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The Grass Flower: Suggestions on its Origin and Evolution
Flora (1988) 181: 353-362 VEB Gustav Fischer Verlag Jena
The Grass Flower: Suggestions on its Origin and Evolution ALFREDO
E.
COCUCCI
and ANA M.
ANTON
Instituto Multidisciplinario de Biologia Vegetal, COrdoba, Argentina
Summary Analysing a large number of different grass flowers, a hypothesis is proposed to explain the floral variation found in the family. It is postulated that the interaction of the palea with the floral apex generates an area of inhibition wich substantially affects the floral apex. Depending on the mode of action in the reduction process, together with an independent phenomenon which affects the gynoecial organization, four major evolutionary patterns are recognized. The form of grass flower which has been most successful appears to be the bi-lodiculate, tri-staminate and bistigmatic, with the stamens belonging to two different cycles - the frontal from the outer whorl and the two lateral from the inner whorl.
Introduction The generally accepted idea that most grass flowers have three stamens in a single whorl is something that always disquieted us, because the spatial arrangement of the androecium does not match the expectation derived from theoretical considerations. Following our analysis of a large number of different grass flowers, we propose an hypothesis based on genetical and physiological grounds, which will, it seems to us, more appropriately explain all the variation found in the flowers of the grasses. We hope that this new concept will persuade agrostologists to revaluate the importance of the flower, one of the most stable parts of the sporophyte, in studies of grass systematics and evolution.
Materials and Methods The information used here comes from three different sources: (1) from material, mainly non-Bambusoid, already in our slide collection and prepared with regular anatomical techniques; (2) material specially prepared for this paper (mainly Bambusoids) and kindly provided by Dr. E. EDGAR (Botany Division, DSIR, Christchurch, New Zealand); it was sectioned and mounted with regular techniques for paraffin embedding, sectioning and staining; (3) examples from ARBER (1934) and CLA YTON & RENVOIZE (1986) were reproduced exactly or translated into diagrams.
Theoretical Foundations Every living organism possesses a number of more or less well defined features which become apparent during its development. The onset of the expression of such characters is determined by the hereditary constitution eN ARDLAW 1952: 126-158; D' ARCY THOMPSON 1966: 265-267). Within this context, morphogenetic processes in different grass flowers have been analysed in an effort to determine evolutionary trends. The flowers of grasses exhibit a great deal of variation in the number of floral organs, their mutual relationship, and their symmetry. The ancestral type, which is present in some members of the Bambusoideae, is portrayed as a trimerous, actinomorphic structure with three perianth parts (reduced tepals), two whorls of three stamens each, and a tri-carpellate ovary with three feathery stigmata (Figs. 1 A, 2A). Such a flower type, by reduction (simplification) and fusion, yields the
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ANTON
Fig. 1. Palea interaction zones. Dense shading: strong interaction (inhibition zone); light shading: mild interaction (Modification or retardation). A. Theoretical diagram of a suppossed ancestor of B, with indication ofthe strong palea interaction zone following a cyclic pattern; B. Diagram derived from A; C. Theoretical diagram of a supposed ancestor of D, following a zonal pattern (compression against the axis), with an indication of the strong palea interaction zone affecting the posterior lodicule and two stamens of the outer whorl, and a mild interaction with respect to the posterior stamen of the inner whorl and the frontal of the outer whorl; D. Diagram derived from C ; strong palea interactions leads to the suppression of the posterior (adaxial) lodicule and the two lateral stamens of the outer whorl, whereas the mild interaction causes a reduction in size of the two lateral lodicules, a modification of the posterior stamen of the inner whorl into a tepaloid staminode, and a delay in the appearance during ontogeny of the frontal stamen; E. Theoretical diagram of a suppossed ancestor of F, with indication of the strong palea interaction zone following a zonal pattern (lateral compression); F. Diagram derived from E. Missing appendages: X=lodicules; 0= stamens.
Grass Flower
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type that characterizes most of the grasses, i.e. a zygomorphic flower with two (occasionally three ore more) perianth elements (lodicules), three stamens, and an ovary with two feathery stigmata (Fig. 2N). Less frequent are zygomorphic flowers with a much reduced androecium, having two or even just one stamen (Fig. 2K, P, R, S and 0), and others in which the gynoecium has a single style and stigma (Fig. 2D, H, M). Finally, there are reductions which produce imperfect flowers. The current interpretation of these derived types presupposes the reduction (suppression) of the adaxial perianthial component opposite the lemma i.e. the posterior lodicule, and the suppression of the inner staminal whorl (PAYER 1857; SCHUSTER 1910; SAUNDERS 1937; DAHLGREN et al. 1985). A close analysis of the tri-androus flower (Fig. 2N) shows a spatial arrangement of its organs where two stamens are almost lateral to the ovary (lateral stamens) and a third one is anterior (frontal or abaxial stamen). The two lodicules form the most external whorl, and alternate with the frontal stamen. Several facts connected with the pattern of organization - facts that we will discuss - lead us to postulate a different interpretation. We base it upon the interaction between the palea and the floral apex such that modification, reduction or suppression of the floral organs follows a cyclic or a zonal pattern. Cyclic reduction affects all members of a whorl equally. As far as is known in grasses, cyclic palea inhibition affects only the perianth whorl (Fig. 1 A - B). Zonal simplification affects one or two sides of the floral apex because the palea primordium inhibits the development of the floral organs close to it (Fig. 1 C - F). This general hypothesis of a palea interaction zone is based on three well known principles of plant morphogenesis: (1) once formed, organs assume a role in subsequent plant development (NOZERAN et aI. 1971: 27; KINET et al. 1985: 115-116, 122); (2) the rate of development of the apical meristem of an axis may be controlled by the organ or group of organs which develop from it (NOZERAN et al. I.c.: 61); (3) the development of an axillary bud is inhibited by its axillant leaf (CHAMPAGNAT 1965: 1106-1137; SINNOT 1960: 98-102). In a way, then, the grass floral apex, because of its proximity to the palea, may be considered as the equivalent of an axillary bud under the influence of a subtending leaf. It is, however, necessary to point out that an independent phenomenon may affect the gynoecial organization in such a way that the three stigmatic branches may reduced to two or one, depending on the number of carpels which loose the ability to develop them. So, three gynoecial categories can be recognized according to the number of stigmata - three (Fig. 2 A), two laterals (Fig. 2 C), or one frontal stigma (Fig. 2D). Each of these may be affected by the palea interaction according to its type. The palea embraces the fl6wer, sometimes almost completely, and varies in shape according to the degree and orientation of the compression of the floret. Three main states can be recognized depending to palea shape, although intermediates may occur. In the first the flower has a quasi-actinomorphic pattern; there are three lodicules present, with the posterior one slightly smaller than the frontal ones; the androecium has six stamens distributed regularly in two whorls, and the gynoecium is composed of three carpels, each bearing a stigma. An example of this condition is well illustrated by Nastus (Fig. 2A, 4A) and Schizostachyum (ARBER, I.c.: 115, Fig. 39 D2). The palea has no prominent keels, and its area of insertion is quasi-circular and concentric with the floral whorls. The second state is characterized by an alteration of the flower patterns because of a change in the shape of the palea - and consequently of its area of insertion. This change in shape of the palea may be due to space constraints in the bud (ARBER I.c.: 112). Here the palea has two prominent keels and a flat internerve area, and its node is not circular since its adaxial side is flat. A general tendency directs the patterns towards a triangular shape which in practice results in a sort of oval contour (Fig. 2B, 4B), and is zygomorphic. The third condition is also zygomorphic, but the position of insertion of the palea has drastically changed through an extreme lateral compression of the floret. So the more or less triangular or oval patterns of the first two states have been changed to a narrow ellipse, where the
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keels of the palea become close. are almost fused or are actually reduced to one. Such is the case in Anthoxanthum (Fig. 1 f, 4 t) and Hierochloi! (Fig. 4 E), where in the perfect flowers the androecium has only one anterior and one posterior stamen. In these flowers, the palea has one or no central vascular bundle, and the entire structure is laterally compressed. Thus, the interaction zone of the palea is much stronger laterally than dorsally; as a result, a suppression of the two lateral stamens of each of the two whorls occurs, accompanied by the suppression of aIllodicules. Data supporting the zonal interaction hypothesis Cyclic inhibition as outlined above affects solely the perianth whorl; zonal interaction is of wider influence and may be superposed over cyclic system. Zonal interaction warrants a somehow larger exposition here. 1. Ontogeny of the adaxial lodicule. The "posterior, adaxial"lodicule of a tri-staminate flower has a different ontogenetic history from the two frontal lodicules. The former has a primordium initiation which agrees with the "stem type" of MEHLENBACHER (1970), whereas the latter each has a "dermal foliar type primordium" (MEHLENBACHER l.c.). It is interesting to note that the so-called "stem type" primordium has almost the same organization which characterizes stamen initiation (KlNET et al. 1985: 17). Thus, in our opinion, the "adaxial lodicule" should be interpreted as a staminode of foliar appearance!). Although the ontogeny of the "posterior lodicuIe" has rarely been investigated - for instance in Stipa henderson; (MEHLENBACHER I.c.) - we feel sure that its interpretation as a foliar or tepaloid staminode will represent the general case for all tri-Iodiculate grasses with three stamens. This is not new for the family, as it has been shown that in grass flowers with more than three lodicules, as in Ochlandra, the extra members appear to have been derived from aborted stamens (DAHLGREN et al. 1985: 431). 2. Direction of the reduction process. The zonal suppression of perianth organs in most cases starts towards the adaxial side, that is in the region close to the palea insertion, the posterior lodicule being the fIrst member affected, as in Oryzoideae (JACQUES-FELIX 1962: 26, Fig. 13). Should this phenomenon extend in the same direction, the staminal whorl should also be affected, and as a consequence, two members of the outer androecium together with one of the inner may be suppressed (Fig. 1C-D). In this way, the floral pattern of the typical bi-Iodiculate, tri-starninate flower is frrmly established (Fig. 2N). 3. Floral apex development. The excellent work of CHENG et aI. (1983), summarizes in a clear graphic way the sequences of events during the development of the flowers in maize. It was clearly shown that the order of appearance of the primordia is: (i) the lateral stamens; (ii) frontal stamen; (iii) two laterallodicules; and later (iv) the ovary. Our interpretation of these facts under our theory of palea interaction is that the inhibition zone of the palea is strong in the posterior side of the floral I) "Stamen lodicules" have been recorded in Cephalostachyum and Schizostachyum among other bamboos (ARBER I.c.: 937); this peculiarity, however, has nothing to do with the ontogenetic process discussed here, since they result from the fusion of stamens with lodicules.
Fig. 2. Phylogenetic scheme of different floral forms in Poaceae. Heavy black: paJea, Iodicules, carpels, and ovule. Missing appendages: X = lodicules; 0 = stamens. Solid line: stamens and staminodes. Solid arrows indicate hightly probable evolutionary trends; broken arrows, less probable evolutionary trends. Two cases deserve further careful revisions: (i) The position of Nwdus (M, in sequence C-S) which stands in close connection with uni-stigmatic Bambusoids and far apart from other non-Bambusoids grasses, and (ii) Streptogyna (R, in sequence F - J - P- R) has a pattern that may be connected with L. However, it is included in the same genus that P; such a connection supposes a very strong change in gynoecial organization, which seems to be less probable. For further details see the text.
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Grass Flower
Bistigmatic A
25 Flora, Bd. 181,5-6
B
•
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A.
E.
COCUCCI
and
A. M. ANTON
A
Fig. 3. Longitudinal sections of different stages in floret development in Oryzopsis virescens (after KAM 1974). A. Early stage of the apex showing lemma initiation (I); B. Initiation of the gynoecium (g) after elongation of the lemma (I) and frontal stamen (s) to the left, and palea (p) to the right; C. Floret during the growth of the gynoecium: initiation oithe tepaloid staminode (posterior lodicule) next to the left of the palea (unlabelled); as the lemmas encloses the palea and the flower, two portions of the lemma appears in the section. Palea-flower insertion plane in solid line; floral apex and shoot axes dotted lines. In A the plane is transverse and both axes coincide. In Band C the plane is tilted, and the apex axis is oblique with respect to the shoot axis; in both figures the original position of the plane has been presented to allow one to visualize the tilting angle of the plane.
apex (dense shaded area in Fig. 1 C), and mild in the lateral and frontal sides (light shaded area in Fig. 1 C). This results in the suppression of the floral primordium behind the ovary and in retardation frontally, producing a reduction of the perianth and a delay in the development of the frontal stamen primordium. Our current general conclusion is that the androecium of most grasses is composed of two whorls, the inner one bearing two stamens and the outer one having only one, the frontal or anterior stamen (Fig. 2 N). It is of interest to note that BUTZIN (1966) and WILLEMSE (1982) when interpreting the floret of Ehrharteae with four stamens, assigned the frontal stamen to the outer verticil and the lateral ones, together with the adaxial stamen, to the inner verticil. These were the only times to our knowledge that the lateral stamens were ascribed to the inner whorl. An interesting antecedent of the same organization pattern can be found in some members of the Orchidaceae (EICHLER 1875: 186, Fig. 11 0 A), where the three fertile stamens present in the flower belong to two different cycles.
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Grass Flower
D
Fig. 4. Camera lucida drawings of spikelettransections. Solid black: palea; shaded: lodicules. Enlargments not to scale. A. Nastus sp. (CHR 345019B); B. Bambusa sp. (CHR 345569B); C. Leersia hexandra (A. T. HUNZIKER 1868, CORD); D. Phyllostachys sp. (CHR 132302); E. Hierochloii redolens (redrawn from ARBER 1934: Fig. 86); F. Anthoxanthum odoratum (redrawn from ARBER 1934: Fig. 71).
25*
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A. E. COCUCCI and A. M. ANTON
The theory of the palea primordium interaction with the floral apex Three main lines of evidence apply to an understanding of the palea inhibition zone in those cases where inhibition takes place adaxially. First, an extreme abbreviation of the internodes between palea, stamens, and carpels produce a sequence of concentric whorls in an almost single transverse plane, rather than in concentric circles at increasingly higher levels over an ideally conical structure. This feature is particularly evident in the palea, and in the lodicule and stamen whorls. Second, at an early stage of development in a floral apex, it is significant that the transverse plane has tilted towards the palea in such a way that in side view, the plane - now represented by a line - is oblique to the main stem axis (Fig. 3) 1). Third, such a change of position of the plane is accompanied by a shift of the floral apex toward the palea primordium. Thus, the posterior zone of the floral apex falls under the influence of the palea primordium zone which determines the suppression of a substantial part of the floral apex. Clear evidence supporting this can be found in Stipa and Oryzopis (see the careful and well documented work of MAZE et al. 1971: 285- 287, Figs. 83-85 and 101-102, and KAM 1974: 128, Figs. 8-12).
We consider, therefore, that our hypothesis of a palea inhibition zone is substantiated by the abbreviation of the floral internodes, the tilting of the floral plane, and as well by the directional movement of the floral plane towards the palea. Although no ontogenetical research has been carried out on the primordium of laterally compressed spikelets, similar principles may induce a change of the palea shape thus bringing the palea closer to the floral organs and inhibiting their development. The evolution of the floral patterns The starting point for the floral forms is indentified as a three perianthial flower with an hexamerous androecium and a trimerous tri-stigmatic gynoecium, which is represented in Fig. 2A by Nastus sp. From this type two forms have evolved by reduction of the stigmatic branches; one is characterized by the loss of the frontal stigmatic branch so that two lateral stigmata remain (Fig.2D). These three basic flower types are differentiated by gynoecial structure (Fig. 2A, C and D). Each ofthem can be further modified (reduction or alteration of other floral appendages) depending on either a cyclic or zonal mode of action in the reduction process. If cyclic, reduction operates by suppression of all the members of verticil (Fig. 2D- E) under the influence of the palea. This type of reduction is found only in flower types with uni-stigmatic (Oreobambos, Fig. 2D) or tri-stigmatic (Dinochloa, Fig. 2E) gynoecia. All flower types derived from the original pattern (Fig. 2A) as well as those derived by cyclic inhibition (Fig. 2D- E) may evolve further under the influence of zonal inhibition. The lowest level in Fig. 2 is represented by Nastus (Fig. 2A), from which the triangular pattern of Oxytenanthera (Fig.2B) and Bambusa (Fig.4B) can be derived without loss of floral components. From it, the pattern of Criciuma, Elythrostachys, Apoclada, Guadella and EremocauIon (Fig. 2C) results as a consequence of the loss of one stigma of the gynoecium. Zonal reduction of the patterns represented in Fig. 2B and C lead to Melocanna (Fig. 2F) and Leersia hexandra (Fig. 2G), where the posterior lodicule is suppressed. Both of these are at the same level as patterns D and E, which also lack lodicules but through cyclic reduction. These patterns D and E may also be derived from B. The particular case of Oreobambos (Fig. 2 D) exhibits a simplification of the stigmata in addition to lodicule reduction. I) It is neccessary to point out that the primordium tilting is part of a dynamic process, due tp the different timing in the development of the spikelet structures. The lemma takes advantage first (tilting the plane towards the palea); then follow in order the palea, and finally the floral appendages. As a consequence, the floral apex is restored to a transverse position, or even tilted a little in an opposite direction (towards the abaxial side) at the mature stage.
Gco.Ao~
.
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Progressive zonal influence of pale a inhibition on the three gynoecial types (Fig. 2D, F and G), leads to equivalent floral patterns such as Anomochloa (Fig. 2H), where there is suppression of the two adaxial stamens of the outer whorl, and Ehrharta (Fig. 21), with a similar signification of the androecium. These types of androecium structures are notfound among derivatives with tri-stigmatic gynoecia (Fig. 2F). The next step, depicted by Phyllostachys (Fig. 2J) and Stipa (Fig. 2L) modifies the adaxial stamen of the inner whorl, reducing it to a tepaloid staminode - the posterior lodicule. Further progression leads to the pattern of most grasses (Fig. 2 N) and Nardus (Fig. 2 M). Again the pathway from the tri-stigmatic gynoecia is not represented. Following the same tendency of antero-posterior zonal inhibition, Schedonnardus and some species of Ctenium (Fig. 2Q) and Centotheca (Fig. 2S) are derived; the palea inhibition is stronger laterally, and as a result, the laterallodicules are lost, and eventually the frontal stamen (Fig. 2 S). Cases such as Anthoxanthum (Fig. 2K), Poa tucumana (Fig. 20) andStreptogyna (Fig. 2P and R) are special: K derives from I by lateral compression of the palea; 0, from N by a similar process. On the other hand, P derives from J, by suppression of the frontal stamen. By using this proposal, almost all flower forms in the Poaceae may be explained. We have ignored flowers with more than six stamens as in the extreme cases of Pariana (21 stamens) or Ochlandra (50-120 stamens), because the interpretation of such rarities needs careful ontogenetic studies that are not yet available. On the other hand, they do not alter our present proposals. We also exclude special cases such as contemporary action in cleistogamy which needs no invoking of palea inhibition because other explanations suffice. Evolutionary changes are brought about by the primary evolutionary forces which produce and sort out genetic variations and operate in a field of space and time. The distribution in time of the morphological events that charaterize the evolution of the grass flower started with palea modification (Fig. 2, step from A to B), followed by gynoecial modification towards uni-stigmatic (from B to D) or bi-stigmatic (from B to C) flowers. The next step is represented by cyclic or zonal inhibition. At last, there is another modification in the androecium; although it may be already present in six-staminate Bambusoids, it is conspicuous in the flower types represented from Ito S (Fig. 2). The anthers change fromlatrorse to introrse orextrorse, giving rise to a pattern with one frontal stamen with introrse or latrorse anther and two lateral stamens with extrorse anthers (ANTON & ASTEGIANO 1973). This model seems to be widely spread in the family (Fig. 2N).
Conclusions 1. The interaction of the palea with the floral apex is postulated as generating an area of inhibition which substantially affects the floral apex. 2. Such an area may be cyclic or zonal; when cyclic, it equally affects all members of a whorl; when zonal, it affects one or both sides of the floral apex. 3. Cyclic inhibition occurred as an early step in the evolution of the grass flower (Fig. 2 D- E), giving rise to lines of limited success. 4. Zonal inhibition is that which has produced most of the grass flower forms. It has operated on ancestors with a complete set of floral appendages (Fig. A) as well as on flower types in which cyclic reduction had already taken place (Fig.2D). 5. Zonal inhibition is chiefly expressed close to the adaxial side of the floral apex; lateral inhibition is a secondary phenomenon derived from it. 6. New opportunities for the analysis of phylogeny in the family emerge from this novel interpretation of the grass flowers. Four major evolutionary patterns can be recognized (Fig. 2): (1) sequence D-H-M; (2) line E; (3) sequence F-JP-R; (4) sequence C-G-I-L-N-Q-S, and its secondary derivatives. 7. The fIrst three evolutionary lines are exclusive to Bambusoid grasses (except Nardus). The fourth comprises Bambusoid and non-Bambusoid representatives up to point N, but thereafter the Bambusoid are absent. 8. The form of grass flower which has been most successful appears to be bi-lodiculate, tri-staminate, and bistigmatic, with stamens belonging to two different cycles - the frontal from the outer whorl, and the two lateral from the inner whorl.
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A. E. COCUCCI and A. M. ANTON, Grass Flower
Acknowledgement We are indebted to Dr. H. E. CONNOR (Centre for Resource Management, University of Canterbury, Christchurch, New Zealand) for his ciritical review of the manuscript and opportune suggestions that led us to a substantial rearrangement of the original paper. We are also grateful to Dr. E. EDGAR for the provision of material.
References ANTON, A. M., & AsTEGIANO, M. E. (1973): Notas sobre la morfologia floral de Gramineas. Kurtziana 7: 49-53. ARBER, A. (1934): The Gramineae. A study of Cereal, Bamboo and Grass. Cambridge. BUTZIN, F. (1966): Zur Kenntnis der tetrandrischen Grarnineen. WiHdenowia 4 (2): 215-220. CHAMPAGNAT, p". (1965): Physiologie de la croissance et de l'inhibition des bourgeons: Dominance apicale et phenomenes analogues. In: RUHLAND, W. (Ed.): Encyclopedia of Plant Physiology. XV: Differentiation and Development. Berlin"Heidelberg. CHENG, P. C., GREYSON, R.I., & WALDEN, D. B. (1983): Organ initiation and the development of unisexual flowers in the tassel and ear of Zea mays. Arner. J. Bot. 70 (3): 450-462. CLAYTON, W. D., & RENVOIZE, S. A. (1986): Genera Graminum. Grasses of the World. London. CLIFFORD, H. T. (1961): Floral evolution in the family Gramineae. Evolution 15 (4): 455-460. DAHLGREN, R. M. T., CLIFFORD, H. T., & YEO, P. F. (1985): The Families of the Monocotyledons. Structure, Evolution and Taxonomy. Berlin-Heidelberg-New York-Tokio. EICHLER, A. W. (1875): Bliitendiagramme. Theill. Leipzig. JACQUES-FELIX, H. (1962): Les Gramim5es (Poaceae) d' Afrique Tropicale. Paris. KAM, Y. K. (1974): Developmental studies of the floret in Oryzopsis virescens and O. hymenoides (Gramineae). Can. J. Bot. 52: 125-149. KINET, J. M., SACHS, R. M., & BERNIER, G. (1985): The Physiology of Flowering. III. The Development of Flowers. Boca Raton, Flocida. MAZE, J., DENGLER, N. G., & BOHM, L. R. (1971): Comparative floret development in Stipa tortilis and Oryzopsis miliacea (Gramineae). Bot. Gaz. 132: 273-298. MCCLURE, F. A. (Ed.: SODERSTROM, T. R.) (1973): Genera of Bamboos Native to the New World (Gramineae: Bambusoideae). Smithsonian Contr. to Bot. 9: I-XII, 1-148. MEHLENBACHER, L. E., JR. (1970): Floret development, embryology and systematic position of Oryzopsis hendersoni (Gramineae). Can. J. Bot. 48): 1741-1758. NOZERAN, R., BANCILHON, L., & NEVILLE, P. (1971): Intervention ofintemal correlations in the morphogenesis of higher plants. In: ABERCROMBIE, M. A., BRANCHET, J., & KING, T. J. (Ed.): Andvances in Plant Morphogenesis. 9. New York. PAYER, J. B. (1857): Traite d'Organogenie de la Fleur [Reprint 1966 by CRAMER, J., & SWANN, H. K. (Ed.): Historiae Naturalis Classica 47]. PHILIPSON, W. R. (1985): Is the grass gynoecium monocarpellary? Amer. J. Bot. 72: 1954-1961. SAUNDERS, E. R. (1937): Floral Morphology. A New Outlook With Special Reference to the Gynoecium. Cambridge. SCHUSTER, J. (1910): Dber die Morphologie der Grasbliite. Flora 100: 2\3-266. SINNOT, E. W. (1960): Plant Morphogenesis. New York. SODERSTROM, T. R., ELLIS, R. P., & JUDZIEWICZ, E. J. (1987): The Phareae and Streptogyneae (Poaceae) of Sri Lanka: A morphological-anatomical study. Smithsonian Contr. to Bot. 65: I - V, 1- 27 . - - - & LoNDONO, X. (1987): Two new genera of Brazilian bamboos related to Guadua (Poaceae: Bambusoideae: Bambuseae). Amer. J. Bot. 74: 27-39. THOMPSOM, D'ARcY. (1966): On Growth and Form. Abridged edition by BONNER, J. T. Cambridge. WARDLAW, C. W. (1952): Phylogeny and Morphogenesis. London. WILLEMSE, L. P. M. (1982): A discussion of the Ehrharteae (Gramineae) with special reference to the malesian taxa formerly included in Microlaena. Blumea 28: 181-194. Received November 27, 1987 Authors' address: ALFREDO E. COCCUCI and ANA M. ANTON, Instituto Multidisciplinario de Biologia Vegetal (CONICET - UNIVERSIDAD NACIONAL DE CORDOBA), Casillo de Correo 495,5000 Cordoba, Argentina. Both are members of the "Carrera del Investigador" (CONICET, Argentina).
L ____________________
The Grass Flower: Suggestions on its Origin and Evolution ALFREDO
E.
COCUCCI
and ANA M.
ANTON
Instituto Multidisciplinario de Biologia Vegetal, COrdoba, Argentina
Summary Analysing a large number of different grass flowers, a hypothesis is proposed to explain the floral variation found in the family. It is postulated that the interaction of the palea with the floral apex generates an area of inhibition wich substantially affects the floral apex. Depending on the mode of action in the reduction process, together with an independent phenomenon which affects the gynoecial organization, four major evolutionary patterns are recognized. The form of grass flower which has been most successful appears to be the bi-lodiculate, tri-staminate and bistigmatic, with the stamens belonging to two different cycles - the frontal from the outer whorl and the two lateral from the inner whorl.
Introduction The generally accepted idea that most grass flowers have three stamens in a single whorl is something that always disquieted us, because the spatial arrangement of the androecium does not match the expectation derived from theoretical considerations. Following our analysis of a large number of different grass flowers, we propose an hypothesis based on genetical and physiological grounds, which will, it seems to us, more appropriately explain all the variation found in the flowers of the grasses. We hope that this new concept will persuade agrostologists to revaluate the importance of the flower, one of the most stable parts of the sporophyte, in studies of grass systematics and evolution.
Materials and Methods The information used here comes from three different sources: (1) from material, mainly non-Bambusoid, already in our slide collection and prepared with regular anatomical techniques; (2) material specially prepared for this paper (mainly Bambusoids) and kindly provided by Dr. E. EDGAR (Botany Division, DSIR, Christchurch, New Zealand); it was sectioned and mounted with regular techniques for paraffin embedding, sectioning and staining; (3) examples from ARBER (1934) and CLA YTON & RENVOIZE (1986) were reproduced exactly or translated into diagrams.
Theoretical Foundations Every living organism possesses a number of more or less well defined features which become apparent during its development. The onset of the expression of such characters is determined by the hereditary constitution eN ARDLAW 1952: 126-158; D' ARCY THOMPSON 1966: 265-267). Within this context, morphogenetic processes in different grass flowers have been analysed in an effort to determine evolutionary trends. The flowers of grasses exhibit a great deal of variation in the number of floral organs, their mutual relationship, and their symmetry. The ancestral type, which is present in some members of the Bambusoideae, is portrayed as a trimerous, actinomorphic structure with three perianth parts (reduced tepals), two whorls of three stamens each, and a tri-carpellate ovary with three feathery stigmata (Figs. 1 A, 2A). Such a flower type, by reduction (simplification) and fusion, yields the
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Fig. 1. Palea interaction zones. Dense shading: strong interaction (inhibition zone); light shading: mild interaction (Modification or retardation). A. Theoretical diagram of a suppossed ancestor of B, with indication ofthe strong palea interaction zone following a cyclic pattern; B. Diagram derived from A; C. Theoretical diagram of a supposed ancestor of D, following a zonal pattern (compression against the axis), with an indication of the strong palea interaction zone affecting the posterior lodicule and two stamens of the outer whorl, and a mild interaction with respect to the posterior stamen of the inner whorl and the frontal of the outer whorl; D. Diagram derived from C ; strong palea interactions leads to the suppression of the posterior (adaxial) lodicule and the two lateral stamens of the outer whorl, whereas the mild interaction causes a reduction in size of the two lateral lodicules, a modification of the posterior stamen of the inner whorl into a tepaloid staminode, and a delay in the appearance during ontogeny of the frontal stamen; E. Theoretical diagram of a suppossed ancestor of F, with indication of the strong palea interaction zone following a zonal pattern (lateral compression); F. Diagram derived from E. Missing appendages: X=lodicules; 0= stamens.
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type that characterizes most of the grasses, i.e. a zygomorphic flower with two (occasionally three ore more) perianth elements (lodicules), three stamens, and an ovary with two feathery stigmata (Fig. 2N). Less frequent are zygomorphic flowers with a much reduced androecium, having two or even just one stamen (Fig. 2K, P, R, S and 0), and others in which the gynoecium has a single style and stigma (Fig. 2D, H, M). Finally, there are reductions which produce imperfect flowers. The current interpretation of these derived types presupposes the reduction (suppression) of the adaxial perianthial component opposite the lemma i.e. the posterior lodicule, and the suppression of the inner staminal whorl (PAYER 1857; SCHUSTER 1910; SAUNDERS 1937; DAHLGREN et al. 1985). A close analysis of the tri-androus flower (Fig. 2N) shows a spatial arrangement of its organs where two stamens are almost lateral to the ovary (lateral stamens) and a third one is anterior (frontal or abaxial stamen). The two lodicules form the most external whorl, and alternate with the frontal stamen. Several facts connected with the pattern of organization - facts that we will discuss - lead us to postulate a different interpretation. We base it upon the interaction between the palea and the floral apex such that modification, reduction or suppression of the floral organs follows a cyclic or a zonal pattern. Cyclic reduction affects all members of a whorl equally. As far as is known in grasses, cyclic palea inhibition affects only the perianth whorl (Fig. 1 A - B). Zonal simplification affects one or two sides of the floral apex because the palea primordium inhibits the development of the floral organs close to it (Fig. 1 C - F). This general hypothesis of a palea interaction zone is based on three well known principles of plant morphogenesis: (1) once formed, organs assume a role in subsequent plant development (NOZERAN et aI. 1971: 27; KINET et al. 1985: 115-116, 122); (2) the rate of development of the apical meristem of an axis may be controlled by the organ or group of organs which develop from it (NOZERAN et al. I.c.: 61); (3) the development of an axillary bud is inhibited by its axillant leaf (CHAMPAGNAT 1965: 1106-1137; SINNOT 1960: 98-102). In a way, then, the grass floral apex, because of its proximity to the palea, may be considered as the equivalent of an axillary bud under the influence of a subtending leaf. It is, however, necessary to point out that an independent phenomenon may affect the gynoecial organization in such a way that the three stigmatic branches may reduced to two or one, depending on the number of carpels which loose the ability to develop them. So, three gynoecial categories can be recognized according to the number of stigmata - three (Fig. 2 A), two laterals (Fig. 2 C), or one frontal stigma (Fig. 2D). Each of these may be affected by the palea interaction according to its type. The palea embraces the fl6wer, sometimes almost completely, and varies in shape according to the degree and orientation of the compression of the floret. Three main states can be recognized depending to palea shape, although intermediates may occur. In the first the flower has a quasi-actinomorphic pattern; there are three lodicules present, with the posterior one slightly smaller than the frontal ones; the androecium has six stamens distributed regularly in two whorls, and the gynoecium is composed of three carpels, each bearing a stigma. An example of this condition is well illustrated by Nastus (Fig. 2A, 4A) and Schizostachyum (ARBER, I.c.: 115, Fig. 39 D2). The palea has no prominent keels, and its area of insertion is quasi-circular and concentric with the floral whorls. The second state is characterized by an alteration of the flower patterns because of a change in the shape of the palea - and consequently of its area of insertion. This change in shape of the palea may be due to space constraints in the bud (ARBER I.c.: 112). Here the palea has two prominent keels and a flat internerve area, and its node is not circular since its adaxial side is flat. A general tendency directs the patterns towards a triangular shape which in practice results in a sort of oval contour (Fig. 2B, 4B), and is zygomorphic. The third condition is also zygomorphic, but the position of insertion of the palea has drastically changed through an extreme lateral compression of the floret. So the more or less triangular or oval patterns of the first two states have been changed to a narrow ellipse, where the
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keels of the palea become close. are almost fused or are actually reduced to one. Such is the case in Anthoxanthum (Fig. 1 f, 4 t) and Hierochloi! (Fig. 4 E), where in the perfect flowers the androecium has only one anterior and one posterior stamen. In these flowers, the palea has one or no central vascular bundle, and the entire structure is laterally compressed. Thus, the interaction zone of the palea is much stronger laterally than dorsally; as a result, a suppression of the two lateral stamens of each of the two whorls occurs, accompanied by the suppression of aIllodicules. Data supporting the zonal interaction hypothesis Cyclic inhibition as outlined above affects solely the perianth whorl; zonal interaction is of wider influence and may be superposed over cyclic system. Zonal interaction warrants a somehow larger exposition here. 1. Ontogeny of the adaxial lodicule. The "posterior, adaxial"lodicule of a tri-staminate flower has a different ontogenetic history from the two frontal lodicules. The former has a primordium initiation which agrees with the "stem type" of MEHLENBACHER (1970), whereas the latter each has a "dermal foliar type primordium" (MEHLENBACHER l.c.). It is interesting to note that the so-called "stem type" primordium has almost the same organization which characterizes stamen initiation (KlNET et al. 1985: 17). Thus, in our opinion, the "adaxial lodicule" should be interpreted as a staminode of foliar appearance!). Although the ontogeny of the "posterior lodicuIe" has rarely been investigated - for instance in Stipa henderson; (MEHLENBACHER I.c.) - we feel sure that its interpretation as a foliar or tepaloid staminode will represent the general case for all tri-Iodiculate grasses with three stamens. This is not new for the family, as it has been shown that in grass flowers with more than three lodicules, as in Ochlandra, the extra members appear to have been derived from aborted stamens (DAHLGREN et al. 1985: 431). 2. Direction of the reduction process. The zonal suppression of perianth organs in most cases starts towards the adaxial side, that is in the region close to the palea insertion, the posterior lodicule being the fIrst member affected, as in Oryzoideae (JACQUES-FELIX 1962: 26, Fig. 13). Should this phenomenon extend in the same direction, the staminal whorl should also be affected, and as a consequence, two members of the outer androecium together with one of the inner may be suppressed (Fig. 1C-D). In this way, the floral pattern of the typical bi-Iodiculate, tri-starninate flower is frrmly established (Fig. 2N). 3. Floral apex development. The excellent work of CHENG et aI. (1983), summarizes in a clear graphic way the sequences of events during the development of the flowers in maize. It was clearly shown that the order of appearance of the primordia is: (i) the lateral stamens; (ii) frontal stamen; (iii) two laterallodicules; and later (iv) the ovary. Our interpretation of these facts under our theory of palea interaction is that the inhibition zone of the palea is strong in the posterior side of the floral I) "Stamen lodicules" have been recorded in Cephalostachyum and Schizostachyum among other bamboos (ARBER I.c.: 937); this peculiarity, however, has nothing to do with the ontogenetic process discussed here, since they result from the fusion of stamens with lodicules.
Fig. 2. Phylogenetic scheme of different floral forms in Poaceae. Heavy black: paJea, Iodicules, carpels, and ovule. Missing appendages: X = lodicules; 0 = stamens. Solid line: stamens and staminodes. Solid arrows indicate hightly probable evolutionary trends; broken arrows, less probable evolutionary trends. Two cases deserve further careful revisions: (i) The position of Nwdus (M, in sequence C-S) which stands in close connection with uni-stigmatic Bambusoids and far apart from other non-Bambusoids grasses, and (ii) Streptogyna (R, in sequence F - J - P- R) has a pattern that may be connected with L. However, it is included in the same genus that P; such a connection supposes a very strong change in gynoecial organization, which seems to be less probable. For further details see the text.
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Fig. 3. Longitudinal sections of different stages in floret development in Oryzopsis virescens (after KAM 1974). A. Early stage of the apex showing lemma initiation (I); B. Initiation of the gynoecium (g) after elongation of the lemma (I) and frontal stamen (s) to the left, and palea (p) to the right; C. Floret during the growth of the gynoecium: initiation oithe tepaloid staminode (posterior lodicule) next to the left of the palea (unlabelled); as the lemmas encloses the palea and the flower, two portions of the lemma appears in the section. Palea-flower insertion plane in solid line; floral apex and shoot axes dotted lines. In A the plane is transverse and both axes coincide. In Band C the plane is tilted, and the apex axis is oblique with respect to the shoot axis; in both figures the original position of the plane has been presented to allow one to visualize the tilting angle of the plane.
apex (dense shaded area in Fig. 1 C), and mild in the lateral and frontal sides (light shaded area in Fig. 1 C). This results in the suppression of the floral primordium behind the ovary and in retardation frontally, producing a reduction of the perianth and a delay in the development of the frontal stamen primordium. Our current general conclusion is that the androecium of most grasses is composed of two whorls, the inner one bearing two stamens and the outer one having only one, the frontal or anterior stamen (Fig. 2 N). It is of interest to note that BUTZIN (1966) and WILLEMSE (1982) when interpreting the floret of Ehrharteae with four stamens, assigned the frontal stamen to the outer verticil and the lateral ones, together with the adaxial stamen, to the inner verticil. These were the only times to our knowledge that the lateral stamens were ascribed to the inner whorl. An interesting antecedent of the same organization pattern can be found in some members of the Orchidaceae (EICHLER 1875: 186, Fig. 11 0 A), where the three fertile stamens present in the flower belong to two different cycles.
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Fig. 4. Camera lucida drawings of spikelettransections. Solid black: palea; shaded: lodicules. Enlargments not to scale. A. Nastus sp. (CHR 345019B); B. Bambusa sp. (CHR 345569B); C. Leersia hexandra (A. T. HUNZIKER 1868, CORD); D. Phyllostachys sp. (CHR 132302); E. Hierochloii redolens (redrawn from ARBER 1934: Fig. 86); F. Anthoxanthum odoratum (redrawn from ARBER 1934: Fig. 71).
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The theory of the palea primordium interaction with the floral apex Three main lines of evidence apply to an understanding of the palea inhibition zone in those cases where inhibition takes place adaxially. First, an extreme abbreviation of the internodes between palea, stamens, and carpels produce a sequence of concentric whorls in an almost single transverse plane, rather than in concentric circles at increasingly higher levels over an ideally conical structure. This feature is particularly evident in the palea, and in the lodicule and stamen whorls. Second, at an early stage of development in a floral apex, it is significant that the transverse plane has tilted towards the palea in such a way that in side view, the plane - now represented by a line - is oblique to the main stem axis (Fig. 3) 1). Third, such a change of position of the plane is accompanied by a shift of the floral apex toward the palea primordium. Thus, the posterior zone of the floral apex falls under the influence of the palea primordium zone which determines the suppression of a substantial part of the floral apex. Clear evidence supporting this can be found in Stipa and Oryzopis (see the careful and well documented work of MAZE et al. 1971: 285- 287, Figs. 83-85 and 101-102, and KAM 1974: 128, Figs. 8-12).
We consider, therefore, that our hypothesis of a palea inhibition zone is substantiated by the abbreviation of the floral internodes, the tilting of the floral plane, and as well by the directional movement of the floral plane towards the palea. Although no ontogenetical research has been carried out on the primordium of laterally compressed spikelets, similar principles may induce a change of the palea shape thus bringing the palea closer to the floral organs and inhibiting their development. The evolution of the floral patterns The starting point for the floral forms is indentified as a three perianthial flower with an hexamerous androecium and a trimerous tri-stigmatic gynoecium, which is represented in Fig. 2A by Nastus sp. From this type two forms have evolved by reduction of the stigmatic branches; one is characterized by the loss of the frontal stigmatic branch so that two lateral stigmata remain (Fig.2D). These three basic flower types are differentiated by gynoecial structure (Fig. 2A, C and D). Each ofthem can be further modified (reduction or alteration of other floral appendages) depending on either a cyclic or zonal mode of action in the reduction process. If cyclic, reduction operates by suppression of all the members of verticil (Fig. 2D- E) under the influence of the palea. This type of reduction is found only in flower types with uni-stigmatic (Oreobambos, Fig. 2D) or tri-stigmatic (Dinochloa, Fig. 2E) gynoecia. All flower types derived from the original pattern (Fig. 2A) as well as those derived by cyclic inhibition (Fig. 2D- E) may evolve further under the influence of zonal inhibition. The lowest level in Fig. 2 is represented by Nastus (Fig. 2A), from which the triangular pattern of Oxytenanthera (Fig.2B) and Bambusa (Fig.4B) can be derived without loss of floral components. From it, the pattern of Criciuma, Elythrostachys, Apoclada, Guadella and EremocauIon (Fig. 2C) results as a consequence of the loss of one stigma of the gynoecium. Zonal reduction of the patterns represented in Fig. 2B and C lead to Melocanna (Fig. 2F) and Leersia hexandra (Fig. 2G), where the posterior lodicule is suppressed. Both of these are at the same level as patterns D and E, which also lack lodicules but through cyclic reduction. These patterns D and E may also be derived from B. The particular case of Oreobambos (Fig. 2 D) exhibits a simplification of the stigmata in addition to lodicule reduction. I) It is neccessary to point out that the primordium tilting is part of a dynamic process, due tp the different timing in the development of the spikelet structures. The lemma takes advantage first (tilting the plane towards the palea); then follow in order the palea, and finally the floral appendages. As a consequence, the floral apex is restored to a transverse position, or even tilted a little in an opposite direction (towards the abaxial side) at the mature stage.
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Progressive zonal influence of pale a inhibition on the three gynoecial types (Fig. 2D, F and G), leads to equivalent floral patterns such as Anomochloa (Fig. 2H), where there is suppression of the two adaxial stamens of the outer whorl, and Ehrharta (Fig. 21), with a similar signification of the androecium. These types of androecium structures are notfound among derivatives with tri-stigmatic gynoecia (Fig. 2F). The next step, depicted by Phyllostachys (Fig. 2J) and Stipa (Fig. 2L) modifies the adaxial stamen of the inner whorl, reducing it to a tepaloid staminode - the posterior lodicule. Further progression leads to the pattern of most grasses (Fig. 2 N) and Nardus (Fig. 2 M). Again the pathway from the tri-stigmatic gynoecia is not represented. Following the same tendency of antero-posterior zonal inhibition, Schedonnardus and some species of Ctenium (Fig. 2Q) and Centotheca (Fig. 2S) are derived; the palea inhibition is stronger laterally, and as a result, the laterallodicules are lost, and eventually the frontal stamen (Fig. 2 S). Cases such as Anthoxanthum (Fig. 2K), Poa tucumana (Fig. 20) andStreptogyna (Fig. 2P and R) are special: K derives from I by lateral compression of the palea; 0, from N by a similar process. On the other hand, P derives from J, by suppression of the frontal stamen. By using this proposal, almost all flower forms in the Poaceae may be explained. We have ignored flowers with more than six stamens as in the extreme cases of Pariana (21 stamens) or Ochlandra (50-120 stamens), because the interpretation of such rarities needs careful ontogenetic studies that are not yet available. On the other hand, they do not alter our present proposals. We also exclude special cases such as contemporary action in cleistogamy which needs no invoking of palea inhibition because other explanations suffice. Evolutionary changes are brought about by the primary evolutionary forces which produce and sort out genetic variations and operate in a field of space and time. The distribution in time of the morphological events that charaterize the evolution of the grass flower started with palea modification (Fig. 2, step from A to B), followed by gynoecial modification towards uni-stigmatic (from B to D) or bi-stigmatic (from B to C) flowers. The next step is represented by cyclic or zonal inhibition. At last, there is another modification in the androecium; although it may be already present in six-staminate Bambusoids, it is conspicuous in the flower types represented from Ito S (Fig. 2). The anthers change fromlatrorse to introrse orextrorse, giving rise to a pattern with one frontal stamen with introrse or latrorse anther and two lateral stamens with extrorse anthers (ANTON & ASTEGIANO 1973). This model seems to be widely spread in the family (Fig. 2N).
Conclusions 1. The interaction of the palea with the floral apex is postulated as generating an area of inhibition which substantially affects the floral apex. 2. Such an area may be cyclic or zonal; when cyclic, it equally affects all members of a whorl; when zonal, it affects one or both sides of the floral apex. 3. Cyclic inhibition occurred as an early step in the evolution of the grass flower (Fig. 2 D- E), giving rise to lines of limited success. 4. Zonal inhibition is that which has produced most of the grass flower forms. It has operated on ancestors with a complete set of floral appendages (Fig. A) as well as on flower types in which cyclic reduction had already taken place (Fig.2D). 5. Zonal inhibition is chiefly expressed close to the adaxial side of the floral apex; lateral inhibition is a secondary phenomenon derived from it. 6. New opportunities for the analysis of phylogeny in the family emerge from this novel interpretation of the grass flowers. Four major evolutionary patterns can be recognized (Fig. 2): (1) sequence D-H-M; (2) line E; (3) sequence F-JP-R; (4) sequence C-G-I-L-N-Q-S, and its secondary derivatives. 7. The fIrst three evolutionary lines are exclusive to Bambusoid grasses (except Nardus). The fourth comprises Bambusoid and non-Bambusoid representatives up to point N, but thereafter the Bambusoid are absent. 8. The form of grass flower which has been most successful appears to be bi-lodiculate, tri-staminate, and bistigmatic, with stamens belonging to two different cycles - the frontal from the outer whorl, and the two lateral from the inner whorl.
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Acknowledgement We are indebted to Dr. H. E. CONNOR (Centre for Resource Management, University of Canterbury, Christchurch, New Zealand) for his ciritical review of the manuscript and opportune suggestions that led us to a substantial rearrangement of the original paper. We are also grateful to Dr. E. EDGAR for the provision of material.
References ANTON, A. M., & AsTEGIANO, M. E. (1973): Notas sobre la morfologia floral de Gramineas. Kurtziana 7: 49-53. ARBER, A. (1934): The Gramineae. A study of Cereal, Bamboo and Grass. Cambridge. BUTZIN, F. (1966): Zur Kenntnis der tetrandrischen Grarnineen. WiHdenowia 4 (2): 215-220. CHAMPAGNAT, p". (1965): Physiologie de la croissance et de l'inhibition des bourgeons: Dominance apicale et phenomenes analogues. In: RUHLAND, W. (Ed.): Encyclopedia of Plant Physiology. XV: Differentiation and Development. Berlin"Heidelberg. CHENG, P. C., GREYSON, R.I., & WALDEN, D. B. (1983): Organ initiation and the development of unisexual flowers in the tassel and ear of Zea mays. Arner. J. Bot. 70 (3): 450-462. CLAYTON, W. D., & RENVOIZE, S. A. (1986): Genera Graminum. Grasses of the World. London. CLIFFORD, H. T. (1961): Floral evolution in the family Gramineae. Evolution 15 (4): 455-460. DAHLGREN, R. M. T., CLIFFORD, H. T., & YEO, P. F. (1985): The Families of the Monocotyledons. Structure, Evolution and Taxonomy. Berlin-Heidelberg-New York-Tokio. EICHLER, A. W. (1875): Bliitendiagramme. Theill. Leipzig. JACQUES-FELIX, H. (1962): Les Gramim5es (Poaceae) d' Afrique Tropicale. Paris. KAM, Y. K. (1974): Developmental studies of the floret in Oryzopsis virescens and O. hymenoides (Gramineae). Can. J. Bot. 52: 125-149. KINET, J. M., SACHS, R. M., & BERNIER, G. (1985): The Physiology of Flowering. III. The Development of Flowers. Boca Raton, Flocida. MAZE, J., DENGLER, N. G., & BOHM, L. R. (1971): Comparative floret development in Stipa tortilis and Oryzopsis miliacea (Gramineae). Bot. Gaz. 132: 273-298. MCCLURE, F. A. (Ed.: SODERSTROM, T. R.) (1973): Genera of Bamboos Native to the New World (Gramineae: Bambusoideae). Smithsonian Contr. to Bot. 9: I-XII, 1-148. MEHLENBACHER, L. E., JR. (1970): Floret development, embryology and systematic position of Oryzopsis hendersoni (Gramineae). Can. J. Bot. 48): 1741-1758. NOZERAN, R., BANCILHON, L., & NEVILLE, P. (1971): Intervention ofintemal correlations in the morphogenesis of higher plants. In: ABERCROMBIE, M. A., BRANCHET, J., & KING, T. J. (Ed.): Andvances in Plant Morphogenesis. 9. New York. PAYER, J. B. (1857): Traite d'Organogenie de la Fleur [Reprint 1966 by CRAMER, J., & SWANN, H. K. (Ed.): Historiae Naturalis Classica 47]. PHILIPSON, W. R. (1985): Is the grass gynoecium monocarpellary? Amer. J. Bot. 72: 1954-1961. SAUNDERS, E. R. (1937): Floral Morphology. A New Outlook With Special Reference to the Gynoecium. Cambridge. SCHUSTER, J. (1910): Dber die Morphologie der Grasbliite. Flora 100: 2\3-266. SINNOT, E. W. (1960): Plant Morphogenesis. New York. SODERSTROM, T. R., ELLIS, R. P., & JUDZIEWICZ, E. J. (1987): The Phareae and Streptogyneae (Poaceae) of Sri Lanka: A morphological-anatomical study. Smithsonian Contr. to Bot. 65: I - V, 1- 27 . - - - & LoNDONO, X. (1987): Two new genera of Brazilian bamboos related to Guadua (Poaceae: Bambusoideae: Bambuseae). Amer. J. Bot. 74: 27-39. THOMPSOM, D'ARcY. (1966): On Growth and Form. Abridged edition by BONNER, J. T. Cambridge. WARDLAW, C. W. (1952): Phylogeny and Morphogenesis. London. WILLEMSE, L. P. M. (1982): A discussion of the Ehrharteae (Gramineae) with special reference to the malesian taxa formerly included in Microlaena. Blumea 28: 181-194. Received November 27, 1987 Authors' address: ALFREDO E. COCCUCI and ANA M. ANTON, Instituto Multidisciplinario de Biologia Vegetal (CONICET - UNIVERSIDAD NACIONAL DE CORDOBA), Casillo de Correo 495,5000 Cordoba, Argentina. Both are members of the "Carrera del Investigador" (CONICET, Argentina).
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