Schultze-Motel, 1970), and the recently described genus Andreaeobryum, represented by the single species A . macrosporum (Steere and Murray, 1976; Murray, 1988). Anatomical characteristics of recently discovered antheridia and sporophytes of Takakia (Davison et a f . , 1989; Mcfarland et a f . , 1989; Smith, 1990) indicate that this is a primitive moss with clear relationships with the Andreaeidae, rather than a liverwort. For this reason the placental organization of Takakia is discussed in this section. The sporophyte of Andreaea consists of a capsule, a very short seta and a conical foot (Fig. 1). After fertilization the archegonial stalk proliferates to form a parenchymatous tissue surrounding the foot. Following spore maturation the sporophyte is elevated by a pseudopodium, formed by elongation of archegonial and stem cells (Roth, 1969; Murray, 1988). The foot has a parenchymatous structure, with no trace of conducting tissue. The internal cells contain abundant lipid reserves in the form of osmiophilic droplets of varying size (Fig. 2 ) . The epidermal cells are slightly larger and have denser cytoplasm with numerous evenly scattered vacuoles of small sizes (Fig. 3). In the lower part of the foot the epidermal cells exhibit prominent wall labyrinths along their outer tangential walls (Fig. 3).
TABLE I Characteristic features of the placenta in mosses Distribution of transfer cells
Distribution of wall ingrowths
Reference' Sporophyte Gametophyte
ANDREAEIDAE Tolioloo rcrorophyllo Andreoco rupmrrk Hedw Andreoeo rorhii Web. & Mohr Andreuobryum marrosponm Sleeve & B. Murr. SPHAGNmAE Sphagnumfmbnarum Wik. Sphagnum fdlaKlinggr. Sphagnum subnitow Rws & warnst. Sphagnum curprdotum Ehrh.
Sporophyte
Gametophpe
Time of ingmwih development
lngrowth morphology
Sporophyte Gametophyte Sporophytc Gametophyte Conducting Foot shape tissue in
16
+
1
+
1 15
11 11
+ +
NIA
Early
NIA
Single layer outer tang.
NIA
Early
NIA
NIA
Early
N/A
NIA
NIA
NIA
NIA
Early
NIA
walls
Smgle layer 0"ter tang. walls
Labyrinth. NIA Labynnth. coarse NIA
}
fwt
Hydroids
-
coarse
?
NIA
7
i"P
NIA
Sporophyte
Slightly elongate
Gametophyte
l h c k . nameous
+ thin areas with plasmodesmara
Thick
7
Tlick and thin
areas with plasmodesmata
~
BRYIDAE Polytrichales Polyrnchum formmum Hedw. Polynchum commune Hedw Polynrchum pil$e..n Hedw Dowoni? superb0 Grev. Dendroltgornchumdcndrordrs
13 13 14
+
+ +
outer tang walls
2-3 inner cell layen
Broth. Pogonoaun dordes P.Beauv Pqonomm neesii (C.MuU.)
10 I
Dozy Olrgontchum hercrnicum Lam.
1
+ + + + +
Atrichurn undulorum P.
1
+
1
+
Outer tang. walls 4
Single layer outer tang
&Dc
Beau".
Tetraphidales
TeonphLs pellucidn Hedw
7 7
Labynnth, NIA coarse
Hydroids. leptoidr
Elongate
tapertog
cells
Single layer thick-
walled cells
loner tang walls
Labyrinth. Shon. coarse Hydroidr
Elongate tapering
Early
Labynnth
Early
Labyrmth
Elongate tapenng
Early
Early
Early Early
maw
Bryales
Bmbaumiinsae
BuxboumiapzpenBest
12
+
Diphwrumfoliorum Mohr.
1
I
Single layer thckwalled cells
Several layem thick-walled
lateral in middle
Walk
Inner tang. walls t outer cell layers
less
eXte"Sl"e
Labyrinth, fine Labyrinth. coarse
Hydroids
Elongate parenchyma
Collapsed
cells at
foot up
Elongate
~
1
1
I
s,ngle layer O"k* 1ang.b walls
Other wall features
Archidiiicae rmerrimm Min.
Archi&--
2
+
+
1
+
+
1
+
1
+
1
outer tang. walls.
Inner tang walls
Single layer cuter tang. Walls
lnncr tang walls t outer aU layers
Early
-
single layer outer tang.
NIA
Ealy
+
Single layer outer tang.
Inner tang. walls + outer cell layers
Earl?
+
+
Single layer OUter tang
Inner tang. walls + 0"kr cell lavers
Early
1
+
f
Single layer O U t a tang
Inner tang. walls + 0)utercell layers
Early
I2
+
+
Single layer outer tang
inner rang. walls f outer cell layers
Early
4
i
+
Single layer outer tang
Inner tang. W a l k + outer cell layers
Early
Outer tang. walls t Inner cells layers Outer tang. walk inner cell layers
Inner tang walls
Early
Inner tang. walls
Early
Single layer uuter Img
Inner tang. W d I * + ""tcrlrrll layers
Fsrl)
Single laycr outer tanp walls
Inner Idag Wdll. +
Early
Smgic laycr outcr tang.
waur Slnglc layer OUlCT tanp.
Inner 1img. Willlb + OuterlwU b y m Inner t ~ g wila .
rjrly
Slnglc layer outer lung. w . 1
lnncr tang. walls I ""trr ccu lilyerr
Early
lnncr tang walk I
Earl)
Dicranineae
Laxobryum glnucum Angstr.
W&
waus
walls
waus
waus
W2.b
17
t
f
9
+
+
5. x
t
4
10
I
I
1
+
wall.
+
1
h
t
I
+
I
I
10
t
+ +
walls
BUlbOUS
""tcrccll lnycrr
+
outcrccll layerr
€ally
f
Labyrinlh. hbyrinth
murc
Hvnnincnc
.
.-
long.
.
""1crICcII 1aycrr
10
"References. I , DEW; 2, Brown and L e m o n (1985); 3, Browningand Gunning (1979a); 4, Chauhan (1990); 5. Chauhan and Lal (lWgl), 6. Ejm6 and Suirc (lW7): 7. HCbant (19751.8.La1 and Chauhan (1981):9. La1 and Narang (1985); 10, Ligrone and Cambardella (19a8a); 11. Ligrane and Renzaglia (1989);12. Ligrone el d.(1982b); 13. Maier (1%7): Maier and Maicr (1972); 15. Murray 11988); 16. Remagha d nl (1991);17. WrncLe and %hulr (1975). btang = tangential.
TABLE I1 Cytoplasmic features of the nlacental cells in mosses Plastids Sporophyte Shape ANDREAEIDAE Takakia cerarophylla Andreaea rupestris Andreaea rothii Andreaeobryum macrosporum
[
?
SPHAGNIDAE Sphagnum fimbriatum Sphagnum fallax Sphagnum subnirens
Sphagnum curpidatum
Elongate Ovoid
Membrane system
{
?
Pleomorphic p.r
Plastoglohuli Starch
++
1.g.
r.gr.
Gametophyte
{
++ ? +
I
{
-
{
11 -
Shape
Membrane system
Pleomorphic
r.gr.
Ovoid
r.gr.
{
?
?
?
-
Ovoid
n.gr.
Ovoid
n.gr. p.r.
Cytoplasmic lipid droplets
Plastoglobuli
Starch
+++
++
?
{
-I ?
Sporophyte
Gametophyte
++
+ ++
++ ?
{
+I -1
BRYIDAE
?
-
I
Polytrichales Polyrrichum formosum Polyrrichum commune Polyrrichum piliferum Dowsonia superba Dendroligotrichum dendroides Pogonarum aloides Pogonafum neesii Oligorrichum hercinicum Atrichum undulatum
Pleomorphic r.gr. p.r.
Tetraphidalcs Tetraphis pellucida
Ovoid
Bryales Buxbaumiincae Buxbaumia piperi Diphyscium foliosum
Pleomorphic p.1. Pleomorphic m.gr.
+
-
-
I Plcomorphi
+
+I-
++
+I+]
?
++
+
Ovoid
n.gr.
+ + -
-
Pleomorphic
r.gr.
t
-
Sphcroidal Spheroidal
pr0.b. Irregular
-
+
~
+
-
+
+
-
Archidiineae Archidium tenerrimiim
Pleomorphic
m.gr.
+
-
Spheroidal
r.gr.
Dicranineae Leucohryum glaucum Dicranum majus Blindia acura Cladophascum gymnomitrioides
Pleomorphic Pleomorphic Pleomorphic Pleomorphic
p.r. m.gr. m.gr. m.gr.
+
-
Spheroidal Spheroidal Spheroidal Spheroidal
r.gr.
-
r.gr. n.gr. r.gr.
-
Fissidentineae Fissidens crassipes
Pleomorphic
r.gr.+ p.r.
Pleomorphic
n.gr.
+
Pottiineae Timmiella harhuloides Phascum cuspidarum
Pleomorphic Pleomorphic
m.gr. r.gr.
+ +
-
Spheroidal Spheroidal
r.gr. r.gr.
Pleomorphic
n.gr. +p.r.
+
-
Pleomorphic
r.gr.
Funariineae Funaria hygromerrica Physcomifriumcoorgense Physcomirrium cyathicarpurn
1
Pleomorphij n.gr.
Bryincae Bryum capillore
Pleomorphic
Aulacomniurn palusrre Plagiomnium cuspidaturn Mnium hornurn
Ovoid Pleomorphic Pleomorphic
r.gr. + p.r. m.gr. m.gr. m.gr.
Leucodontineae Neckera crispa
Pleomorphic
p.r.
Hypnincae Brachvfhecium vehtinum Isopterygium pulchellutn
Pleomorphic Pleomorphic
p.r.
p.r.
+ -
+
}
+
1
+
}
Pleomorphicl r.gr.
-
-
+
}
+ +
++ + + +
+ + + +
+ + +
+
-
+
+
+ -
+
-
-
-
-
1 1
+
}
+
-
-
Spheroidal
r.gr.
-
+
+
-
Pleomorphic Plcomorphic Spheroidal
r.gr.
n.gr.
+ + +
+ + ++
Spheroidal
r.gr.
+
+
-
-
Spheroidal Spheroidal Elongate
r.gr. r.gr.
+
+
+ +
-
-
-
+
-
-
-
-
r.gr.+ p.r.
+
+
Abbreviations: m.gr., massive grana; n.gr., normal grana, like those in leaves; r.gr., rudimentary grana, 2-3 thylakoids only; pro.b., prolamellar body; p.r.. peripheral reticulum.
240
R. LIGRONE et a/.
Figs. 1-4. The gametophyte-sporophyte junction in Andreaea rothii. Fig. 1. Light micrograph, longitudinal section, showing the conical foot and the absence of conducting tissues in the short seta. Fig. 2. The foot parenchyma cells contain abundant lipid droplets. Fig. 3. Wall labyrinths along the outer tangential walls of sporophyte placental cells. Fig. 4. Gametophyte placental cells with irregular wall thickenings (arrowed). Key to abbreviations used on figures: F, foot; G , gametophyte; H , hydroids; M, mitochondria; N, nucleus; P, plastids; S, sporophyte; SE, seta.
The gametophytic cells surrounding the foot also have dense cytoplasm rich in organelles, notably mitochondria. As in all the other mosses examined in this study, these tend to be larger than those in the foot cells. The gametophyte placental cells do not form wall ingrowths but present thickened wall areas with a loose fibrillar texture, interrupted by thinner areas crossed by plasmodesmata (Fig. 4).
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
24 1
Both sporophyte and gametophyte placental cells contain numerous small plastids with a rudimentary thylakoid system and are rich in plastoglobuli. Ultrastructural details of the placenta in Andreaeobryum have yet to be described. However, major morphological differences between Andreaea and Andreaeobryurn include the presence in the latter of a well-developed seta and a “bryoid” foot deeply penetrating the gametophyte tissue, which does not form a pseudopodium (Murray, 1988). Placental transfer cells are restricted to the sporophyte (Murray, 1988). The foot of Takakia is closely similar to that of Andreaeobryum (Renzaglia et al., 1992). This elongated tapering structure (Fig. 5 ) penetrates deeply into the broadened central conducting strand of the gametophyte stem. The inner foot region comprises a broad strand of hydroids extending lengthwise in the seta, but leptoids are absent. The epidermal cells of the foot exhibit well-developed wall ingrowths on their outer tangential walls (Fig. 6). Their dense cytoplasm contains abundant mitochondria, lipid droplets and elongated plastids with rudimentary grana and numerous plastoglobuli (Fig. 6). Starch grains are absent from the sporophyte placental cells but are common in the adjacent tissues, especially the cortex of the foot and gametophyte. Transfer cells are absent in the gametophyte placental cells. These have irregularly thickened walls lined with conspicuous deposits of electron-transparent material (Fig. 7).
2. Sphagnidae This subclass consists of the single genus Sphagnum, with 100 species. The sporophyte of Sphagnum lacks a distinct seta and develops at the apex of specialized gametophytic branches that elongate after spore maturation to form a pseudopodium (Roth, 1969). The foot is bulbous and parenchymatous (Fig. 8). An ultrastructural investigation of the placenta of Sphagnum jimbriatum and S . fallax at stage 2 of sporophyte development revealed that transfer cells were lacking in both the sporophyte and gametophyte (Ligrone and Renzaglia, 1989). This finding has been confirmed in S . subnitens and S . cuspidaturn at stage 1 of sporophyte development. The placental organization is almost identical in the four species. The sporophytic placental cells protrude from the bottom of the foot into a large, mucilage-containing space that separates the two generations (Fig. 8). These cells differ from the internal parenchyma cells of the foot, having denser cytoplasm and relatively small vacuoles (Fig. 9). Moreover, they apparently contain a vast number of plastids of very small sizes and irregular shape with few or no thylakoids, numerous plastoglobules and abundant peripheral reticulum (Fig. 10). These plastids are often aggregated in groups and presumably are sectional profiles of larger, extremely pleomorphic plastids. The nucleus generally lies in a central position and may have an irregular shape. The cells walls, relatively thin and uniform, have a compact fibrillar texture (Fig. 9).
242
R. LIGRONE
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T H E GAMETOPHYTE-SPOROPHYTE JUNCTION
243
On the opposite side of the placenta are several layers of small gametophytic cells (Fig. 13). These have large vacuoles and dense cytoplasm mostly gathered at the periphery and rich in mitochondria, dictyosomes and sheets of rough endoplasmic reticulum (Fig. 11). The plastids are larger and less numerous than their sporophytic counterparts, and generally exhibit well-developed grana (Fig. 12). The gametophyte placental cells characteristically have thickened walls with a loose fibrillar texture, interrupted by pits with a high frequency of plasmodesmata (Fig. 14). In S. fimbriatum these thickened walls contain distinctive tubular structures arranged radially (Ligrone and Renzaglia, 1989). The gametophytic placental tissue contains abundant intercellular spaces that are continuous with the larger placental space. As the sporophyte matures the gametophyte cells closer to the foot degenerate (Fig. 13). Starch is generally lacking in both the sporophyte and gametophyte placental cells, whereas it is abundant in the adjoining parenchyma cells of both generations.
3. Bryidae This subclass includes all peristomate mosses and is divided into two groups: the nematodontous mosses, with peristome teeth composed of whole cells; and the arthrodontous mosses, with peristome teeth composed, primarily or exclusively, of articulated and fused cell plates (Edwards, 1984; Vitt, 1984). The former group traditionally includes the orders Polytrichales and Tetraphidales, whereas the latter includes all the most advanced mosses, classified in the single order Bryales by Vitt (1984) or in several orders by others (cf. Smith, 1978; Miller, 1979; Crosby, 1980; Corley et al., 1981). Typically in the Bryidae the sporophyte foot is highly elongate, conical in shape and penetrates the gametophyte stem tissue. It is partially or completely surrounded by the vaginula, a multilayered parenchymatous sheath derived from the proliferation of archegonial cells and the underlying stem tissue (Roth, 1969). Further details of the ultrastructure of the vaginula are given in Ligrone and Gambardella (1988a). In acrocarpous mosses the sporophyte develops at the apex of the gametophyte stem, which ceases growing since apical growth terminates in the production of archegonia. In pleurocarpous mosses the sporophyte
Figs. 5 7 . The gametophyte-sporophyte junction in Takakia ceratophylla. Fig. 5. Light micrograph, longitudinal section, showing the elongate foot with a central strand of hydroids. Fig. 6. Sporophyte placenta cell showing the wall labyrinth along the outer tangential wall and elongate plastids. Fig. 7. Gametophyte placental cell with electron-transparent inner wall material (arrowed). Figs. %lo. The gametophyte-sporophyte junction in Sphagnum cuspidaturn. Fig. 8. Light micrograph, longitudinal section, showing the bulbous foot at the apex of the pseudopodium (PS). Fig. 9. Sporophyte placental cell with thin walls, numerous vacuoles and small plastids and mitochondria. Fig. 10. Pleomorphic undifferentiated plastids in a sporophyte placental cell.
244
R. LIGRONE et al.
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
245
develops at the apex of short lateral branches, and the main stem grows indefinitely. In some groups, e.g. the Polytrichales, the gametophyte is acrocarpous, but the old sporophytes may be displaced laterally due to subsequent innovative growth of new shoots. Frequently in acrocarpous mosses the foot tip penetrates the gametophyte central strand. This is due to intrusive growth of the foot and parallel sporophyte-induced proliferation and differentiation of the gametophytic tissue (Roth, 1969). Penetration of the central strand by the foot, however, seems to have no taxonomical significance as differences are found even within the same genus (Roth, 1969). The foot of Bryidae has the same histological organization as the seta. When the seta contains a central strand of conducting tissue (Hebant, 1977), this is also present in the foot. The lower part of the foot, however, differs from the seta in lacking a peripheral sterome and in the presence of highly specialized epidermal cells. In the Polytrichales the conducting strand contains both hydroids and leptoids, the latter being simpler in structure than in the gametophyte (HCbant, 1977,1979). Leptoids have also been reported in the foot of Funaria (Wiencke and Schulz, 1975), but generally they seem to be lacking in Bryales (Hebant, 1977, 1979). The foot (and seta) of many groups in the Bryales lacks a central strand of conducting cells, most likely as a consequence of reduction (Crosby, 1980; Schofield, 1985). In several acrocarpous genera, e.g. Polytrichum, Bryum, Funaria and Encalypta, apoplastic continuity between the central strands of the gametophyte and sporophyte may result from the degeneration of foot-tip cells (Roth, 1969; Hebant, 1975; Ligrone and Gambardella, 1988a).
3. Polytrichales The order Polytrichales comprises 20 genera and about 300 species placed by Smith (1971) in the single family Polytrichaceae. Representatives of seven genera have been examined ultrastructurally (Table I). The polytrichaceous mosses have a typical bryoid foot of elongate conical shape that penetrates the gametophyte stem tissue to a considerable depth. A conspicuous central strand of conducting tissue is present in both the gametophyte and sporophyte. As in the seta (Htbant, 1977), a system of intercellular spaces is present in the foot parenchyma (Ligrone and Gambardella, 1988a).
Figs. 11-14. The gametophyte-sporophyte junction in Sphagnum cuspidatum (cont.). Fig. 11. Gametophyte placental cell with characteristic wall thickenings. Fig. 12. Sporophyte placental cell; plastid with well-differentiated grana. Fig. 13. Longitudinal section through the gametophyte placental cells. Note the large intercellular spaces and the degenerating cells nearer the foot (top, arrowed). Fig. 14. Gametophyte placental cell; pitted region of the wall containing numerous plasmodesmata.
246
R. LIGRONE et al.
Figs. 15 and 16. The gametophyte-sporophyte junction in Polytrichales. Fig. 15. Atrichum
undulatum; showing the sporophyte wall labyrinth and thickened tangential walls in the
gametophyte placental cells. Fig. 16. Pogonatum neesii; gametophyte placental cells with greatly thickened walls.
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
247
The placental organization is substantially similar to that in Andreaea, with transfer cells in the foot only. The most prominent wall labyrinths are found in the epidermal cells but a wall-membrane apparatus typical of transfer cells may also be present in the two to three outermost layers of parenchyma cells (Fig. 17). The epidermal transfer cells have dense cytoplasm with numerous mitochondria and abundant endoplasmic reticulum (Fig. 15). The plastids are small, lack starch and have a central rudimentary thylakoid system, surrounded by conspicuous peripheral reticulum (Figs. 18and 19). The internal transfer cells tend to be more vacuolate and with less dense cytoplasm (Fig. 17). Several layers of specialized gametophyte cells surround the foot in Pogonatum and Oligotrichum, whereas a single layer is present in Atrichum (Fig. 15) and Polytrichum. The gametophyte placental cells have thickened walls with irregular outlines but never form a wall labyrinth. Cell wall thickening is most pronounced in Pogonatum (Fig. 16), with a consequent strong reduction of the cell lumen. A similar situation occurs in Oligotrichum. Only the inner tangential walls of the gametophyte placental cells become thickened in Atrichum (Fig. 15), whereas in Polytrichum thickwalled cells with dense cytoplasm are intermingled with larger thin-walled cells with prominent stacks of endoplasmic reticulum. Typically, the gametophyte placental cells have dense cytoplasm with small vacuoles and abundant endoplasmic reticulum. Their plastids may have a more highly organized thylakoid system and less peripheral reticulum than their sporophytic counterparts, but, unlike those in the vaginula, they contain little or no starch. The gametophyte cells closer to the foot often undergo cytoplasmic degeneration. Like Andreaea, the polytrichaceous mosses accumulate abundant lipid reserves in both the placental cells and adjoining parenchyma cells. 4. Tetraphidales The order Tetraphidales consists of two (Crosby, 1980) or three genera (Vitt, 1984), each with three o r four species. Only one of these, Tetraphis pellucida, has been examined ultrastructurally . The foot penetrates the gametophyte central strand and has a central strand of hydroids surrounded by elongate parenchyma cells, whereas leptoids are absent (Figs. 20 and 21). A well-developed wall labyrinth is present in the epidermal cells from very early stages in sporophyte development. In the lower part of the foot the epidermal cells are highly vacuolate and the bulk of the cytoplasm lies adjacent to the labyrinthine walls, whereas in the middle of the foot the epidermal cells contain very small vacuoles and most of their lumen is occupied by dense cytoplasm rich in mitochondria1 lipid droplets (Fig. 23) and chloroplasts with highly organized grana (Fig. 24). O n the opposite side of the placenta are gametophyte cells with thickened
248
R. LIGRONE et al.
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
249
walls that may form large and coarse protuberances (Fig. 22). Conspicuous wall labyrinths are occasionally found on the lateral walls of the gametophyte cells adjoining the middle portion of the foot. The plastids in the gametophyte placental cells are of smaller and more irregular shape than those in the sporophyte. Their inner membrane system is rudimentary and small amounts of starch are sometimes present. Starch and lipid reserves are much more abundant in the adjoining cells of the vaginula. 5. Bryales Divided by Vitt (1984) into 15 suborders, 85 families and 765 genera, this is the largest and most diverse group of mosses. In sharp contrast to an extreme variability in the gametophyte and sporophyte morphology, the placental organization is remarkably uniform. Twenty species, belonging to nine different suborders, have been examined ultrastructurally (Table I), and several others have been examined by light microscopy only (see Roth, 1969, for a comprehensive review). All of these, with the exception of Dicranum (Fig. 25), exhibit transfer cells on both sides of the placenta (Figs. 26, 27, 31, 32 and 34). Labyrinthine walls are generally restricted to the single layer of epidermal cells in the foot and the adjoining layer of gametophyte cells, but isolated wall ingrowths are also frequent in gametophyte cells farther from the foot. Several layers of well differentiated transfer cells have been reported in the gametophyte placenta of Buxbaumia piperi (Ligrone et al., 1982a). In most cases the foot has a regular outline and is separated from the gametophyte by a placental space containing residues of collapsed cells of gametophytic origin (Fig. 25) and sometimes calcium oxalate crystals (Fig. 27). In some instances, however, interpenetration of the sporophyte and gametophyte placental tissue may increase the contact area between the two generations. For example, the elongate epidermal cells of Bryum are wedged among the adjoining gametophyte cells (Ligrone and Gambardella, 1988a), and in Diphyscium the foot is covered with multicellular tubular outgrowths that deeply penetrate the adjoining gametophyte tissue (Figs. 28-30). In general the wall labyrinths are equally well developed in both generations (Figs. 26 and 27) but sometimes are more elaborate in the sporophyte (e.g. Mnium, Aulacomnium, Fissidens) (Figs. 32 and 34). The opposite situation accrues in Diphyscium (Fig. 31). The wall ingrowths in Figs. 17-19. The gametophyte-sporophyte junction in Polytrichales (cont.). Fig. 17. Polytrichum formosum; several layers of sporophyte transfer cells. Fig. 18. Pogonatuni aloides; sporophyte placental cell plastids. Fig. 19. Oligotrichurn hercynicum; sporophyte placental cell plastid. Figs. 20 and 21, Light micrographs of the garnetophyte-sporophyte junction in Tetraphis pellucida. Fig. 20. Transverse section. Fig. 21. Longitudinal section.
250
R. LIGRONE ei al.
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
251
the placental cells of the Bryales are thinner, longer and more convoluted than in the other orders of Bryidae (Fig. 33) and presumably this results in a proportional increase of the surface extension of the wall-membrane apparatus. In Funaria the wall labyrinths develop at a very early stage of sporophyte development, reaching the maximum extension well before capsule differentiation (Wiencke and Schulz, 1978; Browning and Gunning, 1979a). The same has been observed in several other species, such as Mnium hornum (Fig. 33), Brachythecium vefutinum and Fissidens crassipes (Fig. 34). As in the other orders of mosses, the placental cells in Bryales have dense cytoplasm rich in mitochondria and generally are not highly vacuolate. The presence of numerous vacuoles of small sizes instead of large vacuoles may protect the placental tissue against water stress (Oliver and Bewley, 1984), an eventuality that might be particularly prejudicial to sporophyte development. Plastids are somewhat variable in structure, although they are generally much less differentiated compared to those in other tissues (Duckett and Renzaglia, 1988b). A relatively well-developed inner membrane system has been observed in the plastids of sporophyte placental cells of Funaria (Browning and Gunning, 1979a), Physcomitrium (La1 and Chauhan, 1981) and Archidium (Brown and Lemmon, 1985). Massive granal stacks with few or no stroma thylakoids have been found in Timmieffa (Ligrone et a f . , 1982b), Mniurn (Fig. 35), Dicranum (Fig. 37), Cfadophascumand Diphysciurn. Highly pleomorphic plastids with abundant peripheral reticulum closely similar to the saccate mitochondria1 cristae in the same cells, and few or no thylakoids occur in the sporophyte placental cells of Bryum (Fig. 36; Ligrone and Gambardella, 1988a), Buxbaumia (Ligrone et a f . , 1982a), Fissidens and Brachythecium (Ligrone and Gambardella, 1988a). Plastids in gametophyte placental cells are either larger o r smaller than those in the sporophyte and almost always contain starch (Figs. 38-41), whereas this is much less frequent in the sporophytic counterparts (Figs. 35-37). The range in the ultrastructural characteristics of these plastids is illustrated in Figs. 38-41. Shape varies from spheroidal in Cfadophascum (Fig. 38), Diphyscium (Fig. 39) and Bfindia (Fig. 41) to pleomorphic in Fissidens. The thylakoid system is also variable, appearing as irregular arrays of membranes in Diphyscium (Fig. 39), small grana in Cfadophascum (Fig. 38) and large stacks in Bfindia (Fig. 40). The parenchyma cells of the vaginula almost invariably contain large amyloplasts and often also abundant lipid reserves. This feature is most Figs. 22-24. The gametophyte-sporophyte junction in Tetruphispellucidu (cont.). Fig. 22. Gametophyte placental cells with large, coarse wall protuberances (mowed). Fig. 23. Midregion of foot; wall labyrinth o n the outer walls. Fig. 24. Chloroplast in a sporophyte placental cell.
252
R. LIGRONE et al.
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
253
pronounced in the vaginula cells of Diphyscium, which are comparable to endosperm cells of seed plants in the abundance of their reserve materials (Fig. 40). Starch is also abundant in the parenchyma cells of the foot. These cells are highly elongated longitudinally and present high concentrations of plasmodesmata in the cross walls. This may reflect a functional specialization in the acropetal transport of nutrients toward the sporangium. B. LIVERWORTS (Hepatopsida)
As in mosses, in all liverworts, except the Monocleales (Campbell, 1954a; K. S. Renzaglia, unpublished data) the first division of the zygote is transverse and produces a small epibasal and a large hypobasal cell.The destiny of these two cells appears to vary widely. However, the available information about early stages in embryogeny is far from conclusive in as much as original descriptions are relatively few and sometimes conflicting. It is generally agreed that in the Jungermanniales the second division occurs in the epibasal cell and produces a three-celled embryo (Smith, 1955; Schertler, 1979; Crandall-Stotler and Geissler, 1983; Schuster, 1984a). Of the two epibasally derived cells, the outermost one is the capsule initial whereas the other will form the seta and foot. The hypobasal cell undergoes few or no further divisions, forms a filament, referred to as the huustorium, and penetrates the underlying gametophyte tissue. The function of this structure seems to be confined to very early stages in sporophyte development, after which the foot becomes the primary absorptive organ and the haustorium generally becomes indistinct (Schuster, 1984a). In the Metzgeriales, as in the Jungermanniales, the hypobasal cell forms only a haustorial appendage and the foot has a epibasal origin (Clapp, 1912; McCormick, 1914; Campbell, 1916; Showalter, 1926, 1927a,b; Haupt, 1929b; Smith, 1955; Crandall-Stotler, 1981; Schuster, 1984a). The information available on embryogeny in the Calobryales is particularly poor and inconclusive. Early studies by Goebel (1891) and Campbell (1920) report embryo development in Cufobryumbfumei to follow the same pre-determination pattern as in the Jungermanniales and Metzgeriales, with the hypobasal cell producing a haustorium and the epibasal cell giving rise to the sporophyte proper. This type of embryogeny is currently referred to as typical of the whole group (Smith, 1955; Crandall-Stotler, 1981; Schuster, 1984a). Nevertheless, more recent accounts of early embryogeny in Hupfomitrium gibbsiue Steph. (Campbell, 1954b) and Cafobrymindicurn Udar et Figs. 25-27. Bryalean plancentas. Fig. 25. Dicranum majus; the gametophyte cells are thin-walled and lack wall ingrowths. Note the collapsed cells in the intraplacental space (arrowed). Fig. 26. Leucobryum gluucum; extensive wall labyrinths in the placental cells of both generations. Fig. 27. Cladophascum gymnomitrioides; calcium oxalate crystals in the intraplacental space (arrowed).
254
R. LIGRONE et al.
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
255
Chandra (Mehra and Kumar, 1990) have reported a “quadrant stage” much like that in Marchantiales (see below). Moreover, according to these descriptions, no haustorium is formed, and since the cellular divisions following the first one are irregular there is no clear-cut distinction between epi- and hypo-basally derived parts of the embryo. Mehra and Kumar (1990) suggest that in the Calobryales, as in Marchantiales (see below), a filamentous and a quadrant type of early embryogeny may co-exist. In the Sphaerocarpales both the epibasal and hypobasal cell divide transversely. This results in a four-celled filamentous embryo in which each cell, by two successive vertical divisions, produces a tier of four cells (Smith, 1955). Two different patterns of embryo development, sometimes present in closely related taxa or even within the same genus, are recognized in the Marchantiales. In several genera, including Targionia (O’Keefe, 1915), Conocephalutn (Meyer, 1929), Reboulia (Dupler, 1922), Grimaldia (Meyer, 1931), Asterella (Haupt. 1929a) and Marchesta (=Neohodsgonia H. Pears.) (Campbell, 1954c), the zygote forms a four-celled filamentous embryo as in the Sphaerocarpales. In other genera, such as Corsinia (Meyer, 1912, 1914), Marchantia (McNaught, 1929) and Preissia (Haupt, 1926), the two daughter cells arising from the zygote divide by successive vertical walls, at right angles to each other, forming a “quadrant” type of embryo. No distinct haustorium is developed. The same is observed in Riccia, where most species have a quadrant type of embryo, but in certain species a four-celled embryo of the filamentous type is formed. In any case a seta and foot are lacking in this genus and all the cells of the embryo participate in the formation of a globose capsule that remains enclosed within the gametophyte tissue (Lewis, 1906; Pagan, 1932; Smith, 1955). The origin of the different parts of the mature sporophyte in the Sphaerocarpales and Marchantiales cannot be related with certainty, particularly in the filamentous type of embryo, to the epibasal or hypobasal cell, although a hypobasal origin of the foot and seta is often assumed (Campbell, 1954a; Smith, 1955; Schuster, 1984a). An alternative interpretation of embryogeny in these groups may be neotenic suppression of the hypobasal cell, implying that the first transverse division of the zygote is equivalent to the first transverse division of the epibasal cell in the other groups. This hypothesis may account for the lack of a haustorium in Sphaerocarpales, Marchantiales and Calobryales while maintaining a unitary basic pattern of early embryogeny in the whole of mosses and liverworts. Monoclea is apparently unique in the liverworts as, according to Campbell (1954a) and recently confirmed (K. S. Renzaglia, unpublished data), the Figs. 28-32. Bryalean placentas (cont.). Figs. 28-30. Light micrographs; longitudinal sections of the gametophyte-sporophyte junction in Diphysciurn foliosum. The massive foot is covered with multicellular tubular outgrowths. Fig. 31. Longitudinal section of the placenta of Diphysciurn. Wall ingrowths are more highly developed in the gametophyte cells. Fig. 32. Mniurn hornunz: wall ingrowths are more elaborate in the sporophyte.
256
R. LIGRONE
el
al.
T H E GAMETOPHYTE-SPOROPHYTE JUNCTION
257
zygote undergoes free nuclear divisions to the 26-nucleate stage, after which partitioning produces a globose embryo. This description, however, contrasts with the illustration by Cavers (191 1) of a two-celled embryo followed by a quadrant stage, as well as with a description by Johnson (1904) of embryo development in Monoclea forsteri Hook. As in mosses, fertilization causes extensive proliferation in the gametophytic tissue underlying the embryo. The archegonial cells form a calyptra that surrounds the sporophyte until spore maturation. Additional protective structures are perianths or pseudoperianths, stem-derived structures such as perigynia, coelocaules and marsupia, or simple outgrowths of the thallus (Schuster, 1966, 1984a). In various Jungermanniales and Metzgeriales the receptacle tissue below fertilized archegonia contributes to the formation of the calyptra, that is therefore referred to as stem- or shoot-calyptra (Schuster, 1984a). 1. Jungermanniales The order Jungermanniales, the largest among the Hepatopsida with about 180 genera and 7500 species (Bold et al., 1989), comprises the “leafy liverworts”. These are also referred to as acrogynous liverworts in as much as their sporophyte develops at the apex of the main stem or lateral branches that, as in the acrocarpous mosses, cease growing. In contrast to the huge variability of gametophyte morphology, the sporophyte of the Jungermanniales is rather uniform and displays, in all instances, a distinct division into foot, seta and capsule. The foot is generally bulbous or spheroidal (Fig. 42) of relatively small size (20C300 km in diameter), and sometimes reduced to a few cells (e.g. in Lejeunea; Schuster, 1984a). In many instances a “collar” of cells develops at the junction with the seta. This probably reinforces the attachment of the sporophyte to the parental gametophyte. In some genera, e.g. Goebefobryum and Acrobolbus (Schuster, 1966), the collar is particularly bulky, and in extreme cases, as in Jackielfu (Schuster, 1984a), it consists of a massive sheath of multicellular filaments. The foot in Radulu (Figs. 53 and 54) recalls bryopsid mosses such as Bryum and Diphyscum in the presence of irregular radially elongated peripheral cells that interdigitate with the adjacent gametophytic cells. In some cases, e.g. Lejeuneu, Jubula, Frullania and Bryopteris, the foot remains surrounded by a tissue derived solely from the archegonial base, and does not penetrate the stem apex. Such a condition is probably related to the stalked structure of the archegonia in these genera (Crandall-Stotler and Guerke, 1980; Schuster, 1984a). More frequently, the foot is deeply Figs. 33 and 34. Bryalean placentas (cont.). Fig. 33. Oblique section through the thin, convoluted ingrowths in a gametophyte placental cell of Bryum cupillure. Fig. 34. The placenta in a young sporophyte of Fissidens crussipes. Note the early development of the wall labyrinths.
HerbeItaEeae Hwberra 'pp.
1
+
Lcpidoriaceae Kuriro rnchocldos Grolle Zoopsrr Irukiumw Horik
I 1
+ +
1 1
+ +
Cephalozraceae
Cephpholorro brcupidnrv (Nees) Llrnpr. Cephphaloiro lunulifolm Durn
Jungerrnanniaceae Jungermannia gracrllrma Sm
1
t
Gyrnnornitriaceae Marruprlln funrkri Durn
1
+
1
I
+ +
Lophomleo hrrerophyllo (Schrad) Durn.
I
+
Radulaceae Rodulo complonrvo (L ) Durn
1
Scapantaceae Scoponio grveib Kaal Dtplophyllw, albrconr (L ) Durn. GeOCalyC2Le*e
j
5
1
1 1 I 1
I 1
Riccordw mulnfido S Gray
~
~
Outermost fool a l l r . accarbnally
on tareral cell,
+
Outer rang.bwalIr
+
t
+
~
~
~
~
Late
. N,A
,
Lahynnth. fine very dcnre
. N/A
.
-
.Bulbour
Thldtenln~01 mner laogntlal "all> auh
radially am"@ depovtr
N:A
+
+
. N:A
NIA
Several l a y e r r of Ldlz
Late
Ourer tang. aod
Sereral laycn of
Late
lateral naUs
cells
NIA
Late
Late
Lahynnth
Lahynnth Lahynnth } Coane
Outertang *all5 Outerlang. nalk N:A N:A
N:4 N:A N:.4
NIA
NIA
NIA
X:A
N:A
NIA
NIA
NIA
W l
Ni.4
NIA
NIA
NIA
Labynth
BdbO",
Lahynnth Coarse
Con,cal
Coarse
Thm walk. inegular
plaimalernma
CALOBRYALES Colobrywn hlums Necs Hoplomrlnum hookui Neen
MARCHANTUDAE MONOCLEALES Monucleu gouxha Lmdb. SPHAEROCARPALES Sphaermwpm donne//,Aust Sphaerocarpos kzmw A w l . MARCHANTIALES Carrpineae Conpos monocorpos Prosk
I
Several byerr of Fells
+
Outer rang and lateral walls
Several layers of cel- Late
I
+ +
+
I
+ +
Targorgronro h.vpophvllo L
+
Reboulw hemrrphnrnco Raddi
Plogiochosmo rupesrrc Steph
Outer
4
TaC@O"lCiCW
Monnta ondrogmo Evan,
+
+
Several layen of
+
outer tang
Several layers of d l S
+
Outer tang walls
+
+
1
+
} Outer
+
Wi1116
cells
Outer tang. wall
outer tang. wall
Several layers of
cells
} Labyrinth Labyrinth
Transparent
} Labynnth } Labynnth
Transparen1
} Late
} Labyrinth
Late
Labyrinth
Shon coarse
Late
Labyrinth Coax
Labyrioth Coarse
Late
Labyrinth
Labynnth
Late
Late
Labryinth
Labynnth
Late
Late
Labynnth
Labyrinth
} Very Late
Late
outerrang walls and inner parenchyma
Late
15
tang. and lateral walls
+
} Early
}Early
late
-
} Bulboua
-
Conlral
} Labyrinth }
} Spheroidal -
Spheroidal
Spheroidal
~
~
~
BUlhOUS
Bulboua
Bulbous
TABLE IV Cytoplasmic features of placental cells in liverworts Plartids Fametophyte
Sporophyte Sham
Membrane system
Plastodobuli
Starch
Shaoe
Plwmorphic
r.gr.
+
+
Ellipsoidal
Spheroidal Ellipsoidal Pleomorphic
qr.
+ +
+
Cepholoria bicurpidatu Cephnloiio lunulifolio
Ellipsoidal Pleomorphic
n.gr.
+
Ellipsoidal Ellipsoidal
Jungerrnanniaceae Jungermannia gracillima
Spheroidal Ellipsoidal
*.g
+
Ellipsoidal
Membrane system
Plastoglobuli
Starch
Cytoplasmic lipid droplets Sporophyte Gametophyte . . .
JUNCERMANNIALES Herbertamae Herbem sp.
Lepidoziaceae Kurrio Wchoclados Zoopsk liukiuenrk
Cephaloziaceae
Gymnomitriaceae
Manuprlla funckii
Scapaniaceae Scaponzo grocilrr
Diplopkyllum albicons
Geacalycafeae
Lophoeoleo heterophyllo
Radulaceae
Rodulo complonoro
Ellipsoidal
r.gr.
n.gr.
+
+
++
++ +
Ellipsoidal Ellipsoidal
+
+ +
+
Pleomorphic
n.gr.
Pleomorphic Pleomorphic
r.gr. r.gr.
Ellipsoidal Pleamarphic
n.gr.
Ellipsoidal
+
+
Elliposidal
r.gr.
Spheroidal
++
+
Elongate Pleomorphic
n.gr.
Spheroidal
Pleomorphic
n.gr.
Spheroidal
Pleomorphic
pr0.b.
Pleomorphic
Pleomorphic
qr.
Pleomorphic
Pleomorphic Pleomorphic Pleomorphic
r.gr.
+
Ellipsoidal Pleomorphic Pleomorphic
+
+
+
+
METZGERIALES Fossombroniaceae
Fosrornbronio echinoto
Blasiaeeae
B l a h pusillo
Pelliaceae Pollovicinio lyellii Pallovicinio indim Pellia endiviifolia Pellio epiphyllo A"e"raCeae Aneuro pinguk
Cryprothollw mirobilir
Riccordio multifida
} }
+
*.
r.gr.
+
+
++ +
Pleomorphic Plwmorphic Plwmorphic
+
+
+
+
11 +
+ +
1:
+ +
+
'.*. r.gr
Pleomorphic Spheroidal
'.
Sphered Plmmorphic
}
Ovoid
}
Plwrnorpbic Plmmorphic
".*. ".gr.
'.gr.
+
P.'.
Spheroidal
}
w.
".a.
Ovoid
Spheroidal
'.*.
ELlipsoidal Plwmorpbic
r.-
Spheroidal Plwmorphic
pro.b.
spheroidal Spkroidal Plwmorphic
n.gr.
Discoid
0.gr.
Elongate + Rbres Pltomorphic Plwmorphk
,.g.
Elongate Plwmorphic Plwrnorphic Dismid Discoid
Riccia sorocarpa
+
c
NIA
'.*.
+ +
+
'.*. r.*.
+ '.*.+
+ +
NIA
N/A
'gr. p.r. P.'.
NIA
'.gr r.-n.gr
r.gr.
'.gr.
Dismid Discoid
'.*. r.g.
NIA
N/A
NIA
Abbreviations: we., oormal m a . like t h a v in leaves; r . ~ rudimentary . gram, 2-3thylaloids only; r , siogle thylaloids; pr0.b. prolameUar body; p.'. peripheral miarlum.
NIA
NIA
NIA
262
R. LIGRONE et al.
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
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embedded in the stem tissue (Fig. 42), although very little or no true penetration actually occurs, since the axial tissue surrounding the foot develops after fertilization (Schuster, 1984a). The cytology of the placental region, examined in 11 species belonging to eight different families (Table HI), is extremely uniform and highly distinctive. With the exception of Radula, elaborate wall labyrinths develop in the outermost cells of the foot. In this last genus the walls of the sporophytic placental cells are relatively thin and smooth. In the other 10 (Fig. 54) these cells produce thin and highly branched ingrowths of extremely dense wall material (Figs. 43-46). Less extensive wall labyrinths or isolated wall ingrowths are present in the parenchyma cells of the foot. No trace of wall ingrowths is observed in gametophytic placental cells of all eleven genera. The cytoplasmic organization of sporophytic placental cells is somewhat variable. In Zoopsis, Marsupella and Kurzia these cells contain one or a few large vacuoles of irregular shape and the nucleus is suspended in the centre by cytoplasmic strands connected with a peripheral layer of cytoplasm (Figs. 43 and 44). Most organelles, notably plastids and mitochondria, are associated with the wall labyrinth along the outer tangential walls. In Scapania, Diplophyllum, Lophocolea, Radula and Herberta the sporophytic cells have very small vacuoles and are rich in lipid deposits concentrated in proximity to the wall labyrinth (Figs. 45 and 46). The gametophytic placental cells, though lacking wall ingrowths, are clearly distinct from the parenchyma cells farther from the foot in having smaller vacuoles and denser cytoplasm, rich in mitochondria and other organelles. These cells form several concentric layers around the foot, the innermost of which degenerate and collapse during the phase of foot expansion (Figs. 43-45). An interesting specialization has been reported in Jubula, where the gametophyte cells within a 40pm range of the foot continue dividing as sporophyte growth proceeds to form small-celled filaments that extend towards the foot (Crandall-Stotler and Guerke, 1980). This also happens but to a more limited extent in Radula (Fig. 53). In every genus the inner tangential walls of gametophyte placental cells become thickened and may produce radially arranged deposits of dense material (Fig. 47) similar to those found in some Sphagnum species (Ligrone and Renzaglia, 1989), Andreaea, Takakia and Polytrichales. Plastid morphology in the placental cells of the Jungermanniales also is somewhat variable. The sporophyte cells contain numerous small plastids ranging in shape from spheroidal (Kurzia; Fig. 50), ellipsoidal or irregular (Herberta, Cephalozia, Zoopsis and Lophocolea; Fig. 49), to highly Figs. 35-37. Plastids in bryalean sporophyte placental cells. Fig. 35. Mniurn hornum; pleomorphic with massive grana. Fig. 36. Eryum cupillare; undifferentiated plastids intermingled with mitochondria. Fig. 37. Dicrunum mujus; ovoid with massive grana. Note the umbo-shaped mitochondria.
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Figs. 38-41. Plastids in bryalean gametophyte placental cells. Fig. 38. Cladophascum gymnomitrioides; starch grains surrounded by rudimentary grana. Fig. 39. Diphyscium foliosum. Fig. 40. Diphyscium foliosum; vaginula cell. Fig. 41. Blindia acuta.
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
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pleomorphic (Scapania and Diplophyllum; Figs. 51 and 52). The thylakoid system may be as extensive as in the leaf cells (Cephalotia, Lophocolea, Marsupella, Radula and Zoopsis; Figs. 46 and 49), or poorly differentiated (Scapania, Herberta and Diplophyllum; Figs. 51 and 52). Starch may be present (Lophocolea, Herberta, Cephalozia and Marsupella; Figs. 45 and 46) and is sometimes abundant (Kurzia; Figsvvvvv. 43 and 50), but in other genera (e.g. Scapania, Diplophyllum and Radula) is absent (Figs. 51 and 52). Plastids in gametophyte placental cells are generally larger than in the sporophyte, have a well developed thylakoid system and contain very little starch. The gametophyte plastids of Herberta are unusual in having abundant lipid inclusions associated with the thylakoid system (Fig. 48). 2. Mettgeriales The Metzgeriales, with about 20 genera and 550 species, are commonly referred to as the “simple thalloid liverworts”, the gametophytes lacking air chambers, air pores, pegged rhizoids and-with some exceptions, e.g. Blasia and Cavicularia (Renzaglia, 1982)-ventral scales (Bold el al., 1989). They are also called the anacrogynous liverworts, as sporophyte development normally does not terminate the growth of the gametophyte. The foot is generally conspicuous, of conical or spheroidal shape, and frequently bears a massive collar (Fig. 55). The placental region is highly variable, with all the possible combinations in the distribution of transfer cells (Table 111). In Blasia and Fossornbronia well-developed transfer cells are found in both generations (Figs. 56 and 57), generally forming several layers in the gametophyte. Transfer cells are restricted either to the sporophyte in Pallavicinia (Fig. 5 8 ) , or to the gametophyte in Riccardia (Fig. 59). The walls of the sporophytic placental cells in the latter genus are identical in appearance to their gametophytic counterparts in the Jungermanniales: both have thickened outer tangential walls containing radially arranged deposits of dense material (compare Figs. 59 and 60 with Fig. 47). In striking contrast, wall labyrinths are absent in Pellia (Fig. 61), Cryptothallus (Fig. 62) and Aneura. Here the placental cells of both generations are thin-walled save for the limited development of nacreous thickenings in the sporophytic cells of Aneura (Fig. 63). In these genera that lack wall ingrowths the plasmalemma of placental cells often presents an irregular outline along the tangential walls and may form short invaginations apparently not supported by wall material (Fig. 64). Similar invaginations are also found in parenchyma cells of the foot in Cryptothallus. In most species the wall ingrowths, when present, are short and coarse and form relatively simple wall labyrinths. By contrast, in Blasia (Fig. 57) and, to a lesser degree, in Fossombronia (Fig. 56), the sporophyte cells have highly branched wall ingrowths that form three-dimensional networks of
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great complexity. Similarly elaborate wall labyrinths are common in marchantialean liverworts (see Section II.B.4), but are not found in the placenta of Jungermanniales. The placental cells also exhibit a notable diversity in their cytological organization. Generally they have dense cytoplasm rich in organelles and with numerous evenly scattered vacuoles of small sizes, but highly vacuolate placental cells are found in Pellia and Aneuru (Figs. 61 and 63). The sporophyte placental cells of Riccardia contain giant pleomorphic mitochondria, often associated with the nucleus (Fig. 65). Abundant sheets of rough endoplasmic reticulum characterize the gametophyte cells of Aneuru and Cryptothaffus(Fig. 66) and concentric sheets of endoplasmic reticulum surround lipid bodies in the sporophyte placental cells of Cryptothallus (Fig. 67). As in the Jungermanniales, the placental cells in the Metzgeriales contain numerous plastids of small sizes. In sporophytic cells, plastids with a welldeveloped thylakoid system are found in Bfusiu and Fossombroniu (Fig. 68). A less extensive thylakoid system is found in the plastids of Riccurdia (Fig. 69), and in Puffavicinia the thylakoids are associated with prolamellar body-like membranous arrays (Fig. 70). The thylakoid system is rudimentary in the sporophyte plastids of Pellia, Aneuru and in the early stages in Riccardia (Fig. 71) and Cryptothaffus(Fig. 72). At comparable stages in development, starch is absent in Fossombroniu, Blasia and Cryptothaffus,present in small amounts in Riccardia, and abundant in Aneura and Peffia.Plastids in gametophyte placental cells are much less variable and generally contain small starch grains and an inner membrane system of small grana connected by stroma thylakoids. Highly pleomorphic plastids occur in Aneura and Cryptothaffus(Fig. 73). As in other groups, the gametophyte cells closer to the foot, regardless of the presence of a wall labyrinth, degenerate precociously (Figs. 57 and 62). In most species, signs of cytoplasmic degeneration are visible in gametophyte placental cells soon after sporocyte differentiation, whereas the sporophyte placental cells show little changes until spore formation, although they show signs of cytoplasmic degeneration before the seta starts elongating. In Riccardia the wall labyrinths in gametophyte cells reach their maximum complexity after meiosis (Fig. 5 8 ) , at which time the wall thickenings develop in the sporophyte cells. A progressive increase in the thickness of sporophyte placental cell walls also occurs in Cryptothuffus along with capsule maturation. Figs. 42-44. The gametophyte-sporophyte junction in Jungermanniales. Fig. 42. Light micrograph; longitudinal section of the bulbous foot of Kurzia trichoclados. Fig. 43. Kurzia trichoclados; note the fine wall labyrinth and amyloplasts in the highly vacuolate sporophyte placental cells and collapsed gametophyte cells (arrowed) adjacent to the foot. Fig. 44. Marsupellafunckii; the cytology of the junction is virtually identical to that in Kurzia apart from the absence of starch in the sporophyte cells.
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3. Calobryales
The Calobryales are a small group of leafy liverworts that traditionally includes three genera, Haplomitrium, Calobryum and Takakia, each comprising a few species. The first two are considered as synonyms by Schuster (1984b), whereas the last one is now best placed in a separate group close to the Andreaeidae (see Section 1I.A. 1). The sporophyte of Haplomitrium and Calobryum is enclosed within a shoot calyptra until maturity and forms a massive seta terminating downwards with a large bulbous or obconical foot (Bartholomew-Began, 1991). Unlike the gametophyte stem, which contains a central strand of water-conducting dead cells (Hebant, 1977, 1979), both the seta and foot consist of homogeneous parenchyma. However, dead empty cells with electron-dense deposits associated with longitudinal walls have been observed occasionally in the foot of Calobryum blumei (Fig. 76). A wall labyrinth is present in both foot epidermal cells and adjoining gametophyte cells (Figs. 74 and 75). Smaller labyrinths or isolated wall ingrowths may occur in more peripheral gametophyte cells and in the outermost parenchyma cells of the foot. The wall ingrowths in sporophyte placental cells are generally longer and more highly branched than in the gametophyte. Placental transfer cells differentiate before proliferative divisions terminate in the capsule, that is long before the onset of meiotic division. The sporophyte placental cells seemingly contain a single, highly pleomorphic plastid in Haplomitrium (Fig. 78), whereas numerous spheroidal and pleomorphic plastids, frequently associated with the nucleus, are found in Calobryum (Fig. 77). In both instances these organelles have but a rudimentary inner membrane system consisting of small granal stacks and few or no stroma thylakoids. Gametophyte placental cells contain pleomorphic plastids with a better developed thylakoid system, characterized in Calobryum by the presence of granal stacks perpendicular to the long axis of the organelles (Fig. 79). Starch is lacking in gametophyte cells, whereas small starch grains are common in sporophyte cells of Calobryum (Fig. 77). Abundant starch deposits are found in both foot parenchyma and gametophyte cells farther from the foot. Both sporophytic and gametophytic placental cells contain numerous mitochondria, frequently in intimate association with plastids (Figs. 77 and 79). The mitochondria are distinctly larger in sporophytic than in gametophytic placental cells. Figs. 45-47. The gametophyte-sporophyte junction in Jungermanniales (cont.). Fig. 45. Herberta sp; sporophyte transfer cells rich in lipid droplets. Collapsed garnetophyte cells are arrowed. Fig. 46. Lophocolea hererophyllu; sporophyte placental cell rich in lipid droplets. Fig. 47. Lophocolea; the gametophyte placental cell walls have tangential thickenings with radial deposits of dense material.
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T H E GAMETOPHYTE-SPOROPHYTE JUNCTION
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4. Marchantiidae The three orders Monocleales, Sphaerocarpales and Marchantiales are related by a series of morphological and developmental features, including a similar embryogeny, specialized oil body-containing cells (Schuster, 1984a) and blepharoplast morphology (Duckett et al., 1982, 1984; Brown et al., 1983; Carothers etal., 1983), and are classified together within the subclass Marchantiidae by Schuster (1984b). All three present a similar placental organization and will therefore be discussed together. The foot, inconspicuous in the Sphaerocarpales, is relatively large in most Marchantiales, and varies in shape from spheroidal (Sphaerocarpos, Targionia), bulbous (Corsinia, Lunularia, Reboulia), cup-shaped (Marchantia, Preissia) to obtuse-conical (Monoclea; Fig. 80) or conical-elongated (Conocephalum). The placenta has been studied in detail in Monoclea, two species of Sphaerocarpos and eight species of Marchantiales (Tables I11 and IV). All of these except Riccia, whose sporophyte lacks a foot, exhibit much the same organization, with well-differentiated transfer cells in both generations (Figs. 81-86). The wall labyrinths in sporophyte cells consist of highly branched and anastomosing ingrowths and attain a structural complexity not equalled elsewhere in liverworts except Blasia. In several species, e.g. Sphaerocarpos (Fig. 83), Reboulia (Fig. 854, Targionia (Gambardella, 1987), and Monoclea (Fig. 81), gametophyte transfer cells also form extensive wall labyrinths, whereas in others, e.g. Carrpos (Fig. 86), Dumortiera (Fig. 84) and Conocephalum (Ligrone and Gambardella, 1988a), they have but coarse and short wall ingrowths. As a rule, there are several layers of transfer cells in the gametophyte, the innermost ones degenerating early in sporophyte development (Fig. 84), and a single layer in the sporophyte. Small wall labyrinths or isolated wall ingrowths are frequent in the peripheral parenchyma cells of the foot in Reboulia and Conocephalum (Ligrone and Gambardella, 1988a). A study of placental development in Targionia hypophylla (Gambardella, 1987) has shown that the wall labyrinths develop after differentiation of sporocytes, i.e. much later than in mosses (Browning and Gunning, 1979a). Generally both sporophyte and gametophyte placental cells contain numerous plastids with a well-developed thylakoid system. Pleomorphic plastids with a scarcely developed inner membrane system have been observed in sporophyte placental cells of Mannia and Plagiochasma (Gambardella and de Lucia Sposito, 1981, 1983) and a rudimentary inner membrane system associated with prolamellar body-like structures occurs in Figs. 4%5l. Plastids in jungermannialean placental cells. Fig. 48. Herbertu sp. gametophyte; ovoid and lipid bodies associated with the thylakoids. Fig. 49. Cephaloziu bicuspidata sporophyte: well developed grana. Fig. 50. Kurzia trichocludos sporophyte; ovoid amyloplasts. Fig. 51. Scuprmiu graci1i.r sporophytc; plcomorphic undifferentiated plastids.
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sporophyte plastids of Conocephalum (Ligrone and Gambardella, 1988a). The plastid stroma in the gametophyte transfer cells of Reboulia contains a bundle of thin parallel fibres (Fig. 87; Ligrone and Gambardella, 1988a). As in Metzgeriales, the placental cells in Marchantiales contain large stacks of endoplasmic reticulum. Distinctive membrane-bound bundles of tubules are found in young gametophytic placental cells of Reboulia hemisphaerica var. macrocarpa Zodda (Zodda, 1934; Figs. 88 and 89). In crosssection the tubules exhibit hexagonal packing (Fig. 88). Prominent bundles of fibrillar material without a bounding membrane were detected in the var. macrocephala Zodda (Ligrone and Gambardella, 1988a). However, the gametophyte placenta cells in this taxon contain concentric arrays of giant cup-shaped mitochondria (Ligrone and Gambardella, 1988a). Giant pleomorphic mitochondria in intimate association with plastids are also found in the gametophyte placental cells of Carrpos (Fig. 86). Cytoplasmic degeneration starts in gametophyte placental cells during meiotic division, a process often taking several months in the Marchantiales. By contrast the sporophyte cells break down only after spore formation. As in mosses (Browning and Gunning, 1979a), the degenerating transfer cells of Marchantiales (Gambardella, 1987) and other groups obliterate their wall labyrinths by depositing new wall material in the interstices among wall ingrowths. It has been suggested that in mosses this process may help to prevent the flow of water towards the drying capsule after spore maturation (Browning and Gunning, 1979a). This is highly unlikely in liverworts, where obliteration of the wall labyrinth precedes the elongation of the seta, a process needing large amounts of water, particularly in the Jungermanniales and Metzgeriales. No transfer cells are found at the sporophyte-gametophyte junction in Riccia. The sporophyte is entirely enclosed in the gametophyte (Fig. 90) and consists of a spherical capsule with a single-layered wall, surrounded by a two-layered calyptra (Fig. 91). With capsule enlargement the cells of the inner layer of the calyptra collapse and, following spore formation, the walls of thallus cells facing the calyptra become thickened (Fig. 92). Despite the absence of a specialized placental tissue, abundant lipid reserves accumulate in the spores (Fig. 92), indicating the operation of an effective mechanism of nutrient transport towards the sporophyte. Most probably nutrients are Fig. 52. Diplophyllum alhicans; pleomorphic plastid with a rudimentary thylakoid system in a sporophyte placental cell. Figs. 53 and 54. The gametophyte-sporophyte junction in Radula complanata. Fig. 53. Light micrograph, transverse section of the foot showing radially elongate outer cells. Fig. 54. Thin-walled sporophyte cells lacking ingrowths and thicker walled gametophyte cells. Figs. 55 and 56. The gametophyte-sporophyte junction in Metzgeriales. Fig. 55. Pellia epiphylla; light micrograph, longitudinal section showing the collar (arrowed). Fig. 56. Fossomhronia echinata a prominent labyrinth is present in both the sporophyte and gametophyte placental cells.
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translocated across the whole sporophyte surface; the calyptra cells, that have dense cytoplasm rich in mitochondria, may play a major role in this process. C. ANTHOCEROTES (Anthocerotopsida)
The anthocerotes or hornworts comprise about 100 species that currently are classified into five or six genera, i.e. Phaeoceros, Notothylas, Folioceros, Anthoceros, Megaceros and Dendroceros (Schofield, 1985; Hasegawa, 1988). This group is distinguished from all the other embryophytes on the basis of a range of cytological, anatomical and developmental characteristics (Crandall-Stotler, 1980, 1984), and is considered by Schuster (1984~)as an independent evolutionary line of land plants. The archegonia develop from dorsal epidermal cells and at maturity protrude slightly above the thallus surface. The egg cell is bordered by cells of the thallus, in as much as an archegonial venter, in the strict sense, is lacking (Renzaglia, 1978). Unlike mosses and liverworts, the first division of the zygote is longitudinal and produces two cells that then divide transversely. A longitudinal wall perpendicular to the first one divides the embryo into four upper and four lower cells. The upper cells then divide transversely. The resulting 12-celled embryo consists of three tiers of four cells each. In Notothylas the foot arises from the lower tier only and the middle tier functions as a short-term meristem, whereas the cells of the upper tier serve as sporangial initials (Campbell, 1918; Renzaglia, 1978). In the other genera a massive bulbous foot derives from divisions in the lower two tiers, whereas the upper tier produces both a basal meristematic zone and acropetally differentiating sporangial tissues (Renzaglia, 1978; Crandall-Stotler, 1984). When embryogenesis begins, the thallus cells adjoining the archegonium divide and form an investing involucre around the sporophyte. In Notothylas the sporophyte remains enclosed in this involucre until maturation of all the spores is complete. In the other genera the sporophyte emerges from the involucre as soon as the first-formed spore mother cells complete meiosis, and continues growing for long periods because of activity of the basal meristem (Crandall-Stotler, 1984). Unlike mosses and liverworts, where the foot achieves complete cellular differentiation during specific stages in sporophyte development, in anthocerotes cellular proliferation and differentiation at the sporophyte-gametophyte junction proceeds continuously along with sporophyte growth throughout the life-span of the latter. Figs. 57-59. The gametophyte-sporophyte junction in Metzgeriales (cont.). Fig. 57. Blasia pusilla; prominent wall labyrinths in both generations. Fig. 58. Pullavicinia indica; sporophyte wall labyrinth and thin-walled gametophyte cells. Fig. 58. Riccafdia mulr@du; thick-walled sporophyte cells and gametophyte wall labyrinths.
Anrhoceros punc~oturL.
Anlhoreros Jormosar Haseg Anrhoceros gronulosa Haseg Phaeocrros / n e w husk.
Plmeorero.~curohntonus Proak. Foltoceror JuaJo.rlornirrBharadw
Nomrhdrv orhtorlorrr Sull. Noforhvlrv emperaro Haseg
Dmdrocem co~emoxu(Haseg. Dendroreros iovonicur Nees. Dmdroceros mherculons Haft Megocerorj?agellrrrrrSteph.
2 1 I
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spacer
Early and C0"fl""O"I
Cornplcl labyrmths
Complex }labyrinths Complex labyrinths Complex }labyrinths Simple labyrinths Simple lahynnth
I
Bulbous
l l t m walled. branched
unicellular or multiceUular haustoria
}Bulbour BdbU
: :1
}Bulbous
Ovoidal
0547
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T A B L E VI Cytoplasmic features of placental cells in anthocerotes Plastids Gametopbyre Shape Anrhoceros pwcIuNs Anrhocernr fonnosoe A~irhoc~ror gronulosu
)pIeomorphic
Phoeocrror Iowa Phveocerm corobnionur Folmeerosfurrformu
Membrane
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C L ~ Y P ~ O ~ W
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};L%&hir Spheroidal
Sporophyte Plastoglobuli
kyr
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r.gr pyr
*
Abbreviations. n gr . normal grana; r.gr ,rudunentalygrana: pyr , pyrenoid.
/+
+
I+
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1I-
Shape
1
Spheroidal pleomorphir
Spheroidal }pieumorpixuc Spheroidal pleomorphic ptxmd
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Spheroidal pleomorphic
Spheroidal pleomorphic
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++ ++
+
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THE GAMETOPHYTE-SPOROPHYTE JUNCTION
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The foot is ovoidal (Megaceros, Dendroceros; Fig. 93) or bulbous in the other four genera (Figs. 94 and 95) and generally 0.5-0.7mm in diameter except in Notothylas and Dendroceros (0.25-0.4 mm in diameter). The organization of the placenta is fundamentally the same in all the genera and comprises long and branched haustorial cells of sporophytic origin intermingled with gametophyte cells (Figs. 96,97,99 and 101). The two cellular types are separated by abundant intercellular spaces containing PASpositive mucilage, that enlarge locally forming wide lacunae. As in mosses and liverworts, the placental cells are highly specialized and clearly distinct from the other cells of the respective generation. The haustorial cells have uniform and relatively thin walls. They penetrate the gametophyte tissue by intrusive growth involving both cell division and elongation (Gambardella and Ligrone, 1987). The nucleus generally lies and divides far from the growing tip (Fig. 97), and this may branch with (Figs. 96 and 101) or without (Fig. 97) the formation of cross walls. The haustorial cells are highly vacuolated in Megaceros, whereas they contain less prominent vacuoles and more abundant cytoplasm in Anthoceros, Phaeoceros and Folioceros. Numerous vacuoles of small sizes occur in the haustorial cells of Notothylas (Fig. 101) and Dendroceros (Fig. 96). In all genera but Notothylas the haustorial cells contain large spheroidal or irregularly shaped plastids with a rudimentary thylakoid system, abundant plastoglobules, sometimes spherical starch grains and vesicles of various sizes (Vaughn et al., 1992; Figs. 97 and 98). The haustorial cells of Notothylas contain chloroplasts with a well-developed inner membrane system (Fig. 101) and sometimes a distinct pyrenoid, though less prominent than in other vegetative cells of the thallus. The gametophyte placental cells are much smaller than ordinary parenchyma cells of the thallus, have dense cytoplasm with several relatively small vacuoles and are rich in endoplasmic reticulum, dictyosomes and mitochondria which form prominent aggregates in Phueoceros carolinianus (Fig. 102). At maturity they present wall ingrowths of variable sizes, generally along the cell sides abutting intercellular spaces. Wall labyrinths of considerable complexity are found in Phaeoceros, Notothylus and Folioceros (Figs. 99 and 101), whereas in the other genera they are much simpler (Fig. 96). In all genera except Dendroceros the plastids lack starch and have rudimentary thylakoid systems and the pyrenoid is highly reduced or absent (Fig. 102). In the gametophyte placental cells of Dendroceros are
Figs. 60-63. The gametophyte-sporophyte junction in Mctzgeriales (cont.). Fig. 60. Riccardia mulfifidu;thickened tangential walls with radial deposits, sporophyte placental cell. Fig. 61. Pelliu epiphyllu; thin-walled placental cells in both generations. Fig. 62. Cryprofhullus mirubilis; wall ingrowths are absent. The intraplacental space contains collapscd garnetophyte cells (arrowed). Fig. 63. Aneuru pinguis: nacreous wall thickenings in the sporophyte placental cells.
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chloroplasts with a well-developed thylakoid system but lacking a pyrenoid (Fig. 100). Dense bodies with a crystalline substructure are present in large amounts in the intercellular spaces, most notably in the large lacunae, of the placenta in Phaeoceros, Notothylas and Folioceros (Figs. 103-106). These structures react positively to protein stains (Marsh and Doyle, 1985) and are completely digested by pronase or pepsin (Fig. 104), hence they are assumed to be protein (Gambardella and Ligrone, 1987). In longitudinal or oblique sections the crystals consist of alternating dense and light bands. Transverse sections reveal a regular network of hexagonal subunits, approximately 15nm wide, with a light internal core (Fig. 103). Degradation of the crystals has been observed in Phaeoceros and Notothylas (Fig. IOS), notably at advanced stages in sporophyte development, and it has been suggested that these structures may serve as a source of nutrients for the sporophyte growth (Marsh and Doyle, 1985). The larger lacunae in Phaeoceros and Folioceros are formed by dissolution of gametophyte placental cells, a process that presumably is induced by the haustorial cells (Gambardella and Ligrone, 1987). Degeneration of gametophyte cells follows their symplasmic isolation from the adjoining cells, due to the severance of plasmodesmatal connections. Crystals are deposited in the vacuoles of gametophyte cells (Fig. 106) and are liberated in the placental lacunae as a consequence of cellular dissolution. Crystals are but rarely observed in the placenta of Megaceros and are not found in Anthoceros and Deridroceros. Both sporophyte and gametophyte placental cells of Dendroceros contain intravacuolar deposits of dense amorphous material (Fig. 98) that is assumed to be protein in as much as it is negative to the PATA test for carbohydrates and sensitive to digestion by pronase (Ligrone and Renzaglia, 1990). Similar protein deposits also occur in the parenchyma cells of the foot and virtually all the cells of the sporophyte capsule, including the spores. Overall, these observations suggest that protein is synthesized in the haustorial cells, presumably from precursors provided by gametophyte transfer cells, and is then transferred, via plasmodesmata, to the parenchyma cells of the foot and eventually to the cells of the growing capsule. Like the protein crystals in Phaeoceros and Folioceros, the amorphous protein deposits in the gametophyte placental cells of Dendroceros may function as a source of amino acids for the sporophyte, although they are never found free in placental spaces (Ligrone and Renzaglia, 1990). Figs. 64-67. The gametophyte-sporophyte junction in Metzgeriales (cont.). Fig. 64. Cryptorhallus mirabilis; highly irregular plasmalemma in a gametophyte placental cell. Fig. 65. Riccardia mulrificla: giant mitochondrion in a sporophyte placental cell. Fig. 66. Cryplorhullus mirabilis: grazing section of endoplasmic reticulum with abundant attached polysomes in a gametophyte placcntal cell. Fig. 67. Cryprothallus; concentric sheets o f R E R around a lipid body in a sporophyte placental cell.
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The placental region develops very early and is well organized when the sporophyte, less than 1 mm long, is barely discernible with naked eye within the gametophyte thallus. In Phaeoceros abundant intercellular crystals are found in the placenta when the sporophyte emerges from the involucre, whereas wall labyrinths are formed in gametophyte placental cells during the subsequent phase of capsule elongation (Gambardella and Ligrone, 1987).
111. THE TAXONOMIC SIGNIFICANCE OF THE PLACENTA IN BRYOPHYTES AND IMPLICATIONS FOR PHYLOGENY Two main conclusions emerge from the comparative data described here for the first time: (a) placental organization is extremely diverse in the bryophytes as a whole; and (b) with some exceptions, it is highly constant within particular groups of bryophytes. The diagnostic features embrace not only the walls and cytoplasmic contents of the placental cells, but also the timing of their differentiation. Whereas wall characteristics render the placental regions of different groups almost absolutely distinctive, cytoplasmic features and especially plastid ultrastructure tend to be peculiar to particular genera. This remarkable diversity in placental morophology in bryophytes has no obvious (or even obscure) functional meaning. For example, the absence of transfer cells on one or both sides of the placenta can hardly be assumed to indicate a lower efficiency in solute translocation and/or greater nutritional autonomy of the sporophyte. Indeed, in taxa lacking placental wall ingrowths (e.g. Sphagnum and Pellia), the sporophytes are just as highly differentiated and spore production just as prolific as in species where these are well developed. Conversely a typical bryalean placenta is found in Archidium (Brown and Lemmon, 1985) in spite of the extreme reduction of the sporophyte in this genus (Snider, 1975). Similarly in three different bryalean orders, namely Buxbaumiales, Pottiales and Dicranales, the placental regions are just as highly differentiated in genera with rudimentary setae (Diphyscium,Phascum and Cladophascum, respectively) as in those with elongate setae. Although it is now widely accepted that transfer cell morphology is associated with intense short distance transport of solutes (Gunning and Pate, 1974), most of the evidence remains circumstantial and knowledge of the biochemical and physiological mechanisms involved in this process via Figs. 68-72. Plastids in metzgerialean sporophyte placental cells. Fig. 68. Fossombronia echinara; elongate chloroplasts. Fig. 69. Riccardia rnultifida post-meiosis; ovoid with small grana and starch grains adjacent to a giant mitochondrion. Fig. 70. Pallavicinia indica; prolamellar body with radiating grana. Fig. 71. Riccardia mult@da pre-meiosis; ovoid and pleomorphic with single thylakoids. Fig. 72. Cryptothallus; pleomorphic undifferentiated plastids.
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the wall labyrinths has barely increased since the 1970s. Electrophysiological studies of the foot transfer cells in Polytrichum (Caussin et al., 1979, 1982, 1983; Renault et al., 1989) have demonstrated that protonelectrochemical gradients are generated through the wall-membrane apparatus and used to energize the uptake of solutes, particularly amino acids, from the apoplast. However, similar mechanisms also operate equally well in cells lacking wall ingrowths (Despeghel and Delrot, 1983; Kinraide et al., 1984). In the latter context it should be noted that the ultrastructure of thickened placenta walls with radial bands in Sphagnum, Polytrichales, Andreaea, Takakia, Jungermanniales and Riccardia is remarkably similar to that of the microspore intine in angiosperms (Charzynska et al., 1990; Murgia et al., 1991). Not only is the intine freely permeable to solutes, but recently the microspore has also been recognized as a type of transfer cell (Charzynska et a l . , 1990). The same kind of wall ultrastructure also characterizes vessel contact cells in the xylem of herbaceous angiosperms (Mueller and Beckman, 1984). Against a background of these functional considerations, the simplest explanation for the range of highly distinctive placental morphologies found in bryophytes is that each arose independently early in the evolution of each group. Once an effective transport system, with or without transfer cell morphology, had become established between the gametophyte and developing sporophyte, intense selection pressure for further change would disappear. Thus the ancestral condition would likely be retained more or less unchanged throughout the subsequent evolutionary history of each group. Clearly implicit in this hypothesis is the possibility that transfer cell morphology and other apparently similar placental features may not be homologous throughout bryophytes. Indeed, structural and temporal differences in wall ingrowth morphology and development strengthen this notion. Thus, with the exception of the Calobryales, early versus late differentiation of transfer cell morphology sets mosses clearly apart from hepatics. The fine dense wall labyrinths in Jungermanniales are very different from the coarse more transparent ingrowths in the Marchantiidae. Physiological studies are now needed to discover whether the temporal differences in placental transfer cell differentiation reflect differences in the availability of solutes destined for export from the gametophyte (see Gunning et al., 1968; Pate et al., 1970; Davey and Street, 1971; Gunning and Pate, 1974; Henry and Steer, 1980; for examples of the coincidence of wall Fig. 73. Cryptorhullus; highly pleomorphic undifferentiated plastid in a gametophyte placental cell. Figs. 74-76. The gametophyte-sporophyte junction in Calobryales. Fig. 74. Huplomitrium hooker;; wall ingrowths are more extensive in the sporophyte. Fig. 75. Calobryum blumei; a more cxtensive wall labyrinth in the sporophyte. Fig. 76. Calobryum blumei; dead cells with electron-dense deposits lining their walls in the central region of the foot.
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Figs. 77-79. Plastids in calobryalean placental cells. Fig. 77. Culobryum blumei sporophyte; pleomorphic plastids with starch and rudimentary grana. Fig. 78. Haplomitriurn hookeri sporophyte; a single highly pleomorphic plastid. Fig. 79. Calobryum blumei gametophyte; pleomorphic plastid with grana perpendicular to the long axis.
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ingrowth development with the presence of solutes destined for export in vascular plants). Similarly, cytochemical investigations aimed at elucidating the biochemical basis for the structural differences between the labyrinths of different groups may help to establish whether or not these are homologous. Bearing in mind the difficulties in distinguishing between parallel evolution and homology, it is nevertheless possible to draw major taxonomic conclusions from placental morphology and it is highly pertinent to explore the implications for phylogeny. Three basic types of placenta may be identified in mosses: an Andreaeatype, present in the Andreaeales, Takakiales and Polytrichales, a Sphugnum-type, restricted to Sphagnales, and a bryalean type, characteristic of the Bryales and also present in the Tetraphidales. Each type is sharply distinct from the others since the different distribution or absence of transfer cells can be immediately recognized, at least at the ultrastructural level (Table I). Minor variants are found within each type or group, for example the radially elongate foot transfer cells of Bryum and the rhizoidlike outgrowths of Diphysciurn. On the whole, however, the placental organization is remarkably constant even in the exceedingly large group of the Bryales, where taxonomically distant genera present little or no appreciable differences. A greater intergeneric diversity is apparent in the Polytrichales, especially in the gametophyte, perhaps indicating that this order is of considerable antiquity. The highly distinctive placental organization of the Sphagnales reinforces the notion that this is the most divergent group in mosses (Crosby, 1980; Brown et al., 1982; Duckett et al., 1982, 1984; Robinson and Shaw, 1984; Ligrone and Renzaglia, 1989). On the other hand, the discovery that the Andreaeales and Polytrichales share a similar placenta places the former clearly apart from the Sphagnales (cf. the “Pseudopodiate line” devised by Kumar, 1984) and closer to bryalean mosses. The presence of the same basic type of placenta in all the Bryales (with the only known exception, Dicranum majus, almost certainly representing a derived condition) confirms this group, including the Buxbaumiales and Tetraphidales, as a monophyletic unit. The discovery of a bryalean placenta in Tetraphis, previously reported as having labyrinthine walls in the sporophyte only (Roth, 1969), is in line with the notion, based o n studies of spermatid morphology (Duckett et af., 1982) and peristome development (Edwards, 1984; Shaw and Anderson, 1988), of a closer phylogenetic relationship between the Tetraphidales and arthrodontous mosses rather than between either group and the nematodontous Polytrichales. Likewise, the Buxbaumiales possess an arthrodontous peristome (Edwards, lY84; Shaw et ml., 1987) and a typical bryalean placenta. If we assume that placental transfer cells are plesiomorphic in embryophytes (see above) and that the Andreaeales and Polytrichales are primitive to the Bryales (Crosby, 1980; Robinson and Shaw, 1984), then the
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Andreaea-type of placenta appears to be the most likely ancestral type in mosses, with the other two types being derived (see also Ligrone and Renzaglia, 1989). This conclusion is strongly supported by the discovery of a placenta of the Andreaea-type in Takakia, a taxon that has long been classified in the Calobryales (Schuster, 1984b). Such a striking congruence between placental morphology and the anatomical features of the newly discovered antheridia and sporophyte in Takakia is a further confirmation of placental morphology as a taxonomically valuable character. Taxonomic and phyletic relationships between major groups in liverworts are more uncertain than in mosses. For example, it is still debated whether liverwort evolution has proceeded from leafy towards thalloid forms or vice versa. Schofield (1985) thinks of the gametophyte of a hypothetical ancestral liverwort as a flattened dorsiventral thallus with sex organs exposed on the dorsal surface, a model that is most closely approached by the Metzgeriales. Mishler and Churchill (1985) also believe that the ancestral type in liverworts is a simple thalloid gametophyte, though they construct a cladogram where the Metzgeriales and Jungermanniales are considered advanced and the Sphaerocarpales and Marchantiales primitive. Schuster (1984b) observes that the passage from a leafy to a thalloid habit has probably occurred several times independently in different liverwort groups, and suggests that the great diversity of gametophytic types may ultimately be derived back to a simple radial, leafless type. O n the basis of a wide range of characters, he recognizes a “primary dichotomy” between two subclasses, the Jungermaniidae (comprising the Jungermanniales and Metzgeriales) and the Marchantiidae (including the Sphaerocarpales and Marchantiales), with deviations from this generalization occurring principally in three taxa, i.e. Haplomitrium, Takakia and Monoclea. Placental morphology confirms the Jungermanniales and Marchantiidae as taxonomically well-delimited groups but sheds less light on possible inter-relationships between the Jungermanniales, Marchantiidae and the Calobryales. Unlike the ultrastructural uniformity in the appearance of the placental wall labyrinths in bryopsid mosses, their great variability in liverworts renders interpretation of homology, or lack of it, between transfer cells in different groups more problematic. The fine dense labyrinths in the sporophyte placenta of Jungermanniales are very different from the coarse electron-transparent ingrowths that characterize both generations in
Figs. 80-84. The garnetophyte-sporophyte junction in Marchantiidae. Figs. 80-82. Monoclea gottschei. Fig. 80. Light micrograph, longitudinal scction showing the obtuse conical foot. Fig. 81. Coarse electron-transparent wall labyrinth in garnetophyte placental cells. Fig. 82. Wall labyrinth in a sporophyte placental cell. Fig. 83. Sphaerocarpos texanus; wall labyrinths in placental cells of both generations. Fig. 84. Dumortiera hir.suta; short wall protuberances in the garnetophyte and extensive wall ingrowths in the sporophyte. Note the collapsed garnetophyte cells (arrowed).
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Marchantiidae. The ultrastructure of the calobryalean wall ingrowths is somewhat intermediate. The occurrence of sporophytic wall ingrowths and a tendency for the gametophytic placental cells to form thickened outer walls in 10 genera of the Jungermanniales ranging from putatively primitive (e.g. Herberta) to highly advanced (e.g. Zoopsis) (Schuster, 1984b) suggests that this is the ancestral condition in the group. The absence of transfer cell morphology in Radufa is almost certainly a derived condition perhaps related to interdigitation of the cells of the two generations instead of the clearly defined intraplacental lacuna seen in all the other genera. It would now be pertinent to discover whether this feature is peculiar to the Radulaceae, or if it also occurs in the allied families Porellaceae, Jubulaceae and Lejeunaceae. The uniformity in placental ultrastructure in the Marchantiidae which, with the exception of Riccia, extends throughout its three highly disparate orders Marchantiales, Sphaerocarpales and Monocleales, is clearly in accord with the widely recognized anatomical and development uniformity of this subclass (Brown and Lemmon, 1988, 1990; Crandall-Stotler, 1981; Schuster, 1984a,b). The occurrence in Carrpos of a placenta no less highly differentiated than in other members of the group weakens the case for a possible link with Riccia (Proskauer, 1961). Indeed, the absence of any trace of a placenta sets Riccia apart from all other archegoniates and from Coleochaete, the taxon generally considered to be the closest living algal relative to the embryophytes (Graham and McBride, 1979; Graham, 1982,1984,1985; Graham and Wilcox, 1983; Graham and Wedemayer, 1984; Graham and Taylor, 1986; Duckett and Renzaglia, 1988a; Delwiche et al., 1989; Vaughn et a f . ,1992). However, it must be stressed that the information for Riccia is based on a single species. The possible future discovery of the vestiges of a placenta elsewhere in the genus would be an unequivocal demonstration that the sporophyte of Riccia represents the end of a reduction series rather than an ancestral condition. The Metzgeriales are by far the most diverse group of liverworts and include several isolated entities whose affinities are highly problematic (Crandall-Stotler, 1981; Renzaglia, 1982; Schuster, 1984b; Brown and Lemmon, 1988; Carothers and Rushing, 1988). This diversity is almost certainly related to the extreme antiquity of the group, the fossils of which date back at least to the upper Devonian (Krassilov and Schuster, 1984). Although the wide range of placental morphologies further underlines the profound intersubordinal, interfamilial and even intergeneric discontinuities within the order, evaluation as to which of the variations represents Figs. 85 and 86. The gametophyte-sporophyte junction in Marchantiidae (cont.). Fig. 85. Reboulia hemisphaerica; more extensive wall ingrowths in the sporophyte. Fig. 86. Carrpos monocarpos; short wall protuberances in the gametophyte and normal chloroplasts in the placental cells of both generations.
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the primitive condition is at present highly speculative. Perhaps the most plausible choice is the condition found in Blasia and Fossombronia (wall labyrinths in both generations) in as much as these are generally considered to be representatives of very old isolated taxa (Schuster, 1984b). Starting from the condition found in such genera as Blasia and Fossombronia, variant types might have evolved through the suppression of transfer cells in either the gametophyte (Pallavicinia) or the sporophyte (Riccardia) or both (Pellia, Aneura and Cryptothallus). The similarity in placental organization between the Calobryales and putatively primitive members of the Metzgeriales is in accord with Schuster’s (1984b) notion of a common, albeit extremely remote, ancestry for these two groups. On the other hand the fact that putatively primitive members of the Metzgeriales share a similar placental organization with the Marchantiidae might be indicative of a closer phyletic relationship between simple and complex thalloid liverworts than between either group and the Jungermanniales. This possibility is substantiated by ontogenetic data (Crandall-Stotler, 1981) and is closely in line with recently recognized affinities between Blasia and Marchantiidae. Most notable of these are marchantialean-like spermatozoids (Renzaglia and Duckett, 1987a,b), the presence of two rows of ventral scales, the location of the archegonia, sporophyte development, apical organization (Renzaglia, 1982) and monoplastidic spore mother cells (Brown and Lemmon, 1992). However, it must be noted that, as long as the foot is considered to have different embryological origins in the Metzgeriales and Marchantiidae groups (see Section I.B), the placentas in these two groups cannot be considered homologous and therefore are not strictly comparable in the context of phylogeny. The Jungermanniales are given a near ancestral position in liverwort phylogeny by Schuster (1979, 1984b), a conclusion that appears supported by recent comparative analyses of spermatogenesis (Duckett et al. , 1982, 1984; Renzaglia and Duckett, 1991). In accord with these data, the jungermannialean placenta might be the ancestral type in liverworts. This possibility is supported by the striking similarity with the Andreaea-type in mosses. In addition to transfer cells only in the sporophyte, the Jungermanniales, Andreaeales, Takakiales and Polytrichales share a similar substructure in gametophyte placental cells, namely thickened tangential walls with radially arranged deposits of dense material. This perhaps suggests a closer phyletic relationship between the Andreaeales-Takakiales Figs. 87-90. The gametophyte-sporophyte junction in Marchantiidae (cont.). Fig. 87. Rebouliu hernisphuerica; plastids with fibrillar bundles (arrowed) parallel to the long axis in a gametophyte placental cell. Fig. 88. Reboulia; longitudinal section through membrane-bound bundles of tubules in a gametophyte placental cell. Fig. 89. Reboulia; transverse sections through membrane-bound bundles of tubules. Fig. 90. Riccia sorocurpa; light micrograph, longitudinal section of a sporophyte containing spore tetrads. The capsule is completely enclosed in the gametophyte thallus. The archegonial neck is arrowed.
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Figs. 91 and 92. The gametophyte-sporophyte junction in Marchantiidae; Riccia sorocarpa (cont.). Fig. 91. Section through the margin of a young sporophyte. C, two-layered calyptra; J , jacket and nurse cells; SMC, spore mother cell. Fig. 92. Section through the margin of a nearly mature sporophyte. Note the abundant lipid reserves in the spore tetrad (T), the collapsed inner layer of calyptra cells (arrowed) and the thickened walls of the thallus cells (G) facing the calyptra. Figs. 9>95. The gametophyte-sporophyte junction in Anthocerotes. Light micrographs, longitudinal sections. Fig. 93. Megaceros flagellark; ovoidal foot. Fig. 94. Anthoceros formosae: bulbous foot. Fig. 95. Notothylas temperata; smaller bulbous foot than Anthoceros.
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group and Jungermanniales than either the Marchantiidae or the Metzgeriales. This would imply a common origin for mosses and liverworts, from an ancestal form probably represented by an erect, radially symmetrical leafy gametophyte with terminal sporophytes. However, it should also be noted that the same distinctive wall substructure of dense radial bands also turns up in the sporophyte placental cells of Riccardia, a metzgerialean genus generally considered to be advanced (Schuster, 1984b), and in gametophyte placental cells of Sphagnum (Ligrone and Renzaglia, 1989). The possibility that this feature is merely associated with solute permeability rather than indicative of phyletic affinity should not be dismissed. In contrast to mosses and liverworts, the anthocerotes all exhibit the same, highly distinctive type of placenta, with minor variants mainly concerning plastid morphology and the presence, appearance and localization of protein deposits. This uniformity in placental organization emphasizes the homogeneity of this group and its separation from mosses and liverworts, as indicated by a wealth of anatomical, ultrastructural and developmental data (Crandall-Stotler, 1980, 1981, 1984; Duckett et a f . , 1982, 1984; Schuster, 1 9 8 4 ~ ;Carothers and Rushing, 1988; Duckett and Renzaglia, 1988a, 1989). The variations in placental morphology in anthocerotes appear to by very useful both for elucidating intergeneric affinities and for clarifying generic limits. The distinctive protein crystals found in Phaeoceros, Notothylas and Folioceros suggest close affinity between these genera. This contradicts the classification of anthocerotes recently proposed by Hasegawa (1988), where the family “Notothyladaceae”, comprising Notothyfas as the only genus, is separated from the family “Anthocerotaceae”, which includes Phaeoceros, Folioceros, Anthoceros and Megaceros. Recent ultrastructural studies of spermatozoid morphology and development have revealed close similarities between Phaeoceros and Notothyfus (Renzaglia and Duckett, 1988, 1989), although the lack of information on other genera presently precludes wider evaluation of the taxonomic relevance of male gamete microanatomy . The distinctive ultrastructural characteristics of the placenta in Dendroceros seemingly support the isolation of this genus in a separate taxonomical entity, e.g. the family Dendrocerotaceae as proposed by Hasegawa (1988).
IV. PTERIDOPHYTES By contrast to the wealth of comparative ultrastructural data on the gametophyte-sporophyte junction in bryophytes, knowledge of the embryology and the early stages in sporophyte differentiation in pteridophytes is limited exclusively to light microscope studies, the majority dating from the nineteenth century or the first half of the twentieth century and reiterated
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with little or no additional information in reviews and standard textbooks (Wardlaw, 1965; Bierhorst, 1971; Gifford and Foster, 1989). In these accounts it is usually tacitly assumed that the foot is the major site of exchange between gametophyte and sporophyte generations, but supporting experimental and or cytological data are lacking. More recent studies on the causal basis of the alternation of generations in pteridophytes (see reviews by Sheffield and Bell, 1987, 1989) have focused on the cytology of oogenesis and to a lesser extent on apospory and apogamy and do not consider the placental region. However, it is interesting to note that transfer cell morphology appears to be absent at the base of apogamous sporophytes in ferns whereas the cells initiating apogamous sporophytes in the moss Physcomitrium develop labyrinthine wall ingrowths even though a recognizable placenta is absent (Menon and Bell, 1981; La1 and Narang, 1985). Specific information on the placenta of pteridophytes is limited to a mention without micrographic details by Gunning and Pate (1974) of transfer cells in this region in Equisetum, two brief accounts of three ferns Polypodium, Adiantum (Gunning and Pate, 1969b) and Pteridium (Khatoon, 1986), and two very recent studies of Lycopodium (Peterson and Whittier, 1991; Duckett and Ligrone, 1992). Although these works clearly do not form a suitable basis for an incisive appraisal of the taxonomic and possible phylogenetic significance of the placenta in the different groups of pteridophytes and do not permit a comparison between these and other embryophytes, the fragmentary information they contain indicates a most fruitful area of enquiry for the future. In Polypodium and Adiantum wall ingrowths in both gametophyte and sporophyte develop very early, before the expansion of the first leaf, elongation of the root and differentiation of the first xylem: precisely the stage at which the sporophyte is most dependent on the gametophyte for nutrients (Gunning and Pate, 1969b). The ingrowths are more abundant and labyrinthine in the sporophyte in Adiantum and Pteridium, while the opposite occurs in Polypodium. The ingrowths are more highly developed on the tangential walls along the interface but also extend onto the lateral walls in the sporophytic cells in Adiantum and Polypodium. The sporophytic cells, but not those of the gametophyte, contain abundant starch, a situation probably reflecting sugar translocation from the gametophyte to the sporophyte. Unlike mosses and liverworts, where a clear-cut demarcation zone is generally interposed between the sporophyte and gametophyte, in ferns the Figs. 96-9X. The garnetophyte-sporophyte junction in Anthocerotes (cont.). Fig. 96. Dendroceros tubercularis; gametophyte transfer cells and sporophyte haustorial cells. Note the chloroplasts in the former. Fig. 97. Dendroceros tubercularis; branched sporophyte haustorial cell. Note the undifferentiated plastids. Fig. 98. Megacerosjfagellaris;undifferentiated plastids in a sporophyte haustorial cell and crystals (arrowed) in the adjacent garnetophyte cell.
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Figs. 99 and 100. The gametophyte-sporophyte junction in Anthocerotes (cont.). Fig. 99. Phaeoceros luevis; gametophyte transfer cells, sporophyte haustorial cells and placental lacunae (arrowed). Fig. 100. Dendroceros tuberculuris; plastid in a gametophyte transfer cell.
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cells of the two generations interdigitate and mucilage-containing intraplacental species appear to be lacking. Further differences between bryophytes on the one hand and ferns and Lycopodium (see below) on the other are an absence of dead and collapsed cells along the interface and the lack of any evidence for the renewal of the placental cells. These differences are perhaps related to the transient nature of sporophytic dependence on the gametophyte in pteridophytes. Intercellular spaces are lacking in the placental region of Lycopodium uppressum (Chapm.) Lloyd & Underw: the cells of the two generations lie close together or are separated by electron-dense intercellular material (Peterson and Whittier, 1991). As in bryophytes and seed plants (see Section V), symplastic isolation, initially established during the early stages in the differentiation of the axial row in the young archegonium (Bell, 1989), characterize all stages of sporophyte development in pteridophytes. In the foot region of Lycopodium uppressum there is little or no interdigitation of the cells of the two generations and the contiguous walls of both sporophyte and gametophyte develop coarse labyrinthine ingrowths of low electron opacity very similar ultrastructurally to those in the marchantialean placenta. Subsequently the interstices become occluded by dense amorphous wall material. The sporophyte-gametophyte junction in Lycopodium cernuum L. is somewhat different. Here the interface between the two generations, which develops ingrowths but to a more limited extent than in L. uppressurn, is not a special lateral development of the early embryo (i.e. a foot region) as in other species of Lycopodium (Goebel, 1905), but rather the lower part of the primary embryonic axis derived from the suspensor (Duckett and Ligrone, 1992). The homologue of the foot in L. cernuum, in terms of its lateral position and early appearance in sporophyte differentiation, is the protocorm. This juvenile structure lies outside the confines of the parent gametophyte and presumably derives its nutrition partly from photosynthesis and partly from an endophytic fungus. Of particular interest in the present context is that within the protocorm there develop schizogenous, mucilage-filled intercellular spaces closely similar to those in the placental region of bryophytes. These lacunae are the principal habitat of the mycobiont. Although the protocorm cells do not develop wall ingrowths, their invasion by the fungus is associated with the production of massive overgrowths of host cell wall material with a texture similar to that forming the wall thickenings in the gametophytic placental cells of Sphagnum and Jungermanniales. The major differences between the sporophyte-gametophyte junction in two species of Lycopodium on the one hand reflect the considerable antiquity of this genus, and on the other perhaps anticipate diversity in placental morphology in pteridophytes parallelling that in bryophytes. It will now be particularly interesting to discover whether wall ingrowths are also present
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along the margins of the well-developed suspensor present in many species of Selaginellu (Bierhorst, 1971) and to investigate the position and sites of nutrient exchange between gametophyte and sporophyte in the haustorialike foot region of Tmesipferis (Holloway, 1918).
V. SEED PLANTS The classic reviews on transfer cells (Gunning and Pate, 1969a, 1974; Pate and Gunning, 1972; Gunning, 1977) underline the cytoplasmic discontinuities between sporophyte and megagametophyte, between embryo and megagametophyte and between sporophyte and developing microspores (also see Charzynska et al., 1990; Murgia ef al., 1991; Pacini, 1990 for discussion of structural and functional interrelationships between tapetum and microspores) as posing special problems for the transport of solutes. Gunning and Pate go on to point out that, in view of the complex nutritional relationships, plus the fact that the new gametophyte and sporophyte are both parasitic on the parent sporophyte, it is not surprising to find transfer cells in these situations. Indeed, transfer cell morphology has now been described at virtually every site of probable solute exchange via the apoplast in the female reproductive organs of angiosperms (Table VII). In a few situations the zones of transfer cells face each other along the intergenerational apoplastic gap, but more commonly only the receptor surface bears the ingrowths. Sometimes the boundary between the two generations is a common wall lacking plasmodesmata, but more often these are separated by a space containing remains of dead or dying cells. The diverse locations and temporal differences in the development of wall ingrowths during the ontogeny of the various tissues provide perhaps the strongest circumstantial evidence of transfer cell activity in solute transport. As in the placentas of most bryophytes and pteridophytes, it seems to be an anatomical necessity that nutrients directed to the growing sporophyte have to pass through cells with wall ingrowths. Rather than reiterate the substance of the earlier reviews, this account focuses on some of the more significant discoveries since 1977, compares the present stage of knowledge of the gametophyte-sporophyte junction in seed plants with that in bryophytes and pteridophytes and points to areas urgently needing further study. As in bryophytes, in seed plants there are also virtually no physiological data to validate inferences about routes and timing of solute transport based almost entirely on the formation of wall labyrinths. It is, however, Figs. 101 and 102. The gametophyte-sporophyte junction in Anthocerotes (cont.). Fig. 101. Notothylus orbicularis; sporophyte haustorial cells and gametophyte transfer cells. Fig. 102. Phoeoceros carolinianus; mitochondria1 aggregates and a pleornorphic plastid in a gametophyte transfer cell. A small pyrenoid is arrowed.
TABLE VII Occurrence and likely functions of transfer cells in the female reproductive organs of angiosperms. Modified and updated from Pate and Gunning (1972) and Gunning (1977) Organ or tissue
Embryo sac
Young embryo
Location
Probable function
Distribution
Recent references"
Egg cell, micropylar walls
Functions of synergids taken over by egg cell when synergids absent
Plumbag0
2,7,24
Antipodals, chalazal walls Synergids, micropylar walls The so-called filiform apparatus
Nutrition of embryo sac
Several genera
1,10,24
Nutrition of embryo sac
Several genera
Central cell, outer walls at micropylar pole chalazal region
Nutrition of embryo sac
Glycine, Scilla, Helianthus
5,6,7,16,17,23,26
Suspensor. outer walls
Nutrition of young embryo Nutrition of young embryo
Several genera
4,5,12,13,18,27
AIisma
3
Basal cell at micropylar pole
Chemotropic secretion, guidance of pollen tube
1,4,7,8,9,13,14, 15,19,20,24
Older embryo Nucellus Endosperm
Cotyledon epidermis, outer walls Epidermis near base of embryo Inner and outer faces Outer walls facing perisperm Aleurone, outer face
Integument
Inner face of inner
Nutrition of embryo
Some Leguminosae
21
Nutrition of embryo
Glycine, Triticum
5.22
Nutrition of embryo
Some Leguminosae and Cruciferae Mesern bryunthemuni
10,11,12
Nutrition of embryo Nutrition of embryo Facilitating viviparous germination and possibly salt exclusion Transfer to endosperm andlor embryo
21
Caryopses of Gramineae Rhizophoru
21
Some Leguminosae,
5
Glycine
25
"References: 1. Bhandari and Sachdeva (1983); 2. Bing-Quan Huang et al. (1990); 3, Bohdanowicz (1987): 4, Dute el al. (1989); 5 , Folsom and Cass (1986); 6. Folsom and Petersen (1984); 7. Kapil and Bhatnagar (1981); 8, Kennell and Horner (1985a); 9. Kennell and Horner (1985b); 10, Mansfield and Briarty (1990a); 11, Mansfield and Briarty (l990b); 12. Mansfield and Briarty (1991); 13. Mansfield er al. (1991); 14. Mogensen (1972); 15, Mogensen and Suthar (1979); 16, Newcomb (l973a); 17, Newcomb (l973b); 18, Newcomb and Fowke (1974); 19, Newcomb and Steeves (1971); 20, Olsen (1991); 21, Pate and Gunning (1972); 22, Smart and O'Brien (1983); 23, Tilton efal. (1984); 24. Willemse and Van Went (1984); 25, Wise and Juncosa (1989); 26, Yan eral. (1991); 27. Yeung and Clutter (1979).
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noteworthy that maize somatic embryos and embryos developing in vitro (Schel and Kieft, 1986; Fransz and Schel, 1991) appear to lack transfer cells. In Phoenix dactylifera L . differences in the acid phosphatases suggest that phosphate metabolism in the endosperm is independent of that in the cotyledon haustorium, and that acid phosphatases for endosperm phosphate metabolism are not secreted by the embryo nor by the cotyledon haustorium, but instead are stored in the endosperm (Sekhar and De Mason, 1989). There is now a pressing need to identify the specific nature of the metabolites undergoing import into young embryos via the various transfer cell zones (Table VII). Although relating to only two stages in development, the wealth of comparative information on the placenta in bryophytes forms the basis for wide-ranging taxonomic inferences. In angiosperms, by contrast, the situation is very different. A few very detailed developmental studies on a small number of genera, particularly Arabidopsis (Mansfield et a f . , 1991; Mansfield and Briarty, 1991), Capsefla (Schultz and Jensen, 1968a,b, 1969, 1971), Gfycine(Kennel1 and Horner, 1985a,b; Folsom and Cass, 1986; Dute et al., 1989) and Helianthus (Newcomb and Steeves, 1971; Newcomb, 1973a,b; Yan et al., 1991), reveal major differences in the extent and distribution of the wall ingrowths even between closely related genera. These relate partly to different patterns of embryo development and partly to differences in the location of seed storage reserves (e.g. cotyledons, perisperm or endosperm). Only one author (Mikeswell, 1990) attempts comparisons from a taxonomic standpoint. Mikeswell’s (1990) extensive survey of angiosperm families indicates that the differentiation of micropylar and chalaza1 haustoria from embryo sacs or endosperm is primarily confined to sympetalous plants with cellular endosperm and anatropous, unitegmic and tenuinucellate ovules. The presence of endosperm haustoria characterizes the subclass Asteridae, which includes the Plantaginales. The Plantaginaceae seems well aligned with families within the Scrophulariales. Mikeswell’s final conclusion, that the utilization of haustoria as an important embryological character in taxonomy would seem to be warranted, suggests the same could well be true for other transfer cell locations when data are available for more taxa. Ultrastructurally the vast majority of the wall ingrowths associated with the female reproductive tissues in angiosperms are coarse with a transparent matrix like those in the Marchantiidae. However, in rare instances, e.g. the suspensor of Gfycine(Dute et a f . ,1989) they are finer and electron-dense. A highly elaborate wall labyrinth occurs in the large basal cell of the suspensor Figs. 10>10h. The gametophyte-sporophyte junction in Anthocerotes (cont.). Crystals. Fig. 103. Folioceros fuciformis; intercellular. Fig. 104. Phaeoceros luevis; intercellular crystals after digestion with pepsin. Fig. 105. Nofothylasorbicularis; intercellular. Fig. 106. Folioceros fuciforrnis; intracellular.
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of Afisma (Bohdanowicz, 1987).Thepresence of wall ingrowths is associated with cytoplasmic organization typical of transfer cells, namely abundant ribosomes, rough E R and numerous mitochondria. Very large megamitochondria have been described in young embryos of Capseffa(Schultz and Jensen, 1973) and Arabidopsis (Mansfield and Briarty, 1991). It is suggested that these may act as a reservoir for mitochondria1 DNA in relation to the rapid proliferation of mitochondria during embryo development. Although the cells along the gametophyte-sporophyte junction in angiosperms typically contain undifferentiated pleomorphic leucoplasts, with few reserve materials and rudimentary thylakoid systems, some highly unusual forms have also been described. Large plastoglobuli and prolamellar bodies characterize the endosperm plastids in Rhizophora (Wise and Juncosa, 1989). Prolamellar bodies also occur in the so-called “placental haustorium” plastids of Tropaeolum (Nagl and Kuhner, 1976). The suspensor by contrast contains plastids with an extremely dense stroma and scattered membranous vesicles. Much larger plastids with similar contents occur in the suspensor of Stelfaria (Newcomb and Fowke, 1974). Plastid tubules have been noted in the suspensors of Phaseolus and Pisum (Marinos 1970; Schnepf and Nagl, 1970). The current state of knowledge of the gametophyte-sporophyte interface in the gymnosperms is very similar to that for pteridophytes. In contrast to angiosperms, attempts to induce normal development of conifer zygotes and precotyledonary embryos in vitro have been unsuccessful (Gates and Greenwood, 1991, and literature cited therein) suggesting that a unique nutritional environment, probably involving continual variations in the physiological and chemical conditions, is required for embryo development. Although the considerable complexities of embryo development in gymnosperms are well documented at the light microscope level (Wardlaw, 1965), these have been totally ignored by electron microscopists. As far as we are aware the only report of wall ingrowths is in the basal plate wall between the oosphere cytoplasm and proembryo in Pinus (Gunning, 1977). For the future it would be interesting to discover whether or not ultrastructural differences between proembryos and embryos characterize the Gnetales, Cycads, Ginkgo and different families in the Coniferales in the same way that placental differences separate different groups of bryophytes.
ACKNOWLEDGEMENTS This review was made possible by a NATO Collaborative Grant to J . G . Duckett and K. S. Renzaglia and by a Guest Research Fellowship from the Royal Society of London enabling R. Ligrone to work at Queen Mary and Westfield College during 1989 and 1990. This financial support is most gratefully acknowledged. Collection of the specimens of Pogonatum neessii,
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Herberta spp. Zoopsis liukiuensis, Pallavicinia indica, Calobryum blumei, Dumortiera hirsuta, Folioceros fuciformis, Dendroceros javanicus and D. tubercularis used in this study was made possible by a travel grant to J. G. Duckett from the Royal Society of London and by laboratory facilities arranged by Drs M. A . H. Mohamed and A. Nasrulhaq-Boyce in the Botany Department of the University of Malaya, Kuala Lumpur. Cladophascum gymnomitrioides was collected in Lesotho by J. G. Duckett under a British Council LINK between Queen Mary and Westfield College and the National University of Lesotho. The authors also thank D. K. Smith for providing live specimens of Takakia and R. C. Brown and B.E. Lemmon for allowing the use of their embedded material of Carrpos and Monoclea.
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ROBERTO LIGRONE Dipartimento di Biologiu Vegetule, Universita di Napoli, Viu Foria 223, 1-80139 Nupoli, Italy JEFFREY G. DUCKETT School of Biological Sciences, Queen Mary and Westjield College, University of London, Mile End Road, London E l 4 N S , U K
and KAREN S. RENZAGLIA School of Biological Sciences, Box 23590A, East Tennessee State University, Johnson City, TN 37614, USA
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Introduction
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The Taxonomic Significance of the Placenta in Bryophytes and Implications for Phylogeny . . . . . . . . . . . . . . . .
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Seedplants . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . .
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Bryophytes . . . . . . . . . . . . . A. Mosses (Bryopsida) . . . . . . B. Liverworts (Hepatopsida) . . . C. Anthocerotes (Anthocerotopsida)
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I. INTRODUCTION The life-cycle of land plants characteristically involves an embryonic phase during which the sporophyte is associated with the parental gametophyte and has no direct contact with the substratum (Graham, 1985; Duckett and Renzaglia, 1988a). This phase is very short in lower tracheophytes, where the young sporophyte rapidly breaks free from the confines of the gametophyte and develops a root and an aerial photosynthetic system, thus becoming independent. Likewise, seed plants have a relatively short embryonic phase that terminates with seed germination after a dormant period of variable duration. By contrast, the sporophyte of bryophytes is permanently associated with the gametophyte and therefore retains structural if not functional dependence on the latter throughout its life-span. During development the embryo utilizes conspicuous amounts of organic compounds for growth and respiration. Moreover, in most cases, the embryo accumulates abundant reserves, mostly in the form of starch, proteins and lipids, that are utilized later in development. It is widely maintained that the bulk of these substances are of exogenous origin, the embryo being barely able to produce them autonomously. There is abundant evidence from physiological studies (Proctor, 1977; Courtice et a [ . , 1978;Thomas et af.,1978,1979; Browning and Gunning, 1979a,b,c; Caussin et a f . , 1983; Renault et al., 1989) that the sporophyte of bryophytes needs organic nutrients from the gametophyte for normal growth and development, although it contains chlorophyll and, notably in mosses and anthocerotes, may have well-organized photosynthetic tissues (Duckett and Renzaglia, 1988b). The same is presumably true for the embryos of pteridophytes, although no direct evidence is presently available (DeMaggio, 1963; Sheffield and Bell, 1987; Bell, 1989). The situation is more complex in seed plants, as here the reduced gametophyte grows and is fertilized within the parental sporophyte. The embryo is nourished by the gametophyte for a short time, thereafter it starts taking up nutrients directly from the old sporophyte. The dependence of the embryo on exogenously supplied nutrients is reflected by a series of morphological specializations that presumably serve to facilitate nutrient translocation. In bryophytes and most pteridophytes the embryo forms a basal or lateral organ, the foot, that penetrates the gametophyte tissue and is thought to be active in nutrient uptake. In addition, pteridophytes and seed plants possess a suspensor that orientates and keeps the embryo in intimate contact with the nutritive tissue of the gametophyte (Gifford and Foster, 1989). The suspensor is generally small and short-lived in pteridophytes. Conversely, the embryo of seed plants has a relatively large and long-lived suspensor but never forms a foot (Wardlaw, 1965; Gifford and Foster, 1989). At very early stages in development the
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embryo of mosses and most liverworts forms a suspensor-like basal structure. Most frequently this consists of one or few cells and collapses with the subsequent development of the foot. The interface between the sporophyte foot and parental gametophyte in bryophytes and pteridophytes is commonly referred to as the placenta (Pate and Gunning, 1972; Gunning and Pate, 1974; Ligrone and Gambardella, 1988a,b). Generally placental cells have dense cytoplasm rich in mitochondria, endoplasmic reticulum and ribosomes. Most frequently they present a wall-membrane apparatus typical of transfer cells (Pate and Gunning, 1972; Gunning and Pate, 1974). A true placenta is lacking in seed plants, as the embryo does not form a foot, but transfer cells may be found in several different sites such as the interface between the gametophyte and its parental sporophyte, as well as in the suspensor, cotyledons, endosperm and integumentary endothelium (Gunning and Pate, 1969a, 1974; Pate and Gunning, 1972; Gunning, 1977). The formation of an embryo has been widely recognized as one of the most distinctive features of land plants, unknown in chlorophyll a bcontaining algae, with the possible exception of Coleochaete (Graham et al., 1991). Red algae are the only other group in which post-fertilization development may produce an intercalated multicellular diploid phase, the carposporophyte, that remains associated with the gametophyte by means of highly specialized placental structures (Bold and Wynne, 1985). There is no doubt, however, that red algae and land plants have but a very remote common ancestry and similarities in their life-cycles must be due to parallel evolution. The term embryophytes for land plants has therefore received increasing favour in the last years (Mishler and Churchill, 1984, 1985; Bremer, 1985; Crane, 1985; Bremer et al., 1987), although it is still debated whether, in a cladistic context, embryophytes may be considered a monophyletic group (Sluiman, 1985). The placenta has a critical role in the life-cycle of land plants as it connects and integrates two organisms subject to different environmental and genetic constraints. Regardless of whether the land plant sporophyte and its nutritional and developmental association with the gametophyte originated de novo, through a delay in zygotic meiosis (Bower, 1908), or secondarily from a free-living organism (Fritsch, 1945), one of the very first steps must have been the evolution of a placental tissue. Since then the placenta has been evolving over millions of years under the selective pressures that have produced all the extant, and extinct, groups of land plants. This review presents a comparative analysis of the placenta in land plants, including the first detailed systematic survey of bryophytes encompassing several groups not studied before, together with comments on pteridophytes, where comparative data are virtually non-existent, and on placental analogues in seed plants. Far from exhaustive, this is primarily an attempt to
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draw the attention of plant morphologists, physiologists and taxonomists to a topic of considerable relevance to the phylogeny, taxonomy and functional biology of land plants.
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BRYOPHYTES
The bryophytes present a particularly conspicuous placental region, probably as a consequence of the inability of their sporophyte to become autonomous. The nutrient relationships of the two generations have been reviewed recently (Ligrone and Gambardella, 1988a) and will not be discussed in detail here. Ultrastructural studies performed in recent years have revealed remarkable diversity in the organization of the placenta (Ligrone and Gambardella, 1988b). Unfortunately, the paucity of comparative data and in particular a complete absence of information for several major groups, notably the Andreaeidae and Tetraphidales among the mosses and the Jungermanniales and Metzgeriales among the liverworts, have hitherto prevented any wide-ranging conclusions. The most clear-cut feature that distinguishes the sporophytegametophyte junction in different bryophyte groups is the presence or absence of wall labyrinths in the placental cells of each generation (Tables I, I11 and V). Further distinctive attributes are the cell wall structure, notably the shape and arrangement of wall ingrowths, and certain cytoplasmic features of placental cells such as plastid morphology (Tables 11, IV and VI). Some of these characteristics may undergo changes during sporophyte development. For example, in mature sporophytes the wall labyrinth of placental transfer cells is partially or completely obliterated by deposition of new wall material (Browning and Gunning, 1979a; Gambardella, 1987; Gambardella and Ligrone, 1987). It is therefore important that different developmental stages be examined and corresponding stages be considered when comparing different species or groups. This is not an easy task; the sporophytes develop at different times of the year, according to the species, and in liverworts the phase of active sporophyte growth is usually very short. Moreover, attempts to obtain sporophytes under laboratory conditions have been successful only in a very limited number of species. In this account two main stages of sporophyte development are distinguished. Stage 1, pre-meiotic, is characterized by proliferative activity in the sporangial tissue. Stage 2, post-meiotic, is characterized by the presence of maturing spores in the still intact sporangium. The highest demand for exogenous nutrients by the sporophyte, presumably associated with maximum activity of the placenta, has been observed during the first stage of development (Proctor, 1977; Browning and Gunning, 1979b). When not otherwise indicated, the ultrastructural observations reported here refer to that stage. The new information presented in this review encompasses 17 species of mosses, 26 of liverworts and 9 of anthocerotes, with representatives from all the major orders of bryophytes (Tables I-VI).
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Nomenclature for genera and species follows Corley et a f .(1981) for mosses, Grolle (1983) for liverworts, and Stotler and Crandall-Stotler (1977) or Hasegawa (1988) for anthocerotes. A. MOSSES (Bryopsida)
The first division of the zygote within the archegonium is transverse and produces an upper, epibasal cell and a lower, hypobasal cell. According to Roth (1969), in all mosses, except Sphagnum, the epibasal cell generates an elongate flattened embryo with a lenticular apical cell, whereas the hypobasal cell undergoes a few randomly orientated divisions producing a small mass of cells. Subsequently the embryo forms an intercalary meristem which is responsible for the development basipetally of the foot and the lowermost part of the seta, whereas cells differentiating acropetally from the meristem produce the upper seta and the capsule base (Crandall-Stotler, 1984). In Sphagnum the embryo does not form an intercalary meristem. As a consequence, the seta is lacking and the foot is entirely derived from the activity of the hypobasal cell (Roth, 1969). In some bryalean genera, e.g. Archidium and Ephemerum (Crandall-Stotler, 1984), the seta meristem is functional for only a few division cycles and consequently a very small foot and short seta are developed. In most cases the hypobasally derived cells usually degenerate at an early stage of sporophyte development and either disappear or in a few moss genera (Table I) form a small necrotic appendage visible at the tip of the foot (Roth, 1969; HCbant, 1975; Ligrone and Gambardella, 1988a). 1 . Andreaeidae This subclass consists of the genus Andreaea, with 50 to 100 species (Schultze-Motel, 1970), and the recently described genus Andreaeobryum, represented by the single species A . macrosporum (Steere and Murray, 1976; Murray, 1988). Anatomical characteristics of recently discovered antheridia and sporophytes of Takakia (Davison et a f . , 1989; Mcfarland et a f . , 1989; Smith, 1990) indicate that this is a primitive moss with clear relationships with the Andreaeidae, rather than a liverwort. For this reason the placental organization of Takakia is discussed in this section. The sporophyte of Andreaea consists of a capsule, a very short seta and a conical foot (Fig. 1). After fertilization the archegonial stalk proliferates to form a parenchymatous tissue surrounding the foot. Following spore maturation the sporophyte is elevated by a pseudopodium, formed by elongation of archegonial and stem cells (Roth, 1969; Murray, 1988). The foot has a parenchymatous structure, with no trace of conducting tissue. The internal cells contain abundant lipid reserves in the form of osmiophilic droplets of varying size (Fig. 2 ) . The epidermal cells are slightly larger and have denser cytoplasm with numerous evenly scattered vacuoles of small sizes (Fig. 3). In the lower part of the foot the epidermal cells exhibit prominent wall labyrinths along their outer tangential walls (Fig. 3).
TABLE I Characteristic features of the placenta in mosses Distribution of transfer cells
Distribution of wall ingrowths
Reference' Sporophyte Gametophyte
ANDREAEIDAE Tolioloo rcrorophyllo Andreoco rupmrrk Hedw Andreoeo rorhii Web. & Mohr Andreuobryum marrosponm Sleeve & B. Murr. SPHAGNmAE Sphagnumfmbnarum Wik. Sphagnum fdlaKlinggr. Sphagnum subnitow Rws & warnst. Sphagnum curprdotum Ehrh.
Sporophyte
Gametophpe
Time of ingmwih development
lngrowth morphology
Sporophyte Gametophyte Sporophytc Gametophyte Conducting Foot shape tissue in
16
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1
+
1 15
11 11
+ +
NIA
Early
NIA
Single layer outer tang.
NIA
Early
NIA
NIA
Early
N/A
NIA
NIA
NIA
NIA
Early
NIA
walls
Smgle layer 0"ter tang. walls
Labyrinth. NIA Labynnth. coarse NIA
}
fwt
Hydroids
-
coarse
?
NIA
7
i"P
NIA
Sporophyte
Slightly elongate
Gametophyte
l h c k . nameous
+ thin areas with plasmodesmara
Thick
7
Tlick and thin
areas with plasmodesmata
~
BRYIDAE Polytrichales Polyrnchum formmum Hedw. Polynchum commune Hedw Polynrchum pil$e..n Hedw Dowoni? superb0 Grev. Dendroltgornchumdcndrordrs
13 13 14
+
+ +
outer tang walls
2-3 inner cell layen
Broth. Pogonoaun dordes P.Beauv Pqonomm neesii (C.MuU.)
10 I
Dozy Olrgontchum hercrnicum Lam.
1
+ + + + +
Atrichurn undulorum P.
1
+
1
+
Outer tang. walls 4
Single layer outer tang
&Dc
Beau".
Tetraphidales
TeonphLs pellucidn Hedw
7 7
Labynnth, NIA coarse
Hydroids. leptoidr
Elongate
tapertog
cells
Single layer thick-
walled cells
loner tang walls
Labyrinth. Shon. coarse Hydroidr
Elongate tapering
Early
Labynnth
Early
Labyrmth
Elongate tapenng
Early
Early
Early Early
maw
Bryales
Bmbaumiinsae
BuxboumiapzpenBest
12
+
Diphwrumfoliorum Mohr.
1
I
Single layer thckwalled cells
Several layem thick-walled
lateral in middle
Walk
Inner tang. walls t outer cell layers
less
eXte"Sl"e
Labyrinth, fine Labyrinth. coarse
Hydroids
Elongate parenchyma
Collapsed
cells at
foot up
Elongate
~
1
1
I
s,ngle layer O"k* 1ang.b walls
Other wall features
Archidiiicae rmerrimm Min.
Archi&--
2
+
+
1
+
+
1
+
1
+
1
outer tang. walls.
Inner tang walls
Single layer cuter tang. Walls
lnncr tang walls t outer aU layers
Early
-
single layer outer tang.
NIA
Ealy
+
Single layer outer tang.
Inner tang. walls + outer cell layers
Earl?
+
+
Single layer OUter tang
Inner tang. walls + 0"kr cell lavers
Early
1
+
f
Single layer O U t a tang
Inner tang. walls + 0)utercell layers
Early
I2
+
+
Single layer outer tang
inner rang. walls f outer cell layers
Early
4
i
+
Single layer outer tang
Inner tang. W a l k + outer cell layers
Early
Outer tang. walls t Inner cells layers Outer tang. walk inner cell layers
Inner tang walls
Early
Inner tang. walls
Early
Single layer uuter Img
Inner tang. W d I * + ""tcrlrrll layers
Fsrl)
Single laycr outer tanp walls
Inner Idag Wdll. +
Early
Smgic laycr outcr tang.
waur Slnglc layer OUlCT tanp.
Inner 1img. Willlb + OuterlwU b y m Inner t ~ g wila .
rjrly
Slnglc layer outer lung. w . 1
lnncr tang. walls I ""trr ccu lilyerr
Early
lnncr tang walk I
Earl)
Dicranineae
Laxobryum glnucum Angstr.
W&
waus
walls
waus
waus
W2.b
17
t
f
9
+
+
5. x
t
4
10
I
I
1
+
wall.
+
1
h
t
I
+
I
I
10
t
+ +
walls
BUlbOUS
""tcrccll lnycrr
+
outcrccll layerr
€ally
f
Labyrinlh. hbyrinth
murc
Hvnnincnc
.
.-
long.
.
""1crICcII 1aycrr
10
"References. I , DEW; 2, Brown and L e m o n (1985); 3, Browningand Gunning (1979a); 4, Chauhan (1990); 5. Chauhan and Lal (lWgl), 6. Ejm6 and Suirc (lW7): 7. HCbant (19751.8.La1 and Chauhan (1981):9. La1 and Narang (1985); 10, Ligrone and Cambardella (19a8a); 11. Ligrane and Renzaglia (1989);12. Ligrone el d.(1982b); 13. Maier (1%7): Maier and Maicr (1972); 15. Murray 11988); 16. Remagha d nl (1991);17. WrncLe and %hulr (1975). btang = tangential.
TABLE I1 Cytoplasmic features of the nlacental cells in mosses Plastids Sporophyte Shape ANDREAEIDAE Takakia cerarophylla Andreaea rupestris Andreaea rothii Andreaeobryum macrosporum
[
?
SPHAGNIDAE Sphagnum fimbriatum Sphagnum fallax Sphagnum subnirens
Sphagnum curpidatum
Elongate Ovoid
Membrane system
{
?
Pleomorphic p.r
Plastoglohuli Starch
++
1.g.
r.gr.
Gametophyte
{
++ ? +
I
{
-
{
11 -
Shape
Membrane system
Pleomorphic
r.gr.
Ovoid
r.gr.
{
?
?
?
-
Ovoid
n.gr.
Ovoid
n.gr. p.r.
Cytoplasmic lipid droplets
Plastoglobuli
Starch
+++
++
?
{
-I ?
Sporophyte
Gametophyte
++
+ ++
++ ?
{
+I -1
BRYIDAE
?
-
I
Polytrichales Polyrrichum formosum Polyrrichum commune Polyrrichum piliferum Dowsonia superba Dendroligotrichum dendroides Pogonarum aloides Pogonafum neesii Oligorrichum hercinicum Atrichum undulatum
Pleomorphic r.gr. p.r.
Tetraphidalcs Tetraphis pellucida
Ovoid
Bryales Buxbaumiincae Buxbaumia piperi Diphyscium foliosum
Pleomorphic p.1. Pleomorphic m.gr.
+
-
-
I Plcomorphi
+
+I-
++
+I+]
?
++
+
Ovoid
n.gr.
+ + -
-
Pleomorphic
r.gr.
t
-
Sphcroidal Spheroidal
pr0.b. Irregular
-
+
~
+
-
+
+
-
Archidiineae Archidium tenerrimiim
Pleomorphic
m.gr.
+
-
Spheroidal
r.gr.
Dicranineae Leucohryum glaucum Dicranum majus Blindia acura Cladophascum gymnomitrioides
Pleomorphic Pleomorphic Pleomorphic Pleomorphic
p.r. m.gr. m.gr. m.gr.
+
-
Spheroidal Spheroidal Spheroidal Spheroidal
r.gr.
-
r.gr. n.gr. r.gr.
-
Fissidentineae Fissidens crassipes
Pleomorphic
r.gr.+ p.r.
Pleomorphic
n.gr.
+
Pottiineae Timmiella harhuloides Phascum cuspidarum
Pleomorphic Pleomorphic
m.gr. r.gr.
+ +
-
Spheroidal Spheroidal
r.gr. r.gr.
Pleomorphic
n.gr. +p.r.
+
-
Pleomorphic
r.gr.
Funariineae Funaria hygromerrica Physcomifriumcoorgense Physcomirrium cyathicarpurn
1
Pleomorphij n.gr.
Bryincae Bryum capillore
Pleomorphic
Aulacomniurn palusrre Plagiomnium cuspidaturn Mnium hornurn
Ovoid Pleomorphic Pleomorphic
r.gr. + p.r. m.gr. m.gr. m.gr.
Leucodontineae Neckera crispa
Pleomorphic
p.r.
Hypnincae Brachvfhecium vehtinum Isopterygium pulchellutn
Pleomorphic Pleomorphic
p.r.
p.r.
+ -
+
}
+
1
+
}
Pleomorphicl r.gr.
-
-
+
}
+ +
++ + + +
+ + + +
+ + +
+
-
+
+
+ -
+
-
-
-
-
1 1
+
}
+
-
-
Spheroidal
r.gr.
-
+
+
-
Pleomorphic Plcomorphic Spheroidal
r.gr.
n.gr.
+ + +
+ + ++
Spheroidal
r.gr.
+
+
-
-
Spheroidal Spheroidal Elongate
r.gr. r.gr.
+
+
+ +
-
-
-
+
-
-
-
-
r.gr.+ p.r.
+
+
Abbreviations: m.gr., massive grana; n.gr., normal grana, like those in leaves; r.gr., rudimentary grana, 2-3 thylakoids only; pro.b., prolamellar body; p.r.. peripheral reticulum.
240
R. LIGRONE et a/.
Figs. 1-4. The gametophyte-sporophyte junction in Andreaea rothii. Fig. 1. Light micrograph, longitudinal section, showing the conical foot and the absence of conducting tissues in the short seta. Fig. 2. The foot parenchyma cells contain abundant lipid droplets. Fig. 3. Wall labyrinths along the outer tangential walls of sporophyte placental cells. Fig. 4. Gametophyte placental cells with irregular wall thickenings (arrowed). Key to abbreviations used on figures: F, foot; G , gametophyte; H , hydroids; M, mitochondria; N, nucleus; P, plastids; S, sporophyte; SE, seta.
The gametophytic cells surrounding the foot also have dense cytoplasm rich in organelles, notably mitochondria. As in all the other mosses examined in this study, these tend to be larger than those in the foot cells. The gametophyte placental cells do not form wall ingrowths but present thickened wall areas with a loose fibrillar texture, interrupted by thinner areas crossed by plasmodesmata (Fig. 4).
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
24 1
Both sporophyte and gametophyte placental cells contain numerous small plastids with a rudimentary thylakoid system and are rich in plastoglobuli. Ultrastructural details of the placenta in Andreaeobryum have yet to be described. However, major morphological differences between Andreaea and Andreaeobryurn include the presence in the latter of a well-developed seta and a “bryoid” foot deeply penetrating the gametophyte tissue, which does not form a pseudopodium (Murray, 1988). Placental transfer cells are restricted to the sporophyte (Murray, 1988). The foot of Takakia is closely similar to that of Andreaeobryum (Renzaglia et al., 1992). This elongated tapering structure (Fig. 5 ) penetrates deeply into the broadened central conducting strand of the gametophyte stem. The inner foot region comprises a broad strand of hydroids extending lengthwise in the seta, but leptoids are absent. The epidermal cells of the foot exhibit well-developed wall ingrowths on their outer tangential walls (Fig. 6). Their dense cytoplasm contains abundant mitochondria, lipid droplets and elongated plastids with rudimentary grana and numerous plastoglobuli (Fig. 6). Starch grains are absent from the sporophyte placental cells but are common in the adjacent tissues, especially the cortex of the foot and gametophyte. Transfer cells are absent in the gametophyte placental cells. These have irregularly thickened walls lined with conspicuous deposits of electron-transparent material (Fig. 7).
2. Sphagnidae This subclass consists of the single genus Sphagnum, with 100 species. The sporophyte of Sphagnum lacks a distinct seta and develops at the apex of specialized gametophytic branches that elongate after spore maturation to form a pseudopodium (Roth, 1969). The foot is bulbous and parenchymatous (Fig. 8). An ultrastructural investigation of the placenta of Sphagnum jimbriatum and S . fallax at stage 2 of sporophyte development revealed that transfer cells were lacking in both the sporophyte and gametophyte (Ligrone and Renzaglia, 1989). This finding has been confirmed in S . subnitens and S . cuspidaturn at stage 1 of sporophyte development. The placental organization is almost identical in the four species. The sporophytic placental cells protrude from the bottom of the foot into a large, mucilage-containing space that separates the two generations (Fig. 8). These cells differ from the internal parenchyma cells of the foot, having denser cytoplasm and relatively small vacuoles (Fig. 9). Moreover, they apparently contain a vast number of plastids of very small sizes and irregular shape with few or no thylakoids, numerous plastoglobules and abundant peripheral reticulum (Fig. 10). These plastids are often aggregated in groups and presumably are sectional profiles of larger, extremely pleomorphic plastids. The nucleus generally lies in a central position and may have an irregular shape. The cells walls, relatively thin and uniform, have a compact fibrillar texture (Fig. 9).
242
R. LIGRONE
el a/
T H E GAMETOPHYTE-SPOROPHYTE JUNCTION
243
On the opposite side of the placenta are several layers of small gametophytic cells (Fig. 13). These have large vacuoles and dense cytoplasm mostly gathered at the periphery and rich in mitochondria, dictyosomes and sheets of rough endoplasmic reticulum (Fig. 11). The plastids are larger and less numerous than their sporophytic counterparts, and generally exhibit well-developed grana (Fig. 12). The gametophyte placental cells characteristically have thickened walls with a loose fibrillar texture, interrupted by pits with a high frequency of plasmodesmata (Fig. 14). In S. fimbriatum these thickened walls contain distinctive tubular structures arranged radially (Ligrone and Renzaglia, 1989). The gametophytic placental tissue contains abundant intercellular spaces that are continuous with the larger placental space. As the sporophyte matures the gametophyte cells closer to the foot degenerate (Fig. 13). Starch is generally lacking in both the sporophyte and gametophyte placental cells, whereas it is abundant in the adjoining parenchyma cells of both generations.
3. Bryidae This subclass includes all peristomate mosses and is divided into two groups: the nematodontous mosses, with peristome teeth composed of whole cells; and the arthrodontous mosses, with peristome teeth composed, primarily or exclusively, of articulated and fused cell plates (Edwards, 1984; Vitt, 1984). The former group traditionally includes the orders Polytrichales and Tetraphidales, whereas the latter includes all the most advanced mosses, classified in the single order Bryales by Vitt (1984) or in several orders by others (cf. Smith, 1978; Miller, 1979; Crosby, 1980; Corley et al., 1981). Typically in the Bryidae the sporophyte foot is highly elongate, conical in shape and penetrates the gametophyte stem tissue. It is partially or completely surrounded by the vaginula, a multilayered parenchymatous sheath derived from the proliferation of archegonial cells and the underlying stem tissue (Roth, 1969). Further details of the ultrastructure of the vaginula are given in Ligrone and Gambardella (1988a). In acrocarpous mosses the sporophyte develops at the apex of the gametophyte stem, which ceases growing since apical growth terminates in the production of archegonia. In pleurocarpous mosses the sporophyte
Figs. 5 7 . The gametophyte-sporophyte junction in Takakia ceratophylla. Fig. 5. Light micrograph, longitudinal section, showing the elongate foot with a central strand of hydroids. Fig. 6. Sporophyte placenta cell showing the wall labyrinth along the outer tangential wall and elongate plastids. Fig. 7. Gametophyte placental cell with electron-transparent inner wall material (arrowed). Figs. %lo. The gametophyte-sporophyte junction in Sphagnum cuspidaturn. Fig. 8. Light micrograph, longitudinal section, showing the bulbous foot at the apex of the pseudopodium (PS). Fig. 9. Sporophyte placental cell with thin walls, numerous vacuoles and small plastids and mitochondria. Fig. 10. Pleomorphic undifferentiated plastids in a sporophyte placental cell.
244
R. LIGRONE et al.
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
245
develops at the apex of short lateral branches, and the main stem grows indefinitely. In some groups, e.g. the Polytrichales, the gametophyte is acrocarpous, but the old sporophytes may be displaced laterally due to subsequent innovative growth of new shoots. Frequently in acrocarpous mosses the foot tip penetrates the gametophyte central strand. This is due to intrusive growth of the foot and parallel sporophyte-induced proliferation and differentiation of the gametophytic tissue (Roth, 1969). Penetration of the central strand by the foot, however, seems to have no taxonomical significance as differences are found even within the same genus (Roth, 1969). The foot of Bryidae has the same histological organization as the seta. When the seta contains a central strand of conducting tissue (Hebant, 1977), this is also present in the foot. The lower part of the foot, however, differs from the seta in lacking a peripheral sterome and in the presence of highly specialized epidermal cells. In the Polytrichales the conducting strand contains both hydroids and leptoids, the latter being simpler in structure than in the gametophyte (HCbant, 1977,1979). Leptoids have also been reported in the foot of Funaria (Wiencke and Schulz, 1975), but generally they seem to be lacking in Bryales (Hebant, 1977, 1979). The foot (and seta) of many groups in the Bryales lacks a central strand of conducting cells, most likely as a consequence of reduction (Crosby, 1980; Schofield, 1985). In several acrocarpous genera, e.g. Polytrichum, Bryum, Funaria and Encalypta, apoplastic continuity between the central strands of the gametophyte and sporophyte may result from the degeneration of foot-tip cells (Roth, 1969; Hebant, 1975; Ligrone and Gambardella, 1988a).
3. Polytrichales The order Polytrichales comprises 20 genera and about 300 species placed by Smith (1971) in the single family Polytrichaceae. Representatives of seven genera have been examined ultrastructurally (Table I). The polytrichaceous mosses have a typical bryoid foot of elongate conical shape that penetrates the gametophyte stem tissue to a considerable depth. A conspicuous central strand of conducting tissue is present in both the gametophyte and sporophyte. As in the seta (Htbant, 1977), a system of intercellular spaces is present in the foot parenchyma (Ligrone and Gambardella, 1988a).
Figs. 11-14. The gametophyte-sporophyte junction in Sphagnum cuspidatum (cont.). Fig. 11. Gametophyte placental cell with characteristic wall thickenings. Fig. 12. Sporophyte placental cell; plastid with well-differentiated grana. Fig. 13. Longitudinal section through the gametophyte placental cells. Note the large intercellular spaces and the degenerating cells nearer the foot (top, arrowed). Fig. 14. Gametophyte placental cell; pitted region of the wall containing numerous plasmodesmata.
246
R. LIGRONE et al.
Figs. 15 and 16. The gametophyte-sporophyte junction in Polytrichales. Fig. 15. Atrichum
undulatum; showing the sporophyte wall labyrinth and thickened tangential walls in the
gametophyte placental cells. Fig. 16. Pogonatum neesii; gametophyte placental cells with greatly thickened walls.
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
247
The placental organization is substantially similar to that in Andreaea, with transfer cells in the foot only. The most prominent wall labyrinths are found in the epidermal cells but a wall-membrane apparatus typical of transfer cells may also be present in the two to three outermost layers of parenchyma cells (Fig. 17). The epidermal transfer cells have dense cytoplasm with numerous mitochondria and abundant endoplasmic reticulum (Fig. 15). The plastids are small, lack starch and have a central rudimentary thylakoid system, surrounded by conspicuous peripheral reticulum (Figs. 18and 19). The internal transfer cells tend to be more vacuolate and with less dense cytoplasm (Fig. 17). Several layers of specialized gametophyte cells surround the foot in Pogonatum and Oligotrichum, whereas a single layer is present in Atrichum (Fig. 15) and Polytrichum. The gametophyte placental cells have thickened walls with irregular outlines but never form a wall labyrinth. Cell wall thickening is most pronounced in Pogonatum (Fig. 16), with a consequent strong reduction of the cell lumen. A similar situation occurs in Oligotrichum. Only the inner tangential walls of the gametophyte placental cells become thickened in Atrichum (Fig. 15), whereas in Polytrichum thickwalled cells with dense cytoplasm are intermingled with larger thin-walled cells with prominent stacks of endoplasmic reticulum. Typically, the gametophyte placental cells have dense cytoplasm with small vacuoles and abundant endoplasmic reticulum. Their plastids may have a more highly organized thylakoid system and less peripheral reticulum than their sporophytic counterparts, but, unlike those in the vaginula, they contain little or no starch. The gametophyte cells closer to the foot often undergo cytoplasmic degeneration. Like Andreaea, the polytrichaceous mosses accumulate abundant lipid reserves in both the placental cells and adjoining parenchyma cells. 4. Tetraphidales The order Tetraphidales consists of two (Crosby, 1980) or three genera (Vitt, 1984), each with three o r four species. Only one of these, Tetraphis pellucida, has been examined ultrastructurally . The foot penetrates the gametophyte central strand and has a central strand of hydroids surrounded by elongate parenchyma cells, whereas leptoids are absent (Figs. 20 and 21). A well-developed wall labyrinth is present in the epidermal cells from very early stages in sporophyte development. In the lower part of the foot the epidermal cells are highly vacuolate and the bulk of the cytoplasm lies adjacent to the labyrinthine walls, whereas in the middle of the foot the epidermal cells contain very small vacuoles and most of their lumen is occupied by dense cytoplasm rich in mitochondria1 lipid droplets (Fig. 23) and chloroplasts with highly organized grana (Fig. 24). O n the opposite side of the placenta are gametophyte cells with thickened
248
R. LIGRONE et al.
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
249
walls that may form large and coarse protuberances (Fig. 22). Conspicuous wall labyrinths are occasionally found on the lateral walls of the gametophyte cells adjoining the middle portion of the foot. The plastids in the gametophyte placental cells are of smaller and more irregular shape than those in the sporophyte. Their inner membrane system is rudimentary and small amounts of starch are sometimes present. Starch and lipid reserves are much more abundant in the adjoining cells of the vaginula. 5. Bryales Divided by Vitt (1984) into 15 suborders, 85 families and 765 genera, this is the largest and most diverse group of mosses. In sharp contrast to an extreme variability in the gametophyte and sporophyte morphology, the placental organization is remarkably uniform. Twenty species, belonging to nine different suborders, have been examined ultrastructurally (Table I), and several others have been examined by light microscopy only (see Roth, 1969, for a comprehensive review). All of these, with the exception of Dicranum (Fig. 25), exhibit transfer cells on both sides of the placenta (Figs. 26, 27, 31, 32 and 34). Labyrinthine walls are generally restricted to the single layer of epidermal cells in the foot and the adjoining layer of gametophyte cells, but isolated wall ingrowths are also frequent in gametophyte cells farther from the foot. Several layers of well differentiated transfer cells have been reported in the gametophyte placenta of Buxbaumia piperi (Ligrone et al., 1982a). In most cases the foot has a regular outline and is separated from the gametophyte by a placental space containing residues of collapsed cells of gametophytic origin (Fig. 25) and sometimes calcium oxalate crystals (Fig. 27). In some instances, however, interpenetration of the sporophyte and gametophyte placental tissue may increase the contact area between the two generations. For example, the elongate epidermal cells of Bryum are wedged among the adjoining gametophyte cells (Ligrone and Gambardella, 1988a), and in Diphyscium the foot is covered with multicellular tubular outgrowths that deeply penetrate the adjoining gametophyte tissue (Figs. 28-30). In general the wall labyrinths are equally well developed in both generations (Figs. 26 and 27) but sometimes are more elaborate in the sporophyte (e.g. Mnium, Aulacomnium, Fissidens) (Figs. 32 and 34). The opposite situation accrues in Diphyscium (Fig. 31). The wall ingrowths in Figs. 17-19. The gametophyte-sporophyte junction in Polytrichales (cont.). Fig. 17. Polytrichum formosum; several layers of sporophyte transfer cells. Fig. 18. Pogonatuni aloides; sporophyte placental cell plastids. Fig. 19. Oligotrichurn hercynicum; sporophyte placental cell plastid. Figs. 20 and 21, Light micrographs of the garnetophyte-sporophyte junction in Tetraphis pellucida. Fig. 20. Transverse section. Fig. 21. Longitudinal section.
250
R. LIGRONE ei al.
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
251
the placental cells of the Bryales are thinner, longer and more convoluted than in the other orders of Bryidae (Fig. 33) and presumably this results in a proportional increase of the surface extension of the wall-membrane apparatus. In Funaria the wall labyrinths develop at a very early stage of sporophyte development, reaching the maximum extension well before capsule differentiation (Wiencke and Schulz, 1978; Browning and Gunning, 1979a). The same has been observed in several other species, such as Mnium hornum (Fig. 33), Brachythecium vefutinum and Fissidens crassipes (Fig. 34). As in the other orders of mosses, the placental cells in Bryales have dense cytoplasm rich in mitochondria and generally are not highly vacuolate. The presence of numerous vacuoles of small sizes instead of large vacuoles may protect the placental tissue against water stress (Oliver and Bewley, 1984), an eventuality that might be particularly prejudicial to sporophyte development. Plastids are somewhat variable in structure, although they are generally much less differentiated compared to those in other tissues (Duckett and Renzaglia, 1988b). A relatively well-developed inner membrane system has been observed in the plastids of sporophyte placental cells of Funaria (Browning and Gunning, 1979a), Physcomitrium (La1 and Chauhan, 1981) and Archidium (Brown and Lemmon, 1985). Massive granal stacks with few or no stroma thylakoids have been found in Timmieffa (Ligrone et a f . , 1982b), Mniurn (Fig. 35), Dicranum (Fig. 37), Cfadophascumand Diphysciurn. Highly pleomorphic plastids with abundant peripheral reticulum closely similar to the saccate mitochondria1 cristae in the same cells, and few or no thylakoids occur in the sporophyte placental cells of Bryum (Fig. 36; Ligrone and Gambardella, 1988a), Buxbaumia (Ligrone et a f . , 1982a), Fissidens and Brachythecium (Ligrone and Gambardella, 1988a). Plastids in gametophyte placental cells are either larger o r smaller than those in the sporophyte and almost always contain starch (Figs. 38-41), whereas this is much less frequent in the sporophytic counterparts (Figs. 35-37). The range in the ultrastructural characteristics of these plastids is illustrated in Figs. 38-41. Shape varies from spheroidal in Cfadophascum (Fig. 38), Diphyscium (Fig. 39) and Bfindia (Fig. 41) to pleomorphic in Fissidens. The thylakoid system is also variable, appearing as irregular arrays of membranes in Diphyscium (Fig. 39), small grana in Cfadophascum (Fig. 38) and large stacks in Bfindia (Fig. 40). The parenchyma cells of the vaginula almost invariably contain large amyloplasts and often also abundant lipid reserves. This feature is most Figs. 22-24. The gametophyte-sporophyte junction in Tetruphispellucidu (cont.). Fig. 22. Gametophyte placental cells with large, coarse wall protuberances (mowed). Fig. 23. Midregion of foot; wall labyrinth o n the outer walls. Fig. 24. Chloroplast in a sporophyte placental cell.
252
R. LIGRONE et al.
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
253
pronounced in the vaginula cells of Diphyscium, which are comparable to endosperm cells of seed plants in the abundance of their reserve materials (Fig. 40). Starch is also abundant in the parenchyma cells of the foot. These cells are highly elongated longitudinally and present high concentrations of plasmodesmata in the cross walls. This may reflect a functional specialization in the acropetal transport of nutrients toward the sporangium. B. LIVERWORTS (Hepatopsida)
As in mosses, in all liverworts, except the Monocleales (Campbell, 1954a; K. S. Renzaglia, unpublished data) the first division of the zygote is transverse and produces a small epibasal and a large hypobasal cell.The destiny of these two cells appears to vary widely. However, the available information about early stages in embryogeny is far from conclusive in as much as original descriptions are relatively few and sometimes conflicting. It is generally agreed that in the Jungermanniales the second division occurs in the epibasal cell and produces a three-celled embryo (Smith, 1955; Schertler, 1979; Crandall-Stotler and Geissler, 1983; Schuster, 1984a). Of the two epibasally derived cells, the outermost one is the capsule initial whereas the other will form the seta and foot. The hypobasal cell undergoes few or no further divisions, forms a filament, referred to as the huustorium, and penetrates the underlying gametophyte tissue. The function of this structure seems to be confined to very early stages in sporophyte development, after which the foot becomes the primary absorptive organ and the haustorium generally becomes indistinct (Schuster, 1984a). In the Metzgeriales, as in the Jungermanniales, the hypobasal cell forms only a haustorial appendage and the foot has a epibasal origin (Clapp, 1912; McCormick, 1914; Campbell, 1916; Showalter, 1926, 1927a,b; Haupt, 1929b; Smith, 1955; Crandall-Stotler, 1981; Schuster, 1984a). The information available on embryogeny in the Calobryales is particularly poor and inconclusive. Early studies by Goebel (1891) and Campbell (1920) report embryo development in Cufobryumbfumei to follow the same pre-determination pattern as in the Jungermanniales and Metzgeriales, with the hypobasal cell producing a haustorium and the epibasal cell giving rise to the sporophyte proper. This type of embryogeny is currently referred to as typical of the whole group (Smith, 1955; Crandall-Stotler, 1981; Schuster, 1984a). Nevertheless, more recent accounts of early embryogeny in Hupfomitrium gibbsiue Steph. (Campbell, 1954b) and Cafobrymindicurn Udar et Figs. 25-27. Bryalean plancentas. Fig. 25. Dicranum majus; the gametophyte cells are thin-walled and lack wall ingrowths. Note the collapsed cells in the intraplacental space (arrowed). Fig. 26. Leucobryum gluucum; extensive wall labyrinths in the placental cells of both generations. Fig. 27. Cladophascum gymnomitrioides; calcium oxalate crystals in the intraplacental space (arrowed).
254
R. LIGRONE et al.
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
255
Chandra (Mehra and Kumar, 1990) have reported a “quadrant stage” much like that in Marchantiales (see below). Moreover, according to these descriptions, no haustorium is formed, and since the cellular divisions following the first one are irregular there is no clear-cut distinction between epi- and hypo-basally derived parts of the embryo. Mehra and Kumar (1990) suggest that in the Calobryales, as in Marchantiales (see below), a filamentous and a quadrant type of early embryogeny may co-exist. In the Sphaerocarpales both the epibasal and hypobasal cell divide transversely. This results in a four-celled filamentous embryo in which each cell, by two successive vertical divisions, produces a tier of four cells (Smith, 1955). Two different patterns of embryo development, sometimes present in closely related taxa or even within the same genus, are recognized in the Marchantiales. In several genera, including Targionia (O’Keefe, 1915), Conocephalutn (Meyer, 1929), Reboulia (Dupler, 1922), Grimaldia (Meyer, 1931), Asterella (Haupt. 1929a) and Marchesta (=Neohodsgonia H. Pears.) (Campbell, 1954c), the zygote forms a four-celled filamentous embryo as in the Sphaerocarpales. In other genera, such as Corsinia (Meyer, 1912, 1914), Marchantia (McNaught, 1929) and Preissia (Haupt, 1926), the two daughter cells arising from the zygote divide by successive vertical walls, at right angles to each other, forming a “quadrant” type of embryo. No distinct haustorium is developed. The same is observed in Riccia, where most species have a quadrant type of embryo, but in certain species a four-celled embryo of the filamentous type is formed. In any case a seta and foot are lacking in this genus and all the cells of the embryo participate in the formation of a globose capsule that remains enclosed within the gametophyte tissue (Lewis, 1906; Pagan, 1932; Smith, 1955). The origin of the different parts of the mature sporophyte in the Sphaerocarpales and Marchantiales cannot be related with certainty, particularly in the filamentous type of embryo, to the epibasal or hypobasal cell, although a hypobasal origin of the foot and seta is often assumed (Campbell, 1954a; Smith, 1955; Schuster, 1984a). An alternative interpretation of embryogeny in these groups may be neotenic suppression of the hypobasal cell, implying that the first transverse division of the zygote is equivalent to the first transverse division of the epibasal cell in the other groups. This hypothesis may account for the lack of a haustorium in Sphaerocarpales, Marchantiales and Calobryales while maintaining a unitary basic pattern of early embryogeny in the whole of mosses and liverworts. Monoclea is apparently unique in the liverworts as, according to Campbell (1954a) and recently confirmed (K. S. Renzaglia, unpublished data), the Figs. 28-32. Bryalean placentas (cont.). Figs. 28-30. Light micrographs; longitudinal sections of the gametophyte-sporophyte junction in Diphysciurn foliosum. The massive foot is covered with multicellular tubular outgrowths. Fig. 31. Longitudinal section of the placenta of Diphysciurn. Wall ingrowths are more highly developed in the gametophyte cells. Fig. 32. Mniurn hornunz: wall ingrowths are more elaborate in the sporophyte.
256
R. LIGRONE
el
al.
T H E GAMETOPHYTE-SPOROPHYTE JUNCTION
257
zygote undergoes free nuclear divisions to the 26-nucleate stage, after which partitioning produces a globose embryo. This description, however, contrasts with the illustration by Cavers (191 1) of a two-celled embryo followed by a quadrant stage, as well as with a description by Johnson (1904) of embryo development in Monoclea forsteri Hook. As in mosses, fertilization causes extensive proliferation in the gametophytic tissue underlying the embryo. The archegonial cells form a calyptra that surrounds the sporophyte until spore maturation. Additional protective structures are perianths or pseudoperianths, stem-derived structures such as perigynia, coelocaules and marsupia, or simple outgrowths of the thallus (Schuster, 1966, 1984a). In various Jungermanniales and Metzgeriales the receptacle tissue below fertilized archegonia contributes to the formation of the calyptra, that is therefore referred to as stem- or shoot-calyptra (Schuster, 1984a). 1. Jungermanniales The order Jungermanniales, the largest among the Hepatopsida with about 180 genera and 7500 species (Bold et al., 1989), comprises the “leafy liverworts”. These are also referred to as acrogynous liverworts in as much as their sporophyte develops at the apex of the main stem or lateral branches that, as in the acrocarpous mosses, cease growing. In contrast to the huge variability of gametophyte morphology, the sporophyte of the Jungermanniales is rather uniform and displays, in all instances, a distinct division into foot, seta and capsule. The foot is generally bulbous or spheroidal (Fig. 42) of relatively small size (20C300 km in diameter), and sometimes reduced to a few cells (e.g. in Lejeunea; Schuster, 1984a). In many instances a “collar” of cells develops at the junction with the seta. This probably reinforces the attachment of the sporophyte to the parental gametophyte. In some genera, e.g. Goebefobryum and Acrobolbus (Schuster, 1966), the collar is particularly bulky, and in extreme cases, as in Jackielfu (Schuster, 1984a), it consists of a massive sheath of multicellular filaments. The foot in Radulu (Figs. 53 and 54) recalls bryopsid mosses such as Bryum and Diphyscum in the presence of irregular radially elongated peripheral cells that interdigitate with the adjacent gametophytic cells. In some cases, e.g. Lejeuneu, Jubula, Frullania and Bryopteris, the foot remains surrounded by a tissue derived solely from the archegonial base, and does not penetrate the stem apex. Such a condition is probably related to the stalked structure of the archegonia in these genera (Crandall-Stotler and Guerke, 1980; Schuster, 1984a). More frequently, the foot is deeply Figs. 33 and 34. Bryalean placentas (cont.). Fig. 33. Oblique section through the thin, convoluted ingrowths in a gametophyte placental cell of Bryum cupillure. Fig. 34. The placenta in a young sporophyte of Fissidens crussipes. Note the early development of the wall labyrinths.
HerbeItaEeae Hwberra 'pp.
1
+
Lcpidoriaceae Kuriro rnchocldos Grolle Zoopsrr Irukiumw Horik
I 1
+ +
1 1
+ +
Cephalozraceae
Cephpholorro brcupidnrv (Nees) Llrnpr. Cephphaloiro lunulifolm Durn
Jungerrnanniaceae Jungermannia gracrllrma Sm
1
t
Gyrnnornitriaceae Marruprlln funrkri Durn
1
+
1
I
+ +
Lophomleo hrrerophyllo (Schrad) Durn.
I
+
Radulaceae Rodulo complonrvo (L ) Durn
1
Scapantaceae Scoponio grveib Kaal Dtplophyllw, albrconr (L ) Durn. GeOCalyC2Le*e
j
5
1
1 1 I 1
I 1
Riccordw mulnfido S Gray
~
~
Outermost fool a l l r . accarbnally
on tareral cell,
+
Outer rang.bwalIr
+
t
+
~
~
~
~
Late
. N,A
,
Lahynnth. fine very dcnre
. N/A
.
-
.Bulbour
Thldtenln~01 mner laogntlal "all> auh
radially am"@ depovtr
N:A
+
+
. N:A
NIA
Several l a y e r r of Ldlz
Late
Ourer tang. aod
Sereral laycn of
Late
lateral naUs
cells
NIA
Late
Late
Lahynnth
Lahynnth Lahynnth } Coane
Outertang *all5 Outerlang. nalk N:A N:A
N:4 N:A N:.4
NIA
NIA
NIA
X:A
N:A
NIA
NIA
NIA
W l
Ni.4
NIA
NIA
NIA
Labynth
BdbO",
Lahynnth Coarse
Con,cal
Coarse
Thm walk. inegular
plaimalernma
CALOBRYALES Colobrywn hlums Necs Hoplomrlnum hookui Neen
MARCHANTUDAE MONOCLEALES Monucleu gouxha Lmdb. SPHAEROCARPALES Sphaermwpm donne//,Aust Sphaerocarpos kzmw A w l . MARCHANTIALES Carrpineae Conpos monocorpos Prosk
I
Several byerr of Fells
+
Outer rang and lateral walls
Several layers of cel- Late
I
+ +
+
I
+ +
Targorgronro h.vpophvllo L
+
Reboulw hemrrphnrnco Raddi
Plogiochosmo rupesrrc Steph
Outer
4
TaC@O"lCiCW
Monnta ondrogmo Evan,
+
+
Several layen of
+
outer tang
Several layers of d l S
+
Outer tang walls
+
+
1
+
} Outer
+
Wi1116
cells
Outer tang. wall
outer tang. wall
Several layers of
cells
} Labyrinth Labyrinth
Transparent
} Labynnth } Labynnth
Transparen1
} Late
} Labyrinth
Late
Labyrinth
Shon coarse
Late
Labyrinth Coax
Labyrioth Coarse
Late
Labyrinth
Labynnth
Late
Late
Labryinth
Labynnth
Late
Late
Labynnth
Labyrinth
} Very Late
Late
outerrang walls and inner parenchyma
Late
15
tang. and lateral walls
+
} Early
}Early
late
-
} Bulboua
-
Conlral
} Labyrinth }
} Spheroidal -
Spheroidal
Spheroidal
~
~
~
BUlhOUS
Bulboua
Bulbous
TABLE IV Cytoplasmic features of placental cells in liverworts Plartids Fametophyte
Sporophyte Sham
Membrane system
Plastodobuli
Starch
Shaoe
Plwmorphic
r.gr.
+
+
Ellipsoidal
Spheroidal Ellipsoidal Pleomorphic
qr.
+ +
+
Cepholoria bicurpidatu Cephnloiio lunulifolio
Ellipsoidal Pleomorphic
n.gr.
+
Ellipsoidal Ellipsoidal
Jungerrnanniaceae Jungermannia gracillima
Spheroidal Ellipsoidal
*.g
+
Ellipsoidal
Membrane system
Plastoglobuli
Starch
Cytoplasmic lipid droplets Sporophyte Gametophyte . . .
JUNCERMANNIALES Herbertamae Herbem sp.
Lepidoziaceae Kurrio Wchoclados Zoopsk liukiuenrk
Cephaloziaceae
Gymnomitriaceae
Manuprlla funckii
Scapaniaceae Scaponzo grocilrr
Diplopkyllum albicons
Geacalycafeae
Lophoeoleo heterophyllo
Radulaceae
Rodulo complonoro
Ellipsoidal
r.gr.
n.gr.
+
+
++
++ +
Ellipsoidal Ellipsoidal
+
+ +
+
Pleomorphic
n.gr.
Pleomorphic Pleomorphic
r.gr. r.gr.
Ellipsoidal Pleamarphic
n.gr.
Ellipsoidal
+
+
Elliposidal
r.gr.
Spheroidal
++
+
Elongate Pleomorphic
n.gr.
Spheroidal
Pleomorphic
n.gr.
Spheroidal
Pleomorphic
pr0.b.
Pleomorphic
Pleomorphic
qr.
Pleomorphic
Pleomorphic Pleomorphic Pleomorphic
r.gr.
+
Ellipsoidal Pleomorphic Pleomorphic
+
+
+
+
METZGERIALES Fossombroniaceae
Fosrornbronio echinoto
Blasiaeeae
B l a h pusillo
Pelliaceae Pollovicinio lyellii Pallovicinio indim Pellia endiviifolia Pellio epiphyllo A"e"raCeae Aneuro pinguk
Cryprothollw mirobilir
Riccordio multifida
} }
+
*.
r.gr.
+
+
++ +
Pleomorphic Plwmorphic Plwmorphic
+
+
+
+
11 +
+ +
1:
+ +
+
'.*. r.gr
Pleomorphic Spheroidal
'.
Sphered Plmmorphic
}
Ovoid
}
Plwrnorpbic Plmmorphic
".*. ".gr.
'.gr.
+
P.'.
Spheroidal
}
w.
".a.
Ovoid
Spheroidal
'.*.
ELlipsoidal Plwmorpbic
r.-
Spheroidal Plwmorphic
pro.b.
spheroidal Spkroidal Plwmorphic
n.gr.
Discoid
0.gr.
Elongate + Rbres Pltomorphic Plwmorphk
,.g.
Elongate Plwmorphic Plwrnorphic Dismid Discoid
Riccia sorocarpa
+
c
NIA
'.*.
+ +
+
'.*. r.*.
+ '.*.+
+ +
NIA
N/A
'gr. p.r. P.'.
NIA
'.gr r.-n.gr
r.gr.
'.gr.
Dismid Discoid
'.*. r.g.
NIA
N/A
NIA
Abbreviations: we., oormal m a . like t h a v in leaves; r . ~ rudimentary . gram, 2-3thylaloids only; r , siogle thylaloids; pr0.b. prolameUar body; p.'. peripheral miarlum.
NIA
NIA
NIA
262
R. LIGRONE et al.
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
263
embedded in the stem tissue (Fig. 42), although very little or no true penetration actually occurs, since the axial tissue surrounding the foot develops after fertilization (Schuster, 1984a). The cytology of the placental region, examined in 11 species belonging to eight different families (Table HI), is extremely uniform and highly distinctive. With the exception of Radula, elaborate wall labyrinths develop in the outermost cells of the foot. In this last genus the walls of the sporophytic placental cells are relatively thin and smooth. In the other 10 (Fig. 54) these cells produce thin and highly branched ingrowths of extremely dense wall material (Figs. 43-46). Less extensive wall labyrinths or isolated wall ingrowths are present in the parenchyma cells of the foot. No trace of wall ingrowths is observed in gametophytic placental cells of all eleven genera. The cytoplasmic organization of sporophytic placental cells is somewhat variable. In Zoopsis, Marsupella and Kurzia these cells contain one or a few large vacuoles of irregular shape and the nucleus is suspended in the centre by cytoplasmic strands connected with a peripheral layer of cytoplasm (Figs. 43 and 44). Most organelles, notably plastids and mitochondria, are associated with the wall labyrinth along the outer tangential walls. In Scapania, Diplophyllum, Lophocolea, Radula and Herberta the sporophytic cells have very small vacuoles and are rich in lipid deposits concentrated in proximity to the wall labyrinth (Figs. 45 and 46). The gametophytic placental cells, though lacking wall ingrowths, are clearly distinct from the parenchyma cells farther from the foot in having smaller vacuoles and denser cytoplasm, rich in mitochondria and other organelles. These cells form several concentric layers around the foot, the innermost of which degenerate and collapse during the phase of foot expansion (Figs. 43-45). An interesting specialization has been reported in Jubula, where the gametophyte cells within a 40pm range of the foot continue dividing as sporophyte growth proceeds to form small-celled filaments that extend towards the foot (Crandall-Stotler and Guerke, 1980). This also happens but to a more limited extent in Radula (Fig. 53). In every genus the inner tangential walls of gametophyte placental cells become thickened and may produce radially arranged deposits of dense material (Fig. 47) similar to those found in some Sphagnum species (Ligrone and Renzaglia, 1989), Andreaea, Takakia and Polytrichales. Plastid morphology in the placental cells of the Jungermanniales also is somewhat variable. The sporophyte cells contain numerous small plastids ranging in shape from spheroidal (Kurzia; Fig. 50), ellipsoidal or irregular (Herberta, Cephalozia, Zoopsis and Lophocolea; Fig. 49), to highly Figs. 35-37. Plastids in bryalean sporophyte placental cells. Fig. 35. Mniurn hornum; pleomorphic with massive grana. Fig. 36. Eryum cupillare; undifferentiated plastids intermingled with mitochondria. Fig. 37. Dicrunum mujus; ovoid with massive grana. Note the umbo-shaped mitochondria.
264
R. LIGRONE et
a1
Figs. 38-41. Plastids in bryalean gametophyte placental cells. Fig. 38. Cladophascum gymnomitrioides; starch grains surrounded by rudimentary grana. Fig. 39. Diphyscium foliosum. Fig. 40. Diphyscium foliosum; vaginula cell. Fig. 41. Blindia acuta.
THE GAMETOPHYTE-SPOROPHYTE JUNCTION
265
pleomorphic (Scapania and Diplophyllum; Figs. 51 and 52). The thylakoid system may be as extensive as in the leaf cells (Cephalotia, Lophocolea, Marsupella, Radula and Zoopsis; Figs. 46 and 49), or poorly differentiated (Scapania, Herberta and Diplophyllum; Figs. 51 and 52). Starch may be present (Lophocolea, Herberta, Cephalozia and Marsupella; Figs. 45 and 46) and is sometimes abundant (Kurzia; Figsvvvvv. 43 and 50), but in other genera (e.g. Scapania, Diplophyllum and Radula) is absent (Figs. 51 and 52). Plastids in gametophyte placental cells are generally larger than in the sporophyte, have a well developed thylakoid system and contain very little starch. The gametophyte plastids of Herberta are unusual in having abundant lipid inclusions associated with the thylakoid system (Fig. 48). 2. Mettgeriales The Metzgeriales, with about 20 genera and 550 species, are commonly referred to as the “simple thalloid liverworts”, the gametophytes lacking air chambers, air pores, pegged rhizoids and-with some exceptions, e.g. Blasia and Cavicularia (Renzaglia, 1982)-ventral scales (Bold el al., 1989). They are also called the anacrogynous liverworts, as sporophyte development normally does not terminate the growth of the gametophyte. The foot is generally conspicuous, of conical or spheroidal shape, and frequently bears a massive collar (Fig. 55). The placental region is highly variable, with all the possible combinations in the distribution of transfer cells (Table 111). In Blasia and Fossornbronia well-developed transfer cells are found in both generations (Figs. 56 and 57), generally forming several layers in the gametophyte. Transfer cells are restricted either to the sporophyte in Pallavicinia (Fig. 5 8 ) , or to the gametophyte in Riccardia (Fig. 59). The walls of the sporophytic placental cells in the latter genus are identical in appearance to their gametophytic counterparts in the Jungermanniales: both have thickened outer tangential walls containing radially arranged deposits of dense material (compare Figs. 59 and 60 with Fig. 47). In striking contrast, wall labyrinths are absent in Pellia (Fig. 61), Cryptothallus (Fig. 62) and Aneura. Here the placental cells of both generations are thin-walled save for the limited development of nacreous thickenings in the sporophytic cells of Aneura (Fig. 63). In these genera that lack wall ingrowths the plasmalemma of placental cells often presents an irregular outline along the tangential walls and may form short invaginations apparently not supported by wall material (Fig. 64). Similar invaginations are also found in parenchyma cells of the foot in Cryptothallus. In most species the wall ingrowths, when present, are short and coarse and form relatively simple wall labyrinths. By contrast, in Blasia (Fig. 57) and, to a lesser degree, in Fossombronia (Fig. 56), the sporophyte cells have highly branched wall ingrowths that form three-dimensional networks of
266
R. LIGRONE rl ul.
T H E GAMETOPHYTE-SPOROPHYTE JUNCTION
267
great complexity. Similarly elaborate wall labyrinths are common in marchantialean liverworts (see Section II.B.4), but are not found in the placenta of Jungermanniales. The placental cells also exhibit a notable diversity in their cytological organization. Generally they have dense cytoplasm rich in organelles and with numerous evenly scattered vacuoles of small sizes, but highly vacuolate placental cells are found in Pellia and Aneuru (Figs. 61 and 63). The sporophyte placental cells of Riccardia contain giant pleomorphic mitochondria, often associated with the nucleus (Fig. 65). Abundant sheets of rough endoplasmic reticulum characterize the gametophyte cells of Aneuru and Cryptothaffus(Fig. 66) and concentric sheets of endoplasmic reticulum surround lipid bodies in the sporophyte placental cells of Cryptothallus (Fig. 67). As in the Jungermanniales, the placental cells in the Metzgeriales contain numerous plastids of small sizes. In sporophytic cells, plastids with a welldeveloped thylakoid system are found in Bfusiu and Fossombroniu (Fig. 68). A less extensive thylakoid system is found in the plastids of Riccurdia (Fig. 69), and in Puffavicinia the thylakoids are associated with prolamellar body-like membranous arrays (Fig. 70). The thylakoid system is rudimentary in the sporophyte plastids of Pellia, Aneuru and in the early stages in Riccardia (Fig. 71) and Cryptothaffus(Fig. 72). At comparable stages in development, starch is absent in Fossombroniu, Blasia and Cryptothaffus,present in small amounts in Riccardia, and abundant in Aneura and Peffia.Plastids in gametophyte placental cells are much less variable and generally contain small starch grains and an inner membrane system of small grana connected by stroma thylakoids. Highly pleomorphic plastids occur in Aneura and Cryptothaffus(Fig. 73). As in other groups, the gametophyte cells closer to the foot, regardless of the presence of a wall labyrinth, degenerate precociously (Figs. 57 and 62). In most species, signs of cytoplasmic degeneration are visible in gametophyte placental cells soon after sporocyte differentiation, whereas the sporophyte placental cells show little changes until spore formation, although they show signs of cytoplasmic degeneration before the seta starts elongating. In Riccardia the wall labyrinths in gametophyte cells reach their maximum complexity after meiosis (Fig. 5 8 ) , at which time the wall thickenings develop in the sporophyte cells. A progressive increase in the thickness of sporophyte placental cell walls also occurs in Cryptothuffus along with capsule maturation. Figs. 42-44. The gametophyte-sporophyte junction in Jungermanniales. Fig. 42. Light micrograph; longitudinal section of the bulbous foot of Kurzia trichoclados. Fig. 43. Kurzia trichoclados; note the fine wall labyrinth and amyloplasts in the highly vacuolate sporophyte placental cells and collapsed gametophyte cells (arrowed) adjacent to the foot. Fig. 44. Marsupellafunckii; the cytology of the junction is virtually identical to that in Kurzia apart from the absence of starch in the sporophyte cells.
268
R. LIGRONE et ul
TH E GAMETOPHYTE-SPOROPHYTE JUNCTION
269
3. Calobryales
The Calobryales are a small group of leafy liverworts that traditionally includes three genera, Haplomitrium, Calobryum and Takakia, each comprising a few species. The first two are considered as synonyms by Schuster (1984b), whereas the last one is now best placed in a separate group close to the Andreaeidae (see Section 1I.A. 1). The sporophyte of Haplomitrium and Calobryum is enclosed within a shoot calyptra until maturity and forms a massive seta terminating downwards with a large bulbous or obconical foot (Bartholomew-Began, 1991). Unlike the gametophyte stem, which contains a central strand of water-conducting dead cells (Hebant, 1977, 1979), both the seta and foot consist of homogeneous parenchyma. However, dead empty cells with electron-dense deposits associated with longitudinal walls have been observed occasionally in the foot of Calobryum blumei (Fig. 76). A wall labyrinth is present in both foot epidermal cells and adjoining gametophyte cells (Figs. 74 and 75). Smaller labyrinths or isolated wall ingrowths may occur in more peripheral gametophyte cells and in the outermost parenchyma cells of the foot. The wall ingrowths in sporophyte placental cells are generally longer and more highly branched than in the gametophyte. Placental transfer cells differentiate before proliferative divisions terminate in the capsule, that is long before the onset of meiotic division. The sporophyte placental cells seemingly contain a single, highly pleomorphic plastid in Haplomitrium (Fig. 78), whereas numerous spheroidal and pleomorphic plastids, frequently associated with the nucleus, are found in Calobryum (Fig. 77). In both instances these organelles have but a rudimentary inner membrane system consisting of small granal stacks and few or no stroma thylakoids. Gametophyte placental cells contain pleomorphic plastids with a better developed thylakoid system, characterized in Calobryum by the presence of granal stacks perpendicular to the long axis of the organelles (Fig. 79). Starch is lacking in gametophyte cells, whereas small starch grains are common in sporophyte cells of Calobryum (Fig. 77). Abundant starch deposits are found in both foot parenchyma and gametophyte cells farther from the foot. Both sporophytic and gametophytic placental cells contain numerous mitochondria, frequently in intimate association with plastids (Figs. 77 and 79). The mitochondria are distinctly larger in sporophytic than in gametophytic placental cells. Figs. 45-47. The gametophyte-sporophyte junction in Jungermanniales (cont.). Fig. 45. Herberta sp; sporophyte transfer cells rich in lipid droplets. Collapsed garnetophyte cells are arrowed. Fig. 46. Lophocolea hererophyllu; sporophyte placental cell rich in lipid droplets. Fig. 47. Lophocolea; the gametophyte placental cell walls have tangential thickenings with radial deposits of dense material.
270
R. LIGRONE et al.
T H E GAMETOPHYTE-SPOROPHYTE JUNCTION
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4. Marchantiidae The three orders Monocleales, Sphaerocarpales and Marchantiales are related by a series of morphological and developmental features, including a similar embryogeny, specialized oil body-containing cells (Schuster, 1984a) and blepharoplast morphology (Duckett et al., 1982, 1984; Brown et al., 1983; Carothers etal., 1983), and are classified together within the subclass Marchantiidae by Schuster (1984b). All three present a similar placental organization and will therefore be discussed together. The foot, inconspicuous in the Sphaerocarpales, is relatively large in most Marchantiales, and varies in shape from spheroidal (Sphaerocarpos, Targionia), bulbous (Corsinia, Lunularia, Reboulia), cup-shaped (Marchantia, Preissia) to obtuse-conical (Monoclea; Fig. 80) or conical-elongated (Conocephalum). The placenta has been studied in detail in Monoclea, two species of Sphaerocarpos and eight species of Marchantiales (Tables I11 and IV). All of these except Riccia, whose sporophyte lacks a foot, exhibit much the same organization, with well-differentiated transfer cells in both generations (Figs. 81-86). The wall labyrinths in sporophyte cells consist of highly branched and anastomosing ingrowths and attain a structural complexity not equalled elsewhere in liverworts except Blasia. In several species, e.g. Sphaerocarpos (Fig. 83), Reboulia (Fig. 854, Targionia (Gambardella, 1987), and Monoclea (Fig. 81), gametophyte transfer cells also form extensive wall labyrinths, whereas in others, e.g. Carrpos (Fig. 86), Dumortiera (Fig. 84) and Conocephalum (Ligrone and Gambardella, 1988a), they have but coarse and short wall ingrowths. As a rule, there are several layers of transfer cells in the gametophyte, the innermost ones degenerating early in sporophyte development (Fig. 84), and a single layer in the sporophyte. Small wall labyrinths or isolated wall ingrowths are frequent in the peripheral parenchyma cells of the foot in Reboulia and Conocephalum (Ligrone and Gambardella, 1988a). A study of placental development in Targionia hypophylla (Gambardella, 1987) has shown that the wall labyrinths develop after differentiation of sporocytes, i.e. much later than in mosses (Browning and Gunning, 1979a). Generally both sporophyte and gametophyte placental cells contain numerous plastids with a well-developed thylakoid system. Pleomorphic plastids with a scarcely developed inner membrane system have been observed in sporophyte placental cells of Mannia and Plagiochasma (Gambardella and de Lucia Sposito, 1981, 1983) and a rudimentary inner membrane system associated with prolamellar body-like structures occurs in Figs. 4%5l. Plastids in jungermannialean placental cells. Fig. 48. Herbertu sp. gametophyte; ovoid and lipid bodies associated with the thylakoids. Fig. 49. Cephaloziu bicuspidata sporophyte: well developed grana. Fig. 50. Kurzia trichocludos sporophyte; ovoid amyloplasts. Fig. 51. Scuprmiu graci1i.r sporophytc; plcomorphic undifferentiated plastids.
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sporophyte plastids of Conocephalum (Ligrone and Gambardella, 1988a). The plastid stroma in the gametophyte transfer cells of Reboulia contains a bundle of thin parallel fibres (Fig. 87; Ligrone and Gambardella, 1988a). As in Metzgeriales, the placental cells in Marchantiales contain large stacks of endoplasmic reticulum. Distinctive membrane-bound bundles of tubules are found in young gametophytic placental cells of Reboulia hemisphaerica var. macrocarpa Zodda (Zodda, 1934; Figs. 88 and 89). In crosssection the tubules exhibit hexagonal packing (Fig. 88). Prominent bundles of fibrillar material without a bounding membrane were detected in the var. macrocephala Zodda (Ligrone and Gambardella, 1988a). However, the gametophyte placenta cells in this taxon contain concentric arrays of giant cup-shaped mitochondria (Ligrone and Gambardella, 1988a). Giant pleomorphic mitochondria in intimate association with plastids are also found in the gametophyte placental cells of Carrpos (Fig. 86). Cytoplasmic degeneration starts in gametophyte placental cells during meiotic division, a process often taking several months in the Marchantiales. By contrast the sporophyte cells break down only after spore formation. As in mosses (Browning and Gunning, 1979a), the degenerating transfer cells of Marchantiales (Gambardella, 1987) and other groups obliterate their wall labyrinths by depositing new wall material in the interstices among wall ingrowths. It has been suggested that in mosses this process may help to prevent the flow of water towards the drying capsule after spore maturation (Browning and Gunning, 1979a). This is highly unlikely in liverworts, where obliteration of the wall labyrinth precedes the elongation of the seta, a process needing large amounts of water, particularly in the Jungermanniales and Metzgeriales. No transfer cells are found at the sporophyte-gametophyte junction in Riccia. The sporophyte is entirely enclosed in the gametophyte (Fig. 90) and consists of a spherical capsule with a single-layered wall, surrounded by a two-layered calyptra (Fig. 91). With capsule enlargement the cells of the inner layer of the calyptra collapse and, following spore formation, the walls of thallus cells facing the calyptra become thickened (Fig. 92). Despite the absence of a specialized placental tissue, abundant lipid reserves accumulate in the spores (Fig. 92), indicating the operation of an effective mechanism of nutrient transport towards the sporophyte. Most probably nutrients are Fig. 52. Diplophyllum alhicans; pleomorphic plastid with a rudimentary thylakoid system in a sporophyte placental cell. Figs. 53 and 54. The gametophyte-sporophyte junction in Radula complanata. Fig. 53. Light micrograph, transverse section of the foot showing radially elongate outer cells. Fig. 54. Thin-walled sporophyte cells lacking ingrowths and thicker walled gametophyte cells. Figs. 55 and 56. The gametophyte-sporophyte junction in Metzgeriales. Fig. 55. Pellia epiphylla; light micrograph, longitudinal section showing the collar (arrowed). Fig. 56. Fossomhronia echinata a prominent labyrinth is present in both the sporophyte and gametophyte placental cells.
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translocated across the whole sporophyte surface; the calyptra cells, that have dense cytoplasm rich in mitochondria, may play a major role in this process. C. ANTHOCEROTES (Anthocerotopsida)
The anthocerotes or hornworts comprise about 100 species that currently are classified into five or six genera, i.e. Phaeoceros, Notothylas, Folioceros, Anthoceros, Megaceros and Dendroceros (Schofield, 1985; Hasegawa, 1988). This group is distinguished from all the other embryophytes on the basis of a range of cytological, anatomical and developmental characteristics (Crandall-Stotler, 1980, 1984), and is considered by Schuster (1984~)as an independent evolutionary line of land plants. The archegonia develop from dorsal epidermal cells and at maturity protrude slightly above the thallus surface. The egg cell is bordered by cells of the thallus, in as much as an archegonial venter, in the strict sense, is lacking (Renzaglia, 1978). Unlike mosses and liverworts, the first division of the zygote is longitudinal and produces two cells that then divide transversely. A longitudinal wall perpendicular to the first one divides the embryo into four upper and four lower cells. The upper cells then divide transversely. The resulting 12-celled embryo consists of three tiers of four cells each. In Notothylas the foot arises from the lower tier only and the middle tier functions as a short-term meristem, whereas the cells of the upper tier serve as sporangial initials (Campbell, 1918; Renzaglia, 1978). In the other genera a massive bulbous foot derives from divisions in the lower two tiers, whereas the upper tier produces both a basal meristematic zone and acropetally differentiating sporangial tissues (Renzaglia, 1978; Crandall-Stotler, 1984). When embryogenesis begins, the thallus cells adjoining the archegonium divide and form an investing involucre around the sporophyte. In Notothylas the sporophyte remains enclosed in this involucre until maturation of all the spores is complete. In the other genera the sporophyte emerges from the involucre as soon as the first-formed spore mother cells complete meiosis, and continues growing for long periods because of activity of the basal meristem (Crandall-Stotler, 1984). Unlike mosses and liverworts, where the foot achieves complete cellular differentiation during specific stages in sporophyte development, in anthocerotes cellular proliferation and differentiation at the sporophyte-gametophyte junction proceeds continuously along with sporophyte growth throughout the life-span of the latter. Figs. 57-59. The gametophyte-sporophyte junction in Metzgeriales (cont.). Fig. 57. Blasia pusilla; prominent wall labyrinths in both generations. Fig. 58. Pullavicinia indica; sporophyte wall labyrinth and thin-walled gametophyte cells. Fig. 58. Riccafdia mulr@du; thick-walled sporophyte cells and gametophyte wall labyrinths.
Anrhoceros punc~oturL.
Anlhoreros Jormosar Haseg Anrhoceros gronulosa Haseg Phaeocrros / n e w husk.
Plmeorero.~curohntonus Proak. Foltoceror JuaJo.rlornirrBharadw
Nomrhdrv orhtorlorrr Sull. Noforhvlrv emperaro Haseg
Dmdrocem co~emoxu(Haseg. Dendroreros iovonicur Nees. Dmdroceros mherculons Haft Megocerorj?agellrrrrrSteph.
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Complex }labyrinths Complex labyrinths Complex }labyrinths Simple labyrinths Simple lahynnth
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T A B L E VI Cytoplasmic features of placental cells in anthocerotes Plastids Gametopbyre Shape Anrhoceros pwcIuNs Anrhocernr fonnosoe A~irhoc~ror gronulosu
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Phoeocrror Iowa Phveocerm corobnionur Folmeerosfurrformu
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Sporophyte Plastoglobuli
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Abbreviations. n gr . normal grana; r.gr ,rudunentalygrana: pyr , pyrenoid.
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Spheroidal }pieumorpixuc Spheroidal pleomorphic ptxmd
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The foot is ovoidal (Megaceros, Dendroceros; Fig. 93) or bulbous in the other four genera (Figs. 94 and 95) and generally 0.5-0.7mm in diameter except in Notothylas and Dendroceros (0.25-0.4 mm in diameter). The organization of the placenta is fundamentally the same in all the genera and comprises long and branched haustorial cells of sporophytic origin intermingled with gametophyte cells (Figs. 96,97,99 and 101). The two cellular types are separated by abundant intercellular spaces containing PASpositive mucilage, that enlarge locally forming wide lacunae. As in mosses and liverworts, the placental cells are highly specialized and clearly distinct from the other cells of the respective generation. The haustorial cells have uniform and relatively thin walls. They penetrate the gametophyte tissue by intrusive growth involving both cell division and elongation (Gambardella and Ligrone, 1987). The nucleus generally lies and divides far from the growing tip (Fig. 97), and this may branch with (Figs. 96 and 101) or without (Fig. 97) the formation of cross walls. The haustorial cells are highly vacuolated in Megaceros, whereas they contain less prominent vacuoles and more abundant cytoplasm in Anthoceros, Phaeoceros and Folioceros. Numerous vacuoles of small sizes occur in the haustorial cells of Notothylas (Fig. 101) and Dendroceros (Fig. 96). In all genera but Notothylas the haustorial cells contain large spheroidal or irregularly shaped plastids with a rudimentary thylakoid system, abundant plastoglobules, sometimes spherical starch grains and vesicles of various sizes (Vaughn et al., 1992; Figs. 97 and 98). The haustorial cells of Notothylas contain chloroplasts with a well-developed inner membrane system (Fig. 101) and sometimes a distinct pyrenoid, though less prominent than in other vegetative cells of the thallus. The gametophyte placental cells are much smaller than ordinary parenchyma cells of the thallus, have dense cytoplasm with several relatively small vacuoles and are rich in endoplasmic reticulum, dictyosomes and mitochondria which form prominent aggregates in Phueoceros carolinianus (Fig. 102). At maturity they present wall ingrowths of variable sizes, generally along the cell sides abutting intercellular spaces. Wall labyrinths of considerable complexity are found in Phaeoceros, Notothylus and Folioceros (Figs. 99 and 101), whereas in the other genera they are much simpler (Fig. 96). In all genera except Dendroceros the plastids lack starch and have rudimentary thylakoid systems and the pyrenoid is highly reduced or absent (Fig. 102). In the gametophyte placental cells of Dendroceros are
Figs. 60-63. The gametophyte-sporophyte junction in Mctzgeriales (cont.). Fig. 60. Riccardia mulfifidu;thickened tangential walls with radial deposits, sporophyte placental cell. Fig. 61. Pelliu epiphyllu; thin-walled placental cells in both generations. Fig. 62. Cryprofhullus mirubilis; wall ingrowths are absent. The intraplacental space contains collapscd garnetophyte cells (arrowed). Fig. 63. Aneuru pinguis: nacreous wall thickenings in the sporophyte placental cells.
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chloroplasts with a well-developed thylakoid system but lacking a pyrenoid (Fig. 100). Dense bodies with a crystalline substructure are present in large amounts in the intercellular spaces, most notably in the large lacunae, of the placenta in Phaeoceros, Notothylas and Folioceros (Figs. 103-106). These structures react positively to protein stains (Marsh and Doyle, 1985) and are completely digested by pronase or pepsin (Fig. 104), hence they are assumed to be protein (Gambardella and Ligrone, 1987). In longitudinal or oblique sections the crystals consist of alternating dense and light bands. Transverse sections reveal a regular network of hexagonal subunits, approximately 15nm wide, with a light internal core (Fig. 103). Degradation of the crystals has been observed in Phaeoceros and Notothylas (Fig. IOS), notably at advanced stages in sporophyte development, and it has been suggested that these structures may serve as a source of nutrients for the sporophyte growth (Marsh and Doyle, 1985). The larger lacunae in Phaeoceros and Folioceros are formed by dissolution of gametophyte placental cells, a process that presumably is induced by the haustorial cells (Gambardella and Ligrone, 1987). Degeneration of gametophyte cells follows their symplasmic isolation from the adjoining cells, due to the severance of plasmodesmatal connections. Crystals are deposited in the vacuoles of gametophyte cells (Fig. 106) and are liberated in the placental lacunae as a consequence of cellular dissolution. Crystals are but rarely observed in the placenta of Megaceros and are not found in Anthoceros and Deridroceros. Both sporophyte and gametophyte placental cells of Dendroceros contain intravacuolar deposits of dense amorphous material (Fig. 98) that is assumed to be protein in as much as it is negative to the PATA test for carbohydrates and sensitive to digestion by pronase (Ligrone and Renzaglia, 1990). Similar protein deposits also occur in the parenchyma cells of the foot and virtually all the cells of the sporophyte capsule, including the spores. Overall, these observations suggest that protein is synthesized in the haustorial cells, presumably from precursors provided by gametophyte transfer cells, and is then transferred, via plasmodesmata, to the parenchyma cells of the foot and eventually to the cells of the growing capsule. Like the protein crystals in Phaeoceros and Folioceros, the amorphous protein deposits in the gametophyte placental cells of Dendroceros may function as a source of amino acids for the sporophyte, although they are never found free in placental spaces (Ligrone and Renzaglia, 1990). Figs. 64-67. The gametophyte-sporophyte junction in Metzgeriales (cont.). Fig. 64. Cryptorhallus mirabilis; highly irregular plasmalemma in a gametophyte placental cell. Fig. 65. Riccardia mulrificla: giant mitochondrion in a sporophyte placental cell. Fig. 66. Cryplorhullus mirabilis: grazing section of endoplasmic reticulum with abundant attached polysomes in a gametophyte placcntal cell. Fig. 67. Cryprothallus; concentric sheets o f R E R around a lipid body in a sporophyte placental cell.
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The placental region develops very early and is well organized when the sporophyte, less than 1 mm long, is barely discernible with naked eye within the gametophyte thallus. In Phaeoceros abundant intercellular crystals are found in the placenta when the sporophyte emerges from the involucre, whereas wall labyrinths are formed in gametophyte placental cells during the subsequent phase of capsule elongation (Gambardella and Ligrone, 1987).
111. THE TAXONOMIC SIGNIFICANCE OF THE PLACENTA IN BRYOPHYTES AND IMPLICATIONS FOR PHYLOGENY Two main conclusions emerge from the comparative data described here for the first time: (a) placental organization is extremely diverse in the bryophytes as a whole; and (b) with some exceptions, it is highly constant within particular groups of bryophytes. The diagnostic features embrace not only the walls and cytoplasmic contents of the placental cells, but also the timing of their differentiation. Whereas wall characteristics render the placental regions of different groups almost absolutely distinctive, cytoplasmic features and especially plastid ultrastructure tend to be peculiar to particular genera. This remarkable diversity in placental morophology in bryophytes has no obvious (or even obscure) functional meaning. For example, the absence of transfer cells on one or both sides of the placenta can hardly be assumed to indicate a lower efficiency in solute translocation and/or greater nutritional autonomy of the sporophyte. Indeed, in taxa lacking placental wall ingrowths (e.g. Sphagnum and Pellia), the sporophytes are just as highly differentiated and spore production just as prolific as in species where these are well developed. Conversely a typical bryalean placenta is found in Archidium (Brown and Lemmon, 1985) in spite of the extreme reduction of the sporophyte in this genus (Snider, 1975). Similarly in three different bryalean orders, namely Buxbaumiales, Pottiales and Dicranales, the placental regions are just as highly differentiated in genera with rudimentary setae (Diphyscium,Phascum and Cladophascum, respectively) as in those with elongate setae. Although it is now widely accepted that transfer cell morphology is associated with intense short distance transport of solutes (Gunning and Pate, 1974), most of the evidence remains circumstantial and knowledge of the biochemical and physiological mechanisms involved in this process via Figs. 68-72. Plastids in metzgerialean sporophyte placental cells. Fig. 68. Fossombronia echinara; elongate chloroplasts. Fig. 69. Riccardia rnultifida post-meiosis; ovoid with small grana and starch grains adjacent to a giant mitochondrion. Fig. 70. Pallavicinia indica; prolamellar body with radiating grana. Fig. 71. Riccardia mult@da pre-meiosis; ovoid and pleomorphic with single thylakoids. Fig. 72. Cryptothallus; pleomorphic undifferentiated plastids.
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the wall labyrinths has barely increased since the 1970s. Electrophysiological studies of the foot transfer cells in Polytrichum (Caussin et al., 1979, 1982, 1983; Renault et al., 1989) have demonstrated that protonelectrochemical gradients are generated through the wall-membrane apparatus and used to energize the uptake of solutes, particularly amino acids, from the apoplast. However, similar mechanisms also operate equally well in cells lacking wall ingrowths (Despeghel and Delrot, 1983; Kinraide et al., 1984). In the latter context it should be noted that the ultrastructure of thickened placenta walls with radial bands in Sphagnum, Polytrichales, Andreaea, Takakia, Jungermanniales and Riccardia is remarkably similar to that of the microspore intine in angiosperms (Charzynska et al., 1990; Murgia et al., 1991). Not only is the intine freely permeable to solutes, but recently the microspore has also been recognized as a type of transfer cell (Charzynska et a l . , 1990). The same kind of wall ultrastructure also characterizes vessel contact cells in the xylem of herbaceous angiosperms (Mueller and Beckman, 1984). Against a background of these functional considerations, the simplest explanation for the range of highly distinctive placental morphologies found in bryophytes is that each arose independently early in the evolution of each group. Once an effective transport system, with or without transfer cell morphology, had become established between the gametophyte and developing sporophyte, intense selection pressure for further change would disappear. Thus the ancestral condition would likely be retained more or less unchanged throughout the subsequent evolutionary history of each group. Clearly implicit in this hypothesis is the possibility that transfer cell morphology and other apparently similar placental features may not be homologous throughout bryophytes. Indeed, structural and temporal differences in wall ingrowth morphology and development strengthen this notion. Thus, with the exception of the Calobryales, early versus late differentiation of transfer cell morphology sets mosses clearly apart from hepatics. The fine dense wall labyrinths in Jungermanniales are very different from the coarse more transparent ingrowths in the Marchantiidae. Physiological studies are now needed to discover whether the temporal differences in placental transfer cell differentiation reflect differences in the availability of solutes destined for export from the gametophyte (see Gunning et al., 1968; Pate et al., 1970; Davey and Street, 1971; Gunning and Pate, 1974; Henry and Steer, 1980; for examples of the coincidence of wall Fig. 73. Cryptorhullus; highly pleomorphic undifferentiated plastid in a gametophyte placental cell. Figs. 74-76. The gametophyte-sporophyte junction in Calobryales. Fig. 74. Huplomitrium hooker;; wall ingrowths are more extensive in the sporophyte. Fig. 75. Calobryum blumei; a more cxtensive wall labyrinth in the sporophyte. Fig. 76. Calobryum blumei; dead cells with electron-dense deposits lining their walls in the central region of the foot.
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Figs. 77-79. Plastids in calobryalean placental cells. Fig. 77. Culobryum blumei sporophyte; pleomorphic plastids with starch and rudimentary grana. Fig. 78. Haplomitriurn hookeri sporophyte; a single highly pleomorphic plastid. Fig. 79. Calobryum blumei gametophyte; pleomorphic plastid with grana perpendicular to the long axis.
T H E G A M E I ’ O P ~ I Y I ‘ E - S P O R O P I ~ Y ‘JUNCTION r~
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ingrowth development with the presence of solutes destined for export in vascular plants). Similarly, cytochemical investigations aimed at elucidating the biochemical basis for the structural differences between the labyrinths of different groups may help to establish whether or not these are homologous. Bearing in mind the difficulties in distinguishing between parallel evolution and homology, it is nevertheless possible to draw major taxonomic conclusions from placental morphology and it is highly pertinent to explore the implications for phylogeny. Three basic types of placenta may be identified in mosses: an Andreaeatype, present in the Andreaeales, Takakiales and Polytrichales, a Sphugnum-type, restricted to Sphagnales, and a bryalean type, characteristic of the Bryales and also present in the Tetraphidales. Each type is sharply distinct from the others since the different distribution or absence of transfer cells can be immediately recognized, at least at the ultrastructural level (Table I). Minor variants are found within each type or group, for example the radially elongate foot transfer cells of Bryum and the rhizoidlike outgrowths of Diphysciurn. On the whole, however, the placental organization is remarkably constant even in the exceedingly large group of the Bryales, where taxonomically distant genera present little or no appreciable differences. A greater intergeneric diversity is apparent in the Polytrichales, especially in the gametophyte, perhaps indicating that this order is of considerable antiquity. The highly distinctive placental organization of the Sphagnales reinforces the notion that this is the most divergent group in mosses (Crosby, 1980; Brown et al., 1982; Duckett et al., 1982, 1984; Robinson and Shaw, 1984; Ligrone and Renzaglia, 1989). On the other hand, the discovery that the Andreaeales and Polytrichales share a similar placenta places the former clearly apart from the Sphagnales (cf. the “Pseudopodiate line” devised by Kumar, 1984) and closer to bryalean mosses. The presence of the same basic type of placenta in all the Bryales (with the only known exception, Dicranum majus, almost certainly representing a derived condition) confirms this group, including the Buxbaumiales and Tetraphidales, as a monophyletic unit. The discovery of a bryalean placenta in Tetraphis, previously reported as having labyrinthine walls in the sporophyte only (Roth, 1969), is in line with the notion, based o n studies of spermatid morphology (Duckett et af., 1982) and peristome development (Edwards, 1984; Shaw and Anderson, 1988), of a closer phylogenetic relationship between the Tetraphidales and arthrodontous mosses rather than between either group and the nematodontous Polytrichales. Likewise, the Buxbaumiales possess an arthrodontous peristome (Edwards, lY84; Shaw et ml., 1987) and a typical bryalean placenta. If we assume that placental transfer cells are plesiomorphic in embryophytes (see above) and that the Andreaeales and Polytrichales are primitive to the Bryales (Crosby, 1980; Robinson and Shaw, 1984), then the
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Andreaea-type of placenta appears to be the most likely ancestral type in mosses, with the other two types being derived (see also Ligrone and Renzaglia, 1989). This conclusion is strongly supported by the discovery of a placenta of the Andreaea-type in Takakia, a taxon that has long been classified in the Calobryales (Schuster, 1984b). Such a striking congruence between placental morphology and the anatomical features of the newly discovered antheridia and sporophyte in Takakia is a further confirmation of placental morphology as a taxonomically valuable character. Taxonomic and phyletic relationships between major groups in liverworts are more uncertain than in mosses. For example, it is still debated whether liverwort evolution has proceeded from leafy towards thalloid forms or vice versa. Schofield (1985) thinks of the gametophyte of a hypothetical ancestral liverwort as a flattened dorsiventral thallus with sex organs exposed on the dorsal surface, a model that is most closely approached by the Metzgeriales. Mishler and Churchill (1985) also believe that the ancestral type in liverworts is a simple thalloid gametophyte, though they construct a cladogram where the Metzgeriales and Jungermanniales are considered advanced and the Sphaerocarpales and Marchantiales primitive. Schuster (1984b) observes that the passage from a leafy to a thalloid habit has probably occurred several times independently in different liverwort groups, and suggests that the great diversity of gametophytic types may ultimately be derived back to a simple radial, leafless type. O n the basis of a wide range of characters, he recognizes a “primary dichotomy” between two subclasses, the Jungermaniidae (comprising the Jungermanniales and Metzgeriales) and the Marchantiidae (including the Sphaerocarpales and Marchantiales), with deviations from this generalization occurring principally in three taxa, i.e. Haplomitrium, Takakia and Monoclea. Placental morphology confirms the Jungermanniales and Marchantiidae as taxonomically well-delimited groups but sheds less light on possible inter-relationships between the Jungermanniales, Marchantiidae and the Calobryales. Unlike the ultrastructural uniformity in the appearance of the placental wall labyrinths in bryopsid mosses, their great variability in liverworts renders interpretation of homology, or lack of it, between transfer cells in different groups more problematic. The fine dense labyrinths in the sporophyte placenta of Jungermanniales are very different from the coarse electron-transparent ingrowths that characterize both generations in
Figs. 80-84. The garnetophyte-sporophyte junction in Marchantiidae. Figs. 80-82. Monoclea gottschei. Fig. 80. Light micrograph, longitudinal scction showing the obtuse conical foot. Fig. 81. Coarse electron-transparent wall labyrinth in garnetophyte placental cells. Fig. 82. Wall labyrinth in a sporophyte placental cell. Fig. 83. Sphaerocarpos texanus; wall labyrinths in placental cells of both generations. Fig. 84. Dumortiera hir.suta; short wall protuberances in the garnetophyte and extensive wall ingrowths in the sporophyte. Note the collapsed garnetophyte cells (arrowed).
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Marchantiidae. The ultrastructure of the calobryalean wall ingrowths is somewhat intermediate. The occurrence of sporophytic wall ingrowths and a tendency for the gametophytic placental cells to form thickened outer walls in 10 genera of the Jungermanniales ranging from putatively primitive (e.g. Herberta) to highly advanced (e.g. Zoopsis) (Schuster, 1984b) suggests that this is the ancestral condition in the group. The absence of transfer cell morphology in Radufa is almost certainly a derived condition perhaps related to interdigitation of the cells of the two generations instead of the clearly defined intraplacental lacuna seen in all the other genera. It would now be pertinent to discover whether this feature is peculiar to the Radulaceae, or if it also occurs in the allied families Porellaceae, Jubulaceae and Lejeunaceae. The uniformity in placental ultrastructure in the Marchantiidae which, with the exception of Riccia, extends throughout its three highly disparate orders Marchantiales, Sphaerocarpales and Monocleales, is clearly in accord with the widely recognized anatomical and development uniformity of this subclass (Brown and Lemmon, 1988, 1990; Crandall-Stotler, 1981; Schuster, 1984a,b). The occurrence in Carrpos of a placenta no less highly differentiated than in other members of the group weakens the case for a possible link with Riccia (Proskauer, 1961). Indeed, the absence of any trace of a placenta sets Riccia apart from all other archegoniates and from Coleochaete, the taxon generally considered to be the closest living algal relative to the embryophytes (Graham and McBride, 1979; Graham, 1982,1984,1985; Graham and Wilcox, 1983; Graham and Wedemayer, 1984; Graham and Taylor, 1986; Duckett and Renzaglia, 1988a; Delwiche et al., 1989; Vaughn et a f . ,1992). However, it must be stressed that the information for Riccia is based on a single species. The possible future discovery of the vestiges of a placenta elsewhere in the genus would be an unequivocal demonstration that the sporophyte of Riccia represents the end of a reduction series rather than an ancestral condition. The Metzgeriales are by far the most diverse group of liverworts and include several isolated entities whose affinities are highly problematic (Crandall-Stotler, 1981; Renzaglia, 1982; Schuster, 1984b; Brown and Lemmon, 1988; Carothers and Rushing, 1988). This diversity is almost certainly related to the extreme antiquity of the group, the fossils of which date back at least to the upper Devonian (Krassilov and Schuster, 1984). Although the wide range of placental morphologies further underlines the profound intersubordinal, interfamilial and even intergeneric discontinuities within the order, evaluation as to which of the variations represents Figs. 85 and 86. The gametophyte-sporophyte junction in Marchantiidae (cont.). Fig. 85. Reboulia hemisphaerica; more extensive wall ingrowths in the sporophyte. Fig. 86. Carrpos monocarpos; short wall protuberances in the gametophyte and normal chloroplasts in the placental cells of both generations.
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the primitive condition is at present highly speculative. Perhaps the most plausible choice is the condition found in Blasia and Fossombronia (wall labyrinths in both generations) in as much as these are generally considered to be representatives of very old isolated taxa (Schuster, 1984b). Starting from the condition found in such genera as Blasia and Fossombronia, variant types might have evolved through the suppression of transfer cells in either the gametophyte (Pallavicinia) or the sporophyte (Riccardia) or both (Pellia, Aneura and Cryptothallus). The similarity in placental organization between the Calobryales and putatively primitive members of the Metzgeriales is in accord with Schuster’s (1984b) notion of a common, albeit extremely remote, ancestry for these two groups. On the other hand the fact that putatively primitive members of the Metzgeriales share a similar placental organization with the Marchantiidae might be indicative of a closer phyletic relationship between simple and complex thalloid liverworts than between either group and the Jungermanniales. This possibility is substantiated by ontogenetic data (Crandall-Stotler, 1981) and is closely in line with recently recognized affinities between Blasia and Marchantiidae. Most notable of these are marchantialean-like spermatozoids (Renzaglia and Duckett, 1987a,b), the presence of two rows of ventral scales, the location of the archegonia, sporophyte development, apical organization (Renzaglia, 1982) and monoplastidic spore mother cells (Brown and Lemmon, 1992). However, it must be noted that, as long as the foot is considered to have different embryological origins in the Metzgeriales and Marchantiidae groups (see Section I.B), the placentas in these two groups cannot be considered homologous and therefore are not strictly comparable in the context of phylogeny. The Jungermanniales are given a near ancestral position in liverwort phylogeny by Schuster (1979, 1984b), a conclusion that appears supported by recent comparative analyses of spermatogenesis (Duckett et al. , 1982, 1984; Renzaglia and Duckett, 1991). In accord with these data, the jungermannialean placenta might be the ancestral type in liverworts. This possibility is supported by the striking similarity with the Andreaea-type in mosses. In addition to transfer cells only in the sporophyte, the Jungermanniales, Andreaeales, Takakiales and Polytrichales share a similar substructure in gametophyte placental cells, namely thickened tangential walls with radially arranged deposits of dense material. This perhaps suggests a closer phyletic relationship between the Andreaeales-Takakiales Figs. 87-90. The gametophyte-sporophyte junction in Marchantiidae (cont.). Fig. 87. Rebouliu hernisphuerica; plastids with fibrillar bundles (arrowed) parallel to the long axis in a gametophyte placental cell. Fig. 88. Reboulia; longitudinal section through membrane-bound bundles of tubules in a gametophyte placental cell. Fig. 89. Reboulia; transverse sections through membrane-bound bundles of tubules. Fig. 90. Riccia sorocurpa; light micrograph, longitudinal section of a sporophyte containing spore tetrads. The capsule is completely enclosed in the gametophyte thallus. The archegonial neck is arrowed.
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Figs. 91 and 92. The gametophyte-sporophyte junction in Marchantiidae; Riccia sorocarpa (cont.). Fig. 91. Section through the margin of a young sporophyte. C, two-layered calyptra; J , jacket and nurse cells; SMC, spore mother cell. Fig. 92. Section through the margin of a nearly mature sporophyte. Note the abundant lipid reserves in the spore tetrad (T), the collapsed inner layer of calyptra cells (arrowed) and the thickened walls of the thallus cells (G) facing the calyptra. Figs. 9>95. The gametophyte-sporophyte junction in Anthocerotes. Light micrographs, longitudinal sections. Fig. 93. Megaceros flagellark; ovoidal foot. Fig. 94. Anthoceros formosae: bulbous foot. Fig. 95. Notothylas temperata; smaller bulbous foot than Anthoceros.
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group and Jungermanniales than either the Marchantiidae or the Metzgeriales. This would imply a common origin for mosses and liverworts, from an ancestal form probably represented by an erect, radially symmetrical leafy gametophyte with terminal sporophytes. However, it should also be noted that the same distinctive wall substructure of dense radial bands also turns up in the sporophyte placental cells of Riccardia, a metzgerialean genus generally considered to be advanced (Schuster, 1984b), and in gametophyte placental cells of Sphagnum (Ligrone and Renzaglia, 1989). The possibility that this feature is merely associated with solute permeability rather than indicative of phyletic affinity should not be dismissed. In contrast to mosses and liverworts, the anthocerotes all exhibit the same, highly distinctive type of placenta, with minor variants mainly concerning plastid morphology and the presence, appearance and localization of protein deposits. This uniformity in placental organization emphasizes the homogeneity of this group and its separation from mosses and liverworts, as indicated by a wealth of anatomical, ultrastructural and developmental data (Crandall-Stotler, 1980, 1981, 1984; Duckett et a f . , 1982, 1984; Schuster, 1 9 8 4 ~ ;Carothers and Rushing, 1988; Duckett and Renzaglia, 1988a, 1989). The variations in placental morphology in anthocerotes appear to by very useful both for elucidating intergeneric affinities and for clarifying generic limits. The distinctive protein crystals found in Phaeoceros, Notothylas and Folioceros suggest close affinity between these genera. This contradicts the classification of anthocerotes recently proposed by Hasegawa (1988), where the family “Notothyladaceae”, comprising Notothyfas as the only genus, is separated from the family “Anthocerotaceae”, which includes Phaeoceros, Folioceros, Anthoceros and Megaceros. Recent ultrastructural studies of spermatozoid morphology and development have revealed close similarities between Phaeoceros and Notothyfus (Renzaglia and Duckett, 1988, 1989), although the lack of information on other genera presently precludes wider evaluation of the taxonomic relevance of male gamete microanatomy . The distinctive ultrastructural characteristics of the placenta in Dendroceros seemingly support the isolation of this genus in a separate taxonomical entity, e.g. the family Dendrocerotaceae as proposed by Hasegawa (1988).
IV. PTERIDOPHYTES By contrast to the wealth of comparative ultrastructural data on the gametophyte-sporophyte junction in bryophytes, knowledge of the embryology and the early stages in sporophyte differentiation in pteridophytes is limited exclusively to light microscope studies, the majority dating from the nineteenth century or the first half of the twentieth century and reiterated
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with little or no additional information in reviews and standard textbooks (Wardlaw, 1965; Bierhorst, 1971; Gifford and Foster, 1989). In these accounts it is usually tacitly assumed that the foot is the major site of exchange between gametophyte and sporophyte generations, but supporting experimental and or cytological data are lacking. More recent studies on the causal basis of the alternation of generations in pteridophytes (see reviews by Sheffield and Bell, 1987, 1989) have focused on the cytology of oogenesis and to a lesser extent on apospory and apogamy and do not consider the placental region. However, it is interesting to note that transfer cell morphology appears to be absent at the base of apogamous sporophytes in ferns whereas the cells initiating apogamous sporophytes in the moss Physcomitrium develop labyrinthine wall ingrowths even though a recognizable placenta is absent (Menon and Bell, 1981; La1 and Narang, 1985). Specific information on the placenta of pteridophytes is limited to a mention without micrographic details by Gunning and Pate (1974) of transfer cells in this region in Equisetum, two brief accounts of three ferns Polypodium, Adiantum (Gunning and Pate, 1969b) and Pteridium (Khatoon, 1986), and two very recent studies of Lycopodium (Peterson and Whittier, 1991; Duckett and Ligrone, 1992). Although these works clearly do not form a suitable basis for an incisive appraisal of the taxonomic and possible phylogenetic significance of the placenta in the different groups of pteridophytes and do not permit a comparison between these and other embryophytes, the fragmentary information they contain indicates a most fruitful area of enquiry for the future. In Polypodium and Adiantum wall ingrowths in both gametophyte and sporophyte develop very early, before the expansion of the first leaf, elongation of the root and differentiation of the first xylem: precisely the stage at which the sporophyte is most dependent on the gametophyte for nutrients (Gunning and Pate, 1969b). The ingrowths are more abundant and labyrinthine in the sporophyte in Adiantum and Pteridium, while the opposite occurs in Polypodium. The ingrowths are more highly developed on the tangential walls along the interface but also extend onto the lateral walls in the sporophytic cells in Adiantum and Polypodium. The sporophytic cells, but not those of the gametophyte, contain abundant starch, a situation probably reflecting sugar translocation from the gametophyte to the sporophyte. Unlike mosses and liverworts, where a clear-cut demarcation zone is generally interposed between the sporophyte and gametophyte, in ferns the Figs. 96-9X. The garnetophyte-sporophyte junction in Anthocerotes (cont.). Fig. 96. Dendroceros tubercularis; gametophyte transfer cells and sporophyte haustorial cells. Note the chloroplasts in the former. Fig. 97. Dendroceros tubercularis; branched sporophyte haustorial cell. Note the undifferentiated plastids. Fig. 98. Megacerosjfagellaris;undifferentiated plastids in a sporophyte haustorial cell and crystals (arrowed) in the adjacent garnetophyte cell.
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Figs. 99 and 100. The gametophyte-sporophyte junction in Anthocerotes (cont.). Fig. 99. Phaeoceros luevis; gametophyte transfer cells, sporophyte haustorial cells and placental lacunae (arrowed). Fig. 100. Dendroceros tuberculuris; plastid in a gametophyte transfer cell.
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cells of the two generations interdigitate and mucilage-containing intraplacental species appear to be lacking. Further differences between bryophytes on the one hand and ferns and Lycopodium (see below) on the other are an absence of dead and collapsed cells along the interface and the lack of any evidence for the renewal of the placental cells. These differences are perhaps related to the transient nature of sporophytic dependence on the gametophyte in pteridophytes. Intercellular spaces are lacking in the placental region of Lycopodium uppressum (Chapm.) Lloyd & Underw: the cells of the two generations lie close together or are separated by electron-dense intercellular material (Peterson and Whittier, 1991). As in bryophytes and seed plants (see Section V), symplastic isolation, initially established during the early stages in the differentiation of the axial row in the young archegonium (Bell, 1989), characterize all stages of sporophyte development in pteridophytes. In the foot region of Lycopodium uppressum there is little or no interdigitation of the cells of the two generations and the contiguous walls of both sporophyte and gametophyte develop coarse labyrinthine ingrowths of low electron opacity very similar ultrastructurally to those in the marchantialean placenta. Subsequently the interstices become occluded by dense amorphous wall material. The sporophyte-gametophyte junction in Lycopodium cernuum L. is somewhat different. Here the interface between the two generations, which develops ingrowths but to a more limited extent than in L. uppressurn, is not a special lateral development of the early embryo (i.e. a foot region) as in other species of Lycopodium (Goebel, 1905), but rather the lower part of the primary embryonic axis derived from the suspensor (Duckett and Ligrone, 1992). The homologue of the foot in L. cernuum, in terms of its lateral position and early appearance in sporophyte differentiation, is the protocorm. This juvenile structure lies outside the confines of the parent gametophyte and presumably derives its nutrition partly from photosynthesis and partly from an endophytic fungus. Of particular interest in the present context is that within the protocorm there develop schizogenous, mucilage-filled intercellular spaces closely similar to those in the placental region of bryophytes. These lacunae are the principal habitat of the mycobiont. Although the protocorm cells do not develop wall ingrowths, their invasion by the fungus is associated with the production of massive overgrowths of host cell wall material with a texture similar to that forming the wall thickenings in the gametophytic placental cells of Sphagnum and Jungermanniales. The major differences between the sporophyte-gametophyte junction in two species of Lycopodium on the one hand reflect the considerable antiquity of this genus, and on the other perhaps anticipate diversity in placental morphology in pteridophytes parallelling that in bryophytes. It will now be particularly interesting to discover whether wall ingrowths are also present
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along the margins of the well-developed suspensor present in many species of Selaginellu (Bierhorst, 1971) and to investigate the position and sites of nutrient exchange between gametophyte and sporophyte in the haustorialike foot region of Tmesipferis (Holloway, 1918).
V. SEED PLANTS The classic reviews on transfer cells (Gunning and Pate, 1969a, 1974; Pate and Gunning, 1972; Gunning, 1977) underline the cytoplasmic discontinuities between sporophyte and megagametophyte, between embryo and megagametophyte and between sporophyte and developing microspores (also see Charzynska et al., 1990; Murgia ef al., 1991; Pacini, 1990 for discussion of structural and functional interrelationships between tapetum and microspores) as posing special problems for the transport of solutes. Gunning and Pate go on to point out that, in view of the complex nutritional relationships, plus the fact that the new gametophyte and sporophyte are both parasitic on the parent sporophyte, it is not surprising to find transfer cells in these situations. Indeed, transfer cell morphology has now been described at virtually every site of probable solute exchange via the apoplast in the female reproductive organs of angiosperms (Table VII). In a few situations the zones of transfer cells face each other along the intergenerational apoplastic gap, but more commonly only the receptor surface bears the ingrowths. Sometimes the boundary between the two generations is a common wall lacking plasmodesmata, but more often these are separated by a space containing remains of dead or dying cells. The diverse locations and temporal differences in the development of wall ingrowths during the ontogeny of the various tissues provide perhaps the strongest circumstantial evidence of transfer cell activity in solute transport. As in the placentas of most bryophytes and pteridophytes, it seems to be an anatomical necessity that nutrients directed to the growing sporophyte have to pass through cells with wall ingrowths. Rather than reiterate the substance of the earlier reviews, this account focuses on some of the more significant discoveries since 1977, compares the present stage of knowledge of the gametophyte-sporophyte junction in seed plants with that in bryophytes and pteridophytes and points to areas urgently needing further study. As in bryophytes, in seed plants there are also virtually no physiological data to validate inferences about routes and timing of solute transport based almost entirely on the formation of wall labyrinths. It is, however, Figs. 101 and 102. The gametophyte-sporophyte junction in Anthocerotes (cont.). Fig. 101. Notothylus orbicularis; sporophyte haustorial cells and gametophyte transfer cells. Fig. 102. Phoeoceros carolinianus; mitochondria1 aggregates and a pleornorphic plastid in a gametophyte transfer cell. A small pyrenoid is arrowed.
TABLE VII Occurrence and likely functions of transfer cells in the female reproductive organs of angiosperms. Modified and updated from Pate and Gunning (1972) and Gunning (1977) Organ or tissue
Embryo sac
Young embryo
Location
Probable function
Distribution
Recent references"
Egg cell, micropylar walls
Functions of synergids taken over by egg cell when synergids absent
Plumbag0
2,7,24
Antipodals, chalazal walls Synergids, micropylar walls The so-called filiform apparatus
Nutrition of embryo sac
Several genera
1,10,24
Nutrition of embryo sac
Several genera
Central cell, outer walls at micropylar pole chalazal region
Nutrition of embryo sac
Glycine, Scilla, Helianthus
5,6,7,16,17,23,26
Suspensor. outer walls
Nutrition of young embryo Nutrition of young embryo
Several genera
4,5,12,13,18,27
AIisma
3
Basal cell at micropylar pole
Chemotropic secretion, guidance of pollen tube
1,4,7,8,9,13,14, 15,19,20,24
Older embryo Nucellus Endosperm
Cotyledon epidermis, outer walls Epidermis near base of embryo Inner and outer faces Outer walls facing perisperm Aleurone, outer face
Integument
Inner face of inner
Nutrition of embryo
Some Leguminosae
21
Nutrition of embryo
Glycine, Triticum
5.22
Nutrition of embryo
Some Leguminosae and Cruciferae Mesern bryunthemuni
10,11,12
Nutrition of embryo Nutrition of embryo Facilitating viviparous germination and possibly salt exclusion Transfer to endosperm andlor embryo
21
Caryopses of Gramineae Rhizophoru
21
Some Leguminosae,
5
Glycine
25
"References: 1. Bhandari and Sachdeva (1983); 2. Bing-Quan Huang et al. (1990); 3, Bohdanowicz (1987): 4, Dute el al. (1989); 5 , Folsom and Cass (1986); 6. Folsom and Petersen (1984); 7. Kapil and Bhatnagar (1981); 8, Kennell and Horner (1985a); 9. Kennell and Horner (1985b); 10, Mansfield and Briarty (1990a); 11, Mansfield and Briarty (l990b); 12. Mansfield and Briarty (1991); 13. Mansfield er al. (1991); 14. Mogensen (1972); 15, Mogensen and Suthar (1979); 16, Newcomb (l973a); 17, Newcomb (l973b); 18, Newcomb and Fowke (1974); 19, Newcomb and Steeves (1971); 20, Olsen (1991); 21, Pate and Gunning (1972); 22, Smart and O'Brien (1983); 23, Tilton efal. (1984); 24. Willemse and Van Went (1984); 25, Wise and Juncosa (1989); 26, Yan eral. (1991); 27. Yeung and Clutter (1979).
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noteworthy that maize somatic embryos and embryos developing in vitro (Schel and Kieft, 1986; Fransz and Schel, 1991) appear to lack transfer cells. In Phoenix dactylifera L . differences in the acid phosphatases suggest that phosphate metabolism in the endosperm is independent of that in the cotyledon haustorium, and that acid phosphatases for endosperm phosphate metabolism are not secreted by the embryo nor by the cotyledon haustorium, but instead are stored in the endosperm (Sekhar and De Mason, 1989). There is now a pressing need to identify the specific nature of the metabolites undergoing import into young embryos via the various transfer cell zones (Table VII). Although relating to only two stages in development, the wealth of comparative information on the placenta in bryophytes forms the basis for wide-ranging taxonomic inferences. In angiosperms, by contrast, the situation is very different. A few very detailed developmental studies on a small number of genera, particularly Arabidopsis (Mansfield et a f . , 1991; Mansfield and Briarty, 1991), Capsefla (Schultz and Jensen, 1968a,b, 1969, 1971), Gfycine(Kennel1 and Horner, 1985a,b; Folsom and Cass, 1986; Dute et al., 1989) and Helianthus (Newcomb and Steeves, 1971; Newcomb, 1973a,b; Yan et al., 1991), reveal major differences in the extent and distribution of the wall ingrowths even between closely related genera. These relate partly to different patterns of embryo development and partly to differences in the location of seed storage reserves (e.g. cotyledons, perisperm or endosperm). Only one author (Mikeswell, 1990) attempts comparisons from a taxonomic standpoint. Mikeswell’s (1990) extensive survey of angiosperm families indicates that the differentiation of micropylar and chalaza1 haustoria from embryo sacs or endosperm is primarily confined to sympetalous plants with cellular endosperm and anatropous, unitegmic and tenuinucellate ovules. The presence of endosperm haustoria characterizes the subclass Asteridae, which includes the Plantaginales. The Plantaginaceae seems well aligned with families within the Scrophulariales. Mikeswell’s final conclusion, that the utilization of haustoria as an important embryological character in taxonomy would seem to be warranted, suggests the same could well be true for other transfer cell locations when data are available for more taxa. Ultrastructurally the vast majority of the wall ingrowths associated with the female reproductive tissues in angiosperms are coarse with a transparent matrix like those in the Marchantiidae. However, in rare instances, e.g. the suspensor of Gfycine(Dute et a f . ,1989) they are finer and electron-dense. A highly elaborate wall labyrinth occurs in the large basal cell of the suspensor Figs. 10>10h. The gametophyte-sporophyte junction in Anthocerotes (cont.). Crystals. Fig. 103. Folioceros fuciformis; intercellular. Fig. 104. Phaeoceros luevis; intercellular crystals after digestion with pepsin. Fig. 105. Nofothylasorbicularis; intercellular. Fig. 106. Folioceros fuciforrnis; intracellular.
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of Afisma (Bohdanowicz, 1987).Thepresence of wall ingrowths is associated with cytoplasmic organization typical of transfer cells, namely abundant ribosomes, rough E R and numerous mitochondria. Very large megamitochondria have been described in young embryos of Capseffa(Schultz and Jensen, 1973) and Arabidopsis (Mansfield and Briarty, 1991). It is suggested that these may act as a reservoir for mitochondria1 DNA in relation to the rapid proliferation of mitochondria during embryo development. Although the cells along the gametophyte-sporophyte junction in angiosperms typically contain undifferentiated pleomorphic leucoplasts, with few reserve materials and rudimentary thylakoid systems, some highly unusual forms have also been described. Large plastoglobuli and prolamellar bodies characterize the endosperm plastids in Rhizophora (Wise and Juncosa, 1989). Prolamellar bodies also occur in the so-called “placental haustorium” plastids of Tropaeolum (Nagl and Kuhner, 1976). The suspensor by contrast contains plastids with an extremely dense stroma and scattered membranous vesicles. Much larger plastids with similar contents occur in the suspensor of Stelfaria (Newcomb and Fowke, 1974). Plastid tubules have been noted in the suspensors of Phaseolus and Pisum (Marinos 1970; Schnepf and Nagl, 1970). The current state of knowledge of the gametophyte-sporophyte interface in the gymnosperms is very similar to that for pteridophytes. In contrast to angiosperms, attempts to induce normal development of conifer zygotes and precotyledonary embryos in vitro have been unsuccessful (Gates and Greenwood, 1991, and literature cited therein) suggesting that a unique nutritional environment, probably involving continual variations in the physiological and chemical conditions, is required for embryo development. Although the considerable complexities of embryo development in gymnosperms are well documented at the light microscope level (Wardlaw, 1965), these have been totally ignored by electron microscopists. As far as we are aware the only report of wall ingrowths is in the basal plate wall between the oosphere cytoplasm and proembryo in Pinus (Gunning, 1977). For the future it would be interesting to discover whether or not ultrastructural differences between proembryos and embryos characterize the Gnetales, Cycads, Ginkgo and different families in the Coniferales in the same way that placental differences separate different groups of bryophytes.
ACKNOWLEDGEMENTS This review was made possible by a NATO Collaborative Grant to J . G . Duckett and K. S. Renzaglia and by a Guest Research Fellowship from the Royal Society of London enabling R. Ligrone to work at Queen Mary and Westfield College during 1989 and 1990. This financial support is most gratefully acknowledged. Collection of the specimens of Pogonatum neessii,
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Herberta spp. Zoopsis liukiuensis, Pallavicinia indica, Calobryum blumei, Dumortiera hirsuta, Folioceros fuciformis, Dendroceros javanicus and D. tubercularis used in this study was made possible by a travel grant to J. G. Duckett from the Royal Society of London and by laboratory facilities arranged by Drs M. A . H. Mohamed and A. Nasrulhaq-Boyce in the Botany Department of the University of Malaya, Kuala Lumpur. Cladophascum gymnomitrioides was collected in Lesotho by J. G. Duckett under a British Council LINK between Queen Mary and Westfield College and the National University of Lesotho. The authors also thank D. K. Smith for providing live specimens of Takakia and R. C. Brown and B.E. Lemmon for allowing the use of their embedded material of Carrpos and Monoclea.
REFERENCES Bartholomew-Began, S. E. (199 1). “A morphogenetic re-evaluation of Haplomitrium Nees, Hepatophyta”. Bryophytorum Bibliotheca 41, 1 4 8 4 . Lubrecht and Cramer, Vaduz. Bell, P. R. (1989). The alternation of generations. Advances in Botanical Research 16, 55-93. Bhandari, N. N. and Sachdeva, A. (1983). Some aspects of organization and histochemistry of the embryo sac of Scilla sibirica Sato. Protoplasma 115,170-178. Bierhorst, D. W. (1971). “Morphology of Vascular Plants”. Macmillan, New York. Bing-Quan Huang, Russell, S. D., Strout, G. W. and Lian-Ju Mao (1990). Organization of isolated embryo sacs and eggs of Plumbago zeylanica (Plumbaginaceae) before and after fertilization. American Journal of Botany 77, 1401-1410. Bohdanowicz, J. (1987). Alisma embryogenesis: the development and ultrastructure of the suspensor. Protoplasma 137, 71-83. Bold, H. C., Alexopoulos, C. J. and Delevoryas, T. (1989). “Morphology of Plants and Fungi”. Harper & Row, New York. Bold, H. C. and Wynne, M. J. (1985). “Introduction to the Algae: Structure and Reproduction”. Prentice-Hall, New York. Bower, F. 0. (1908). “The Origin of a Land Flora”. Macmillan, London. Bremer, K. (1985). Summary of green plant phylogeny and classification. Cladistics 1. 369-385. Bremer’, K., Humphries, C. J., Mishler, B. D. and Churchill, S. P. (1987). On cladistic relationships in green plants. Taxon 36, 339-349. Brown, R. C. and Lemmon, B. E. (1985). Phylogenetic aspects of sporogenesis in Archidium. Micrographs in Systematic Botany from the Missouri Botanical Garden 11, 25-39. Brown, R. C. and Lemmon B. E. (1988). Sporogenesis in bryophytes. Advances in Bryology 3, 159-223. Brown, R. C. and Lemmon, B. E. (1990). Sporogenesis in bryophytes. In “Microspores: Evolution and Ontogeny” (S. Blackmore and R. B. Knox, eds), pp. 55-94. Academic Press, London. Brown, R. C., and Lemmon, B. E. (1992). Polar organizers in monoplastidic meiosis of hepatics (Bryophyta). Cell Motility and the Cytoskeleton 22, 72-79. Brown, R. C., Lemmon, B. E. and Carothers, Z . B. (1982). Spore wall development in Sphagnum lescurii. Canadian Journal of Botany 60,23962409.
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