Evolution of the helobial flower

Aquatic Botany, 44 (1993) 303-324

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Elsevier Science Publishers B.V., Amsterdam

Evolution of the helobial flower U. Posluszny a and W.A. Charlton b

1Department of Botany, Universityof Guelph, Guelph, Ont. NIG 2WI. Canada bPiantScienceand CytogeneticsGroup, Departmentof Celland StructuralBiology, Williamson Building, Universityof Manchester, ManchesterMI3 9PL, UK (Accepted 25 June 1992)

ABSTRACT Posluszny, U. and Charlton, W.A., 1993. Evolution of the helobial flower. Aquat. Bot., 44." 303-324. We propose a hypothesis for the derivation of flowers and reproductive structures in the Alismatidae (Helobiae) which is based on evolution of features of 'flower' and 'inflorescence' in different ways from an ancestral pre-floral condition with a multiaxial reproductive structure. We base this proposition on the existence of many cases of structures with attributes of both 'flower" and "inflorescence'. In one suite of cases the lateral ax:s appear to have become flower-like while the main axis has become an inflorescence axis; in another the axes have become inflorescence-like proximally and flowerlike distally. Like other evolutionary plans, it can also be read in the reverse direction, and would then imply that features of 'flower' and 'inflorescence' had become re-partitioned in different ways in the group. We interpret as reduced the simpler forms of flower among the group.

INTRODUCTION

The Alismatidae or Helobiae are an assemblage of hydrophytic monocotyledons which have long been considered to be a natural group (e.g. Hutchinson, 1959; Tomlinson, 1982) on account of general features of embryology, vegetative structure, and habitat preference. Within this presumed natural group, though, there is an enormous diversity of floral structures and indeed reproductive structures. At one extreme there are the solitary flowers of Najas, where the male flower consists of a stamen surrounded by two membranous involucres, the female of an apparently terminal ovule surrounded by a single involucre (Posluszny and Sattler~ 1976b); at the other extreme are flowers like those of some of the Alismataceae and Limnocharitaceae, with distinct calyx and corolla, numerous stamens and carpels. Inflorescences are similarly varied: at one extreme flowers can be solitary as in Najas, or at the other extreme they can be assembled into vast inflorescences with hundreds Correspondence to: U. Posluszny, Department o f Botany, University o f Guelph, Guelph, Ont. N I G 2Wl, Canada.

"© 1993 Elsevier Science Publishers B.V. All rights reserved 0304-3770/93/$06.00

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of flowers, such as those found in Alisma plantago-aquatica L. or Limnophyton angolense Buchen. There are areas where distinct evolutionary trends have been detected. For instance, in the Hydrocharitaceae there are cases with conspicuous entomophilous flowers, but in other cases there appear to be significant trends in floral reduction and modification in connection with various forms ofhydrophilous pollination and the marine habit (Sculthorpe, 1967; Kaul, 1968b). Morphological series can be found within other families. The problems lie in obtaining a perspective which can be used to evaluate the whole group, particulafly when floral diversity is so great. We feel that it may be helpful to attempt to start from a fresh viewpoint. We propose to consider the Alismatidae in terms of three basic subgroups which can largely coexist with existing systematic treatments. We propose that the families of the Alismatidae can be split into 'petaloid' types, 'tepaloid' types, and 'extra-simplC types. We are using the division of families given in Tomlinson (1982). In petaloid types there is a distinctive perianth divisible into calyx and corolla. This group includes Alismataceae, Limnocharitaceae and Hydrocharitaceae (taking the simpler forms of Hydrocharitaceae as derived) and we are including Butomaceae where the perianth is petaloid but there are differences between the members of the inner and outer whorls (see Singh and Sattler, 1974). In tepaloid types the perianth is not divisible into calyx and corolla, and is normally sepal-like. Such families are Scheuchzeriaceae, Juncaginaceae, Lilaeaceae, Potamogetonaceae, perhaps Zosteraceae and Aponogetonaceae. In the extra-simple types, the remaining families, perianth is lacking or vestigial. The tepaloid types, which are liable to have unorthodox floral morphologies including stamen/perianth superposition, have given rise to the most speculation in the past and provide the main thrust for the present review. Kunth (1841) and Miki (1937) interpreted the flower of Potamogeton as a condensed inflorescence branch, and subsequently Uhl (1947) extended this pseudanthial interpretation to most of the tepaloid types. A rather different perspective is added by later developmental studies, and there have been suggestions that the inflorescences themselves may have features which are more commonly associated with flowers (Charlton, 1981; Posluszny et al., 1986). The continuum between 'flower' and 'inflorescence' seems to be a potentially fruitful areh to explore; however, if we are to use this approach, we have to bear in mind that the terms 'flower' and 'inflorescence' can be used only in a colloquial sense. T H E F L O W E R A N D T H E I N F L O R E S C E N C E IN ' T E P A L O I D ' FAMILIES

For the purpose of this discussion we include the families listed above, with the possibility that Zosteraceae may be included. All these families consis-

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tently show perianth/stamen su~rposition (e.g. Sattler, 1965; Lieu, 1979; Posluszny, 1983; Posluszny et at, 1986), except for Ruppia and the Aponogetonaceae, and, generally, Zosteraceae. In Ruppia there is no separate perianth but there is an outgrowth from the back of the stamen connective (Posluszny and Sattler, 1974b). Most Zosteraceae have nothing that could be interpreted as perianth, but some have 'retinacula' which have been so interpreted (Bentham and Hooker, 1883) and these do occur in approximately the appropriate positional relationship to the ~tameu. hi Apo,ot~tonaceae the stamens are not superposed over perianth segments and the perianth may be reduced (Singh and Sattler, 1977b). We propose to leave consideration of this family until later. The situation in Maundia (Juncaglnaceae) may also provide an exception: according to Markgraf (1936) there are no perianth members below the lowest whorl of stamens. There is no developmental information for Maundia. The perianth/stamen association is extremely stable. We have looked at many hundreds, if not thousands, of flowers of Scheuchzeria, Potamogeton, Lilaea and Triglochin and have seen no clear cases of a stamen developing without an associated perianth member; occasional mature stamens appear to have none but usually a small residuum c~n be found on dissection. Similarly it is extremely rare to find a perianth member without an associated stamen. We have seen this situation only in the small flowers with reduced numbers of parts which frequently occur near the tip of inflorescences ofPotamogewn (Charlton and Posluszny, 1991 ). Characteristically the number of carpels in a whorl corresponds to the number of periamh/stamen associations in a whorl: one in perfect flowers of Lilaea, (two in Ruppia?), three in Triglochin, four in many species of Potamogeton. There can be more than one whorl of perianth/stamen associations (there are two in Triglochin) or of carpels - - two in Triglochin and two in Ruppia. In some cases in Potamogeton additional complete or incomplete whorls of carpels can occur, and, if carpel initiation is continued, carpels can ultimately be initiated in spiral sequence (Charlton and Posluszny, 1991 ). Some of the features of these flowers have led to suggestions that they may be pseudanthia, as we have already noted. Uhl (1947) followed Kunth ( 1841 ) and Miki (! 937) but made the most general contribution in this direction. According to Uhl, each flower represented a condensed inflorescence branch; each perianth/stamen association would represent a bract subtending a male flower reduced to a single stamen; the gynoecium would represent either a single female flower or a number of female flowers each reduced to a single carpel. Miki's (1937) interpretation of Potamogeto~ differed mainly in that he saw each stamen as representing a ma~e flower originally of two stamens. The stamen/perianth association could indeed represent a bract and a reduced male flower. The positional association is appropriate for a bract subtending a lateral structure, and the constancy of the relationship implies a causal developmental connection of the kind deduced by Snow and Snow

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(1942) between leaf and axillary bud. Sattler ( 1965 ) pointed out, in the case of Potarnogeton, that thv association could also be interpreted as a gonophyll (after Melville, 1962, 1963). It could also be interpreted as an androclad/ bract unit (after Meeuse (1966) based on Neumayer, 1924). Unlike the situation in a number of other cases of stamen/perianth superposition (Lacroix and Sattler, 1988) there is no suggestion of the two structures arising on a common primordiuw. At least in Triglochin and Potamogeton a single trace from the floral vascular supply branches to supply both components, and in Scheuchzeria each stamen is supplied by a branch from one of the bundles supplying the associated perianth member (Uhl, 1947), and these cases would fit with any of the possible interpretations. Finally, Miki's notion that the stamen in Potaraogeton is derived from two original stamens gets some support from the peculiar diprimordial form of stamen initiation which has been described ~br the lateral stamens of Potamogeton densus L. ( = Groenlandia densa (L.) Fourr.) (Posluszny and Sattler, 1973), Potamogeton berchtoldii Fieber (Charlton and Posluszp.y, 1991 ) and possibly Potamogeton crispL~s L. (Hegelmaier, 1870). In these cases each stamen arises as two initially separate pdmordia above the margins of the as,~ociated perianth segment, and the two loci subsequently become connected by upgrowth in between, it is also possible to find two perianth segments sharing a single stamen in Potamogeton (Charlton and Posluszny, 1991 ) and it was suggested here that two primordial sites might be initiated and then merge before determinatio, as a single stamen. There are, therefore, various pogsible complementary ¢iews of the perianth/stamen relationship in these plants, but all appear to pivot around the relationship of a subtending foliar organ to some sort of lateral 'axillary' structure. These flowers, then, do lend themselves to a pseudanthial interl::~cation as far as the androecial component is concerned. The gynoecial component of these flowers does not lend itself directly to the, same sort of arguments, since the carpels do not consistently seem to have any sort of superposition relationship to other organs. They are unquestionably carpels since the ovules arise definitely on the actual carpel primordia. Of course this would not preclude their original evolution from gonophyns, but we pt'obably do not have to take this into account in the context of evolution within the group. If a pseudanthial interpretation were to be accorded to the androecial component of the flowers, further discussion of the nature of the gynoecium is probably not very helpful - - there is nolhing much to indicace whether to opt for a hypo~,hcsiswhich equates each carpel or the whole set of carpels with a female flower, and the whole assemblage including androecial aaa gynoecial components would in either case be pseudanthial. Burger (1977) developed a different pseudanthial hypothesis for the evolution of flowers within ~his group. He suggested that the condensation of six flowers like the perfect flowers of Lilaea, i.e. with a single perianth/stamen association and a single carpel, could give rise to a tetracyclic trimerous flower

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like that of Triglochin. He also made a more general suggestion that other types of what we are referring to as 'tepaloid' helobial flowers, and indeed 'petaloid' ones, could be derived by condensation and rearrangement of simple archetypal flowers, which he envisaged as having originally one perianth segment, two stamens, and a carpel. On the whole the arguments are ingenious, but there are defects in detail, particularly in relation to the organisation of Lilaea flowers. Perhaps a more serious argument against Burger's hypothesis is that, in the case of the tepaloid Helobiae at least, all the flowers can be envisaged as being constructed on variations of the same plan without rearrangement. They can all be considered to be built on a plan where the members of successive whorls (taking a perianth/stamen association as a single member) alternate with one another. This applies whatever the number of crg.ans per whorl; it applies whether or not there is more than one whorl of any type; it also applies in the monomerous perfect flowers of Lilaea. It also applies across almost the whole range of floral variation found in Potamogeton (Posluszny, 1981; Charlton and Posluszny, 1991 ). It usually applies in the small flowers with reduced numbers of parts found near the tips of inflorescences in various species; it usually applies in Potamogeton compressus L. and Potamogeton zosteriformis Fern. where there are normally only one or two carpels; in all these cases, where there is a single carpel it may appear to be inserted approximately in the centre of the floral apex (particularly in P. zosteriformis) but it is commonly oriented as though it were positioned between two of the stamens. It applies where there are more than the normal four carpels. A fifth carpel tends to occupy the largest space between and above the whorl of four in P. berchtoldii. In some cases in Potamogeton lucens L. many more carpels may be formed after the first whorl of four, and the first of these supernumerary carpels commonly occur as further alternating pairs or whorls; later carpels are likely to be added in a spiral phyllotactic sequence, alternating with earlier ones. The size relationships between primordia and floral ~t,ex appear to determine how many members occur in a whorl, or whether they occur sin~y. In addition, the pattern of variation in the gynoecium of Potamogeton appears to be largely independent of the pattern of variation in the androecium, so that it seems unlikely on this count too that the Potarnogeton flower is derived from an assemblage of simpler perfect flowers. Sattler (1965) and Posluszny and Sattler (1974a) concluded that the flowers of Potamogeton exhibit features of both 'flower' and 'inflorescence' in the traditional sense. We wish to extend this hypothesis to all the tepaloid Alismatida¢ since: (i) The perianth/androecium relationship can be considered to be more akin to "inflorescence' than 'flower'; (ii) the condition of the g3~oecium is indistinguishable from that of a 'flower'; (iii) the phyllotactic sequence of the flower runs through the initiation of both the perianth/stamen associations and the gynoecium.

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Using data for Triglochin striata Ruiz and Pavon from Lieu (1979), and data from Triglochin maritimum L., Charlton ( 1981 ) concluded that the inflorescence of Triglochin can be considered to have some features which are traditionally associated with 'flower' in the traditional sense. The arguments presented below are based on Triglochin but they apply also in greater or lesser measure to other tepaloid Alismatidae. Lateral structures in the inflorescence are initiated without subtending bracts. $cheuchzeria palustris L. is an exception here, since all flowers except the uppermost are subtended by well-developed bracts. Potamogeton may also represent an exception, since there are structures which have been called bracts in a number of species (Posluszny and Sattler, 1974a; Posluszny, 1981; Charlton and Posluszny, 1991 ). Since the bract in these cases is normally initiated at least as much on the developing flower primordium as on the inflorescence, it is quite possible it is not a bract in the normal sense of the word. When organogenesis is complete a residual meristem is generally left at the tip of the young inflorescence. This occurs also in Potamogeton spp., particularly those with paired or whorled arrangements of flowers (Charlton and Posluszny, 1991 ) and in Lilaea (Posluszny et al., 1986). In Scheuchzeria the inflorescence meristem is ultimately converted into a floral mefistem (Posluszny, 1983). In larger inflorescences, and indeed some quite small ones, there is a strong tendency to have a whorled arrangement of lateral structures (including pairs as two-membered whorls) on the inflorescence. This has been recorded in Lilaea (Posluszny et al., 1986) and several species of Potamogeton (Posluszny and Sattler, 1974a; Charlton and Posluszny, 1991 ) as well as in

Triglochin. In the only case which has been studied in detail, T. striata (Lieu, 1979) the lateral primordia are initiated like leaf primordia in that peficlinal cell divisions occur in several layers of cells including the subepidermal layer; however, the same a~pearance would be presented if the inflorescence apex had only one tunica layer. The flowers of Triglochin and Lilaea each receive only a single vascular trace from the inflorescence vasculature (Uhl, 1947). This is the same as a perianth segment receives. This appearance may, however, be deceptive; flowers of Potamogeton receive only a single bundle but this appears to be a compound bundle (Uhl, 1947). The flower of Scheuchzeria, on the other hand, is supplied by numerous bundles (Uhl, 1947). A number of the features of these inflorescences, then, are reminiscent of 'flower' in the traditional sense, but also some of the features of the flowers are reminiscent of 'inflorescence' in the traditional sense. Are the two structures different expressions of the same original structure? We have previously made this suggestion in rather different terms (Posluszny et al., 1986): that the range of reproductive structures in the Alismatidae might be derived by

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radiation from a common point at which demarcation between fower an~ inflorescence did not exist in the traditional sense. Now we wish to take this as a working hypothesis which might be extended to include all the Alismatidae. There are a few other observations which may add to the hypothesis. In Lilaea 'inflorescence" and 'flower" pathways seem to be related alternatives with some possibilities for a continuum of intermediates. The primordia at the base of the inflorescence have the potential to develop into either female flowers (represented here by a single carpel), inflorescence branches, or even intermediate structures, e.g. a female flower with, at its base, a small inflorescence branch or a smaller female flower. The distribution of sexuality in the flowers and inflorescences is conventional on the whole but there are some interesting features. In the inflorescence of Lilaea female flowers occur at the base, bisexual in the middle, and male at the top. This polarisation is the reverse of that found in flowe~, both in general and in the Alismatidae. On the other hand, sexual development within flowers can be considered to be polarised in another way, in relation to the longitudinal axis of the inflorescence, because stamen development occurs at the side of the flower towards the base of the inflorescence, carpel development towards the top. This statement could even be considered to include the unisexual flowers, since their perianth/stamen associations, or carpels are oriented in the same direction as those in perfect flowers. The same polarisation of floral development in relation to the longitudinal axis of the inflorescence axis actually occurs in some cases with quite uniformly bisexual flowers. In flowers of T. striata six stamen primordia are initiated, but only the stamens positioned towards the base of the inflorescence in each flower normally develop microsporangia (Lieu, 1979). There are related situations in the gynoecium of Potamogeton (Charlton and Posluszny, 1991 ). In P. compressus, which normally has only one or two carpels, the carpels, occur much more frequently at the side ofthe gynoecial area towards the tip of the inflorescence. In flowers of Potamogeton with five carpels four alternate normally with the stamens, and the fifth occupies one of the positions alternating with the first four; this is almost invariably the position towards the tip of the inflorescence. In all these cases, whatever the distribution along the inflorescence of the sexuality of individual flowers, there is a tendency for the distribution of sexuality within flowers to become polarised in relation to the longitudinal axis of the inflorescence; this polarisation is in the same direction as that w~hin conventional bisexual flowers. Phyllotactically, inflorescences are more variable than flowers. This can b~ within species and within a genus, and both apply in Potamogeton. Here flow~ers are basically tetramerous with alternating whorls, but there is some possibility for variation; the phyllotaxis ofinflorescences ranges from simple distichous or spiral arrangements in few-flowered species, through cases where

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paired arrangements are usual, to cases with large numbers of flowers which can have spiral or whorled arrangements. On a comparative basis within the tepaloid Alismatidae, we have to conclude that, although what we describe colloquially as 'flower' and 'inflorescence' each have features reminiscent of the other, they do not actually resemble each other very closely. However, they could be derived from an original reproductive structure which was not differentiated at all into the two components (i.e. in a pre-floral state - - after Emberger, 1950, 1951 ). We simply have to propose that the original structure was multiaxial; the main axis became differentiated into 'inflorescence' and the lateral axes became condensed and differentiated into 'flowers'. The polarisation of sexuality differs along the longitudinal axes of flower and inflorescence, and it is necessary to rationalise this. There is the consoling fact that there is a sort of secondary polarisation of sexuality in some of the inflorescences. Ifa similar effect were operative at the time the lateral axes of our hypothetical multiaxial structure were becoming condensed and differentiated into flowers, the standard distribution of sexual structures within flowers could be reached. We accept that this is mere speculation at this remove in relation to the evolution of the gro,.:p! From the evidence available for the group the basic components of the original reproductive structure would be, on the one hand, a carpel, and on the other a stamen superposed over a perianth segment. It is doubtful whether either of ti-~ese could be described as a 'flower' and consequently our hypothesis is not a pseudanthial one. We are envisaging the group as demonstrating how a structure which the eye sees as flowers assembled on an inflorescence could be derived from archaic pre-floral components. TH E FLOWER A N D T H E INFLORESCENCE IN ' P E T A L O I D ' FAMILIES

Considering this group with the same hypothesis in mind, the reproductive structures of the Alismataceae stand out at once as a starting point because the fower and the inflor~escence share trimerous symmetry. The only consistent exception occurs in Ranalisma, where the inflorescence bracts are paired (Buchenau, 1903; Den Hartog, 1957), and this exceptional case will be considered later. The symmetry and development of the flowers of several Alismataceae have been described latterly by Kaul (1967a), Singh and Sattler (1972, 1973, 1977a), Leins and Stadler (1973) and Sattler and Singh (1978). The tbllowing account is drawn from the review of the whole area given by Sattler and Singh (1978). The three sepals arise in rapid spiral succession. Three petal/ stamen complexes are then formed in alternation with the sepals. Each complex consists of a petal and a pair (at least) of stamens. In some cases three common primordia, called CA primordia, arise successively preceding the appearance of the complexes, a~d a petal and two stamen primordia arise on

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each. There is a continuum between this condition and one where the specific association between each petal and pair of stamens is reflected only in the time of initiation of each complex. S~lbsequently further stamens may arise in alternation with the six derived from She three complexes, in some cases only in the three sites directly above the complexes. In flowers with large numbers of stamens they continue to be initiated approximately in a/ternating whorls. In fowers with small numbers of stamens, carpels may arise initially in three groups alternating with the three petal/stamen complexes, in some species (but not in others) preceded by the appearance of relatively evident primary gynoecial primordia on which the carpels subsequently arise. In other cases the carpels arise approximately in whorls. Sattler and Singh concluded that the primary pattern of these flowers (and others in the Alismatales) is trimerous: after the formation of the three sepals, the three petal/ stamen complexes form another trimerous element alternating with the sepals, and trimery is continued into the gynoecium when the carpels are initiated in three groups. Each carpel normally has one ovule. Inflorescence structure was reviewed by Charlton (1973). The inflorescences are also built on a trimerous plan: bracts are formed in pseudowhorls of three, in one cycle or in several alternating cycles. The bracts subtend flowers, cymose flower complexes, or, in the lower part of large inforescences, inflorescence branches which repeat the trimerous plan of the main axis of the inflorescence. In some cases inflorescences of submerged plants m~y become more or less sterilised and modified in relation to vegetative reproduction. In the more extreme examples the modified inflorescences are distinctive horizontally growing structures of more or less unlimited growth, producing daughter plants at intervals, and these have been called pseudostolons (Den Hartog, 1957; Charlton, 1968), Departures from trimery occur occasionally in small forms of Echinodorus tenellus (Mart.) Buch., where bracts may occasionally occur in pairs rather than threes (Charlton, 1974). Other forms of departure fro~ trimery occur in species described as having heterogeneous inflorescences (Charlton, 1973): in these the first bract of the inflorescence normally does not subtend a lateral structure, and there may be differences between the three lateral structures associated with each subsequent pseudowhorl of bracts. In many cases the main axis of the inflorescence terminates in a flower whose three sepals alternate with the last cycle of bracts, and if there are any inflorescence branches they terminate similarly. In the Alismataceae the whole reproductive assemblage, inflorescence and flowers, can be described as a multiaxial reproductive structure with trimerous symmetry, the trimery being continuous throughout the structure, based on bracts and the structures they subtend in the proximal .~egion,and on ~loral organs and assemblages of floral organs in the dista~ region. This is merely a description, but it is strikingly reminiscent of the way in which we are viewing the reproductive structvres of the tepaloid Alismatidae, and it may be useful

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to see whether a similar hypothesis could be erected for the petaloid types. However, before attempting this, we should examine the organisation of the reproductive structures of the other petaloid Alismatidae. In the sole member of the Butomaceae, Butomus umbellatus L., the inflorescence has a pseudowhorl of three bracts, each subtending a complex cymose arrangement of flowers, and inflorescence growth finishes with the production of a terminal flower (Charlton and Ahmed, 1973b; Wilder, 1974a). This, like the other flowers, has a trimerous plan very similar to some of those of the Alismataceae, including the relationship between petal and stamen pair (Singh and Sattler, 1974; Sattler and Singh, 1978). The carpels differ from those of Alismataceae, having numerous ovules in laminar placentation. This feature is shared with Limnocharitaceae and Hydrocharitaceae. The genus Ranalisma forms a connecting link between the Alismataceae and Limnocharitaceae; Charlton and Ahmed (1973b) suggested that it represented an offshoot from the common stock which gave rise to these families. The actual morphology of the solitary trimerous terminal flower of Ranalisma is typical of the Alismataceae (Buchenau, 1903), and in Ranalisma humile (Kuntze) Hutck this includes the general nature of the trimery (Charlton, 1991 ). The vascular structure of the flower of this small plant is disproportionately complex among small Alismataceae. There are two largely independent vascular systems - - an inner and an outer - - resembling those of some of the large Alismataceae and reminiscent of those of the Limnocharitaceae (Charlton and Ahmed, 1973a). The inflorescence has only two subopposite bracts, one of which subtends a lateral complex which allows the inflorescence to branch sympodially - - in this respect it is very similar to Limnocharitaceae and quite different to the rest of the Alismataceae (Charlton and Ahmed, 1973b)o Floral organogenesis in R. humile is in general typical of the Alismataceae, including the formation of CA primordia, but it is unique among the Alismatidae in having unidirectional development up to the stage of initiation of the first six stamen primordia (Charlton, 1991 ). The sepal primordia and the CA primordia are initiated first towards the side of the flower adjacent to the lateral branch complex of the inflorescence - - in fact the third CA primordium, which would be expected at the other side of the flower, does not appear as such. Petal primordia and the associated stamen pairs appear first toward the side of the flower nearest to the lateral branch complex, i.e. where the CA primordia had formed. The third petal and stamen pair arise rather later at the opposite side of the flower without being preceded by a CA primordium. Stamens may occasionally be replaced by petals. Positionally the unidirectional development is related to the plane of bilateral symmetry of the inflorescence and, in developmental terms, may actually represent a continuation of it. Taking Ranalisma as a partial link between Alismataceae and

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Limnocharitaceae, its unidirectional form of development may be evidence that the trimerous flower plan is not necessarily fundamental to the group. Nevertheless, the flower plan of those Limnocharitaceae which have been studied is basically trimerous, though differing in detail from the situation in the Alismataceae, particularly in having centrifugal stamen development. In Hydrocleis nymphoides (Wind.) Buch. the plan is the same as in many Alismataceae up to the formation of CA primordia and initiation of the first six stamens as three pairs associated with the three petals (Sattler and Singh, 1973). After that the carpel primordia are initiated in a whorl, and subsequently stamens and then staminodes are formed alternating with the first six in a centrifugal pattern. In Limnocharisflava (L.) Buch., as described by Sattier and Singh (1977), there are no CA primordia, and the three petals are formed in alternation with the three sepals. Three pnmary androecial primordia are then formed, alternating with the petals, and three stamens are initiated on each ofthese. Further stamens are initiated between these groups and then more whorls of stamens~ and finally staminodes, are initiated centrifugally in alternating whorls. Carpel primordia are formed at first in three groups alternating with the petals and therefore superposed above the groups of stamens formed on the primary androecial primordia. In both Hydrocleis and Limnocharis there are numerous ovules inserted on the radial walls ofthe carpels. The inflorescences of Limnocharitaceae, as already mentioned, are quite similar to those of Ranalisma. In both Hydrocleis nymphoides and Limnocharis./lava there are two subopposite bracts, the first of which subtends a lateral branch complex, and a terminal flower. The lateral branch complex consists of a cymose arrangement of flowers and the cymose development is terminated by the production of a vegetative bud which can give rise to another inflorescence after a period of vegetative growth in Limnocharis (Wil~ der, 1974a), or almost immediately in Hydrocleis so that the horizontal inflorescence appears to grow indefinitely, producing a cluster of flowers and a vegetative shoot at intervals (Charlton and Ahmed, 1973b; Wilder, 1975). The Hydrocharitaceae exhibit an enormous range of floral and inflorescence characters in comparison with the Alismataceae, Butomaceae and Limnocharitaceae. Comparative developmental information is rather lacking. The flowers are commonly dioecious and show adaptations to various forms of hydrophily or insect pollination (Sculthorpe, 1967; Kaul, 1968b; Cook, 1982). The ovary is always inferior with a number of loculi and there are normally fairly numerous ovules attached to the radial walls of the loculi, in a manner reminiscent of Limnocharitaceae. Some of the flowers appear to be extremely reduced. Some of the larger flowers have a well-developed perianth of sepals and petals, and stamens associated in pairs along antesepalous and antepetalous radii. The associations of stamens b~ve been considered to be derived from stamen fascicles (Kaul, 1968b). However, in development the flowers

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ofHydrocharis morsus-ranae L. show regular formation of alternating trimerous whorls ofperianth and androeeial structures and there is no evidence for fasciculate development (Scribailo and Posluszny, 1985). In the androecium of the male flower four whorls are formed, the uppermost of which become staminodes; subsequent intercalary growth at the base elevates radially adjacent pairs on what appears to be a common structure. In the female flower only one whorl of staminodial primordia is formed alternating with the petals and these primordia usually bifurcate during development, giving paired staminodes. Although the ovary is inferior, gynoecial development begins with the formatior of a whorl of six horseshoe-shaped primordia much resembling those found in Limnocharitaceae (e.g. Sattler and Singh, 1973, 1977) and it is subsequent intercalary development which gives rise to the inferior condition. In many cases there is an intricate interrelationship between inflorescences and stolons (W;,lder, 1974b,c, 1975) and there appears also to have been a tendency towards simplification by suppression of bracts and bracteoles (Kaul, 1970; Wilder, 1975). Development of these structures usually involves apical bifurcation and in some of these cases, particularly those with tendencies to eliminate subtending foliar structures, it is difficult to decide how to describe the branching pattern. Kaul (1970) proposed that the basic form of the inflorescence was one with two bracts each subtending a sympodium of flowers; although there appeared to be a terminal flower he was not entirely convinced about this. It is probable that the relationship between inflorescence and flower in this complex family is originally similar to that in Ranalisma and the Limnocharitaceae. There are a few significant observations which can be made at this point. There are enough features of floral structure and development in common among the petaloid Alismatidae, as well as features of the reproductive and vegetative shoots, that they must be considered a natural group (see Tomlinson, 1982). The Alismataceae in fact are the 'odd family out' in the group in terms of carpel structure and the trimerous inflorescence plan (though this is shared with Butomaceae). The basic plan of the reproductive shoot in the group seems therefore to be an inflorescence with two bracts, at least one of which subtends a lateral structure, and an apparently terminal trimerous flower. Earlier in this section we gave a description of the organisation of the reproductive shoots of the Alismataceae and pointed out that it resembled the concept of a multiaxial reproductive structure which we had developed for the tepaloid Alismatidae. However, it seems unlikely from the isolated features of the Alismataceae that the family can be used as a model for the group. Rather we should consider how it could be derived from the basic plan of the group. It could be derived quite simply from the basic plan form by two processes: an invasion of an element of the flower, the trimery, from the flower

315

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into the bract arrangement of the inflorescence, and an extension of the growth of the inflorescence in many cases to include further trimerous sets of bracts. In relation to this it is interesting to note that inflorescences nearest to the supposed ancestral plan, those with only one or sometimes two sets of bracts, differ quite consistently in other characters from the inflorescences with more extensive growth. The data for this comparison are extracted from Charlton (1973), and given in Table 1. A recognisable terminal flower is present in all cases with restricted growth, but inflorescences of extensive growth often terminate by abortion, and this is presumably a derived state. Inflorescences of extensive growth are normally homogeneous, i.e. all the bracts in a set subtend the same general kind of lateral structure, though there may be a gradient of complexity along the inflorescence. Inflorescences of restricted growth are normally heterogeneous, and, except for R. humile, this is expressed by the first bract of the inflorescence not subtending a lateral structure, while all subsequent bracts do. The sterility of the first bract could be considered to make it more sepal-like, and this would be compatible with a condition of invasion of floral features into the inflorescence. In the more extensive inflorescences this relic of floral feature seems to have been lost. Luronium natans (L.) Rat'. appears to be exceptional, but the inflorescence here also functions as a pseudostolon, and the exceptions reside in modifications associated with that. The features reminiscent of 'flower" in the inflorescence of Alismataceae TABLE I

Some inflorescence features in the Alismataceae

Alisma Burnatia Caldesia Echinodarus subgenus Echinodorus Limnophyton Sagittaria Baldellia Damasonium Echinodorus subgenus Helianthium Luronium Ranalisma

Number of cycles of bracts

Heterogeneous

Terminal flower present

Several Several Several

No

Yes Not always Not always

Several Several Several 1 (-2)

No No

1

1 (-2) Several 1 (2 bracts)

but develops further sympodially

No No

No Yes Yes

Yes Yes Not usually Yes Yes

Yes Yes Yes

Yes

Yes No

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U. POSLUSZNYANDW.A.CHARLTON

appear then to be rather unimportant in relation to the Alismatidae as a whole, or ever just the petaloid Alismatidae; they are merely a secondary specialisation. What appears to be the basic reproductive structure is a very simple inflorescence with two bracts which may subtend lateral floral complexes, and a terminal flower with some form of trimerous symmetry. In contrast to the situation in the tepaloid Alismatidae, there is not an immediately apparent problem in the petaloid group in separating flower from inflorescence, but the reproductive structure is still a multiaxial one, differing from that of the tepaloid series in that all axes can terminate in flowers. We could propose, then, for the petaloid series that all axes of the proposed original multiaxial reproductive structure became differentiated proximally into 'inflorescence' and distally into 'flower'. We then have to attempt to answer the question: are the proposed basic components of the tepaloid group, or derivatives of them, perceptible in the petaloid group? POSSIBLE HOMOLOGIES BETWEEN REPRODUCTIVE STRUCTURES OF THE PETALOID AND TEPALOID ALISMATIDAE

The carpels of the two groups do not show exactly the same range of structure, but the carpels of the Alismataceae link the two groups. This family normally has carpels developmentally very similar to those of most of the tepaloid group: they develop through a peltate stage and initiate a single ovule on the cross-zone. Carpels of Butomaceae and Limnocharitaceae do not have a peltate stage and have numerous ovules in laminar placentation; the inferior ovary of Hydrocharitaceae appears to be a modification of this state. It seems reasonable to conclude that the gynoecial components are homologous. Kaul (1976) pointed out that the carpel vasculature ofDamasonium polyspermum Cosson particularly linked the conditions in Alismataceae and Limnocharitaceae. He also concluded that laminar placentation was probably primitive within the Alismatales. It is much more difficult to homologlse the remaining components. As a starting point we propose that petals and stamens may be homologous in the petaloid group. Evidence for this can be drawn from R. humile where stamens can be replaced by petals as a result of experimental treatment (Charlton 1979 ) or in undisturbed plants (Charlton, 1991 ). There is also evidence from occasional teratologies ofLuronium natans that the petal/stamen pair in AIismataceae may actually represent a partly sterilised stamen fascicle: very occasionally it has been found to be replaced by a single stamen in experimentally treated and control plants (Fig. 1 ). However, the perianth/stamen association in tepaloid AlismatJdae is so strong that one miO~t see the petal/ stamen pair association as a similar relationship. Our suggestion rather discounts this possibility; instead we propose that, if the stamen or stamen fas-

EVOL!JTIONOFTHEHELOBIALFLOWER

317

Fig. 1. Transverse sections of flower buds ofLurotdum natans. (a) Normal fl~3wer,from plant grown in control medium with 1% sucrose, with three sepals (S), and three petal/stamen pairs comprising aRogether three petals (P), and six stamens ( • ) . (b) Flower from plant treated with 100 mg 1-t gibberellic acid in culture medium containing 2% sucrose. There are three sepals (S), one petal/stamen pair comprising a petal (P) with two associated stamens ( • ) , ant~ the other two petal/stamen associatiens have been replaced by single stamens ( A ).

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U. POSLUSZNYAND W.A.CHARLTON

cicle in petaloid Alismatidae did originally have a subtending structure, it has been suppressed. The relative situation is actually little different from that of the flowers in Alismatidae which are initiated without subtending bracts in most of the tepaloid group, and with subtending bracts in the petaloid group. There is another curious feature in the androecium of the petaloid group. Though the earliest-formed stamens are associated with petals, forming three groups, subsequently formed stamens may not be specifically associated with the groups and simply follow an approximately whorled phyllotactic system as a whole in the flower. A simple explanation for this would be that there is a continuum between the 'fascicles' formed first and single stamens formed later. This explanation would be suitable for centripetal and centrifugal forms of initiation. There is no evidence for stamen fascicles in the tepaloid Alismatidae but our arguments imply that the stamen here may be homologous with a fascicle. The arguments above are based on a trimerous arrangement of possible fascicles in the petaloid group. It should be acknowledged that what is known of the vascular anatomy of these flowers tends to give an entirely different impression. In Alismataceae with relatively small numbers of stamens their vascular traces usually arise separately from the central vascular system (Singh, 1966; Charlton and Ahmed, 1973a). Where there are numerous stamens they may be innervated by branches from common trunk bundles, but these do not correspond with the positions of the three fascicles we have identified and they are more numerous (Kaul, 1967a, b, 1968a). Only in Alisma triviale Pursh is there any suggestion of a common vascular supply to the petal and associated stamens (Singh and Sattler, 1972). An argument related to that used above for the stamens and petals can be used for the sepals of the petaloid group. While stamens or stamen fascicles could represent structures which had lost their subtending associates, the sepals could represent phyllomes which no longer subtended lateral structures. Thus a stamen or stamen fascicle, or a sepal, would represent different derivations of the same initial complex structure. The situation in Limnocharis ]lava, where primary androecial primordia alternate with petal primordia in a manner not observed in other petaloid types, probably implies that the petals here are homologous with sepals. Continuing our efforts to pursue homologies, there is probably also a relationship between bracts and sepals. There is a continuum of a kind between bracts and sepals in the Alismataceae, in that they are similar in appearance and form a continuous phynotactic series in many cases. There is perhaps a relationship between the tepals and the 'bracts' which are initiated partly on the floral apex in Potamogeton. If the homology can be extended to the bracts in Limnocharitaceae, Hydrocharitaceae, Butomacea¢ and Ranalisma, then we have generated a hypothesis which enables us to suggest where and how the divergence between the petaloid and tepaloid groups occurred in the evolution of flowers and inflorescences. We have made a case for the tepaloid

EVOLUTION OF THE HELOBIAL FLOWER

319

types that the main axis of an original multiaxial reproductive structure became differentiated into inflorescence while the lateral axes became differentiated into flowers. We have made a case for the petaloid types that all axes of a multiaxial structure became did'erentiated distally into flower and proximally into inflerescence. If our plan of homology is accurate then we can equate bract, sepal and tepal with one phyllomic component of the original structure, which subtended a lateral complex. The lateral complex has become resolved into a stamen in the tepaloid types, and is still associated with the phyllomic component. In the petaloid types the lateral complex is likely to be an inflorescence branch of some kind, when we describe the phyllome as a bract, or it may be suppressed, when we describe the phyllome as a sepal; finally the phyllome may be suppressed and the lateral complex represented by a stamen or stamen fascicle. We suggest that the divergence between the tepaloid and petaloid types involved the divergence of the relationships between phyllome and subtended structure in the two groups, at the same time that the axes of the original multiaxial structure became differentiated into inflorescence and flower in different ways in the two groups. At this stage the Aponogetonaceae remain as an individual group. The flowers are basically trimerous, though there may be increase in numbers of meml~ers in either androecium, gynoecium, or both; they do not show perianth/stamen superposition; there seems to be a trend towards reduction of perianth; the flowers are not subtended by bracts; there are several ovules per carpel. The reproductive morphology of this group could reaeily be derived from our hypothetical multiaxial reproductive structure by a rather different combination of the processes we have suggested above. The arrangement in Scheuchzcria also is rather individual, but it too can be derived from our hypothetical s**ructure by a combination of the processes suggested above. It seems to differ from other tepaloid cases in the manner in which the main axis of the structure has been modified: it has acquired inflorescence character proximally and flower character distally. In this feature, and in the presence of well-defined bracts, it resembles the situation in the petaloid group rather than the tepaloid group. There is a curious possible parallel in a matter of symmetry between some petaloid and tepaloid types. The flower of R. humile shows unidirectional development (Charlton, 1991 ) so that organ ":nitiationoccurs first at the side away from the continuation vegetative bud at the base of the inflorescence. In Triglochin (Lieu, 1979; Charlton, 1981 ) and in Potamogeton (Charlton and Posluszny, 1991 ) the initial rate of development of lateral structures on the inflorescence is accentuated at the side away from the corresponding continuation vegetative bud~ and reduced at the opposite side, sometimes to the point of suppression of development.

320

U. POSLUSZNYANDW.A.CHARLTON

T H E FLOWER A N D INFLORESCENCE IN T H E EXTRA-SIMPLE TYPES

We think that all the Alismatidae with simple floral structures, often unisexual and often terminating branches, must be viewed as cases of reduction. In many of them there are structures which appear to represent perian~h, and there are other features which may be derived from a flower type of plan. However there are also some quite eccentric features. We give a brief review below in which the main source of data is Tomlinson ( 1982); other particularly pertinent references are cited individually. In the Zannichelliaceae, two general. Althenia and Lepilaena have a threemembered perianth in the flowers of both sexes; Zannichellia and Pseudalthenia (= Vleisia) have a spathe-like structure which may represent a perianth but only in the female flower. The female flower has a small number of carpels and these are oriented, in relation to the axis on which they are born, exactly as are carpels in the flowers of other Alismatidae (see Posluszny and Sattler, 1976a; Posluszny and Tomlinson, 1977). The male flower has a single stamen which may have from two to eight microsporangia according to the species. There is little to indicate whether the more elaborate forms might represent stamen fascicles or fused stamens. There is no vestige ofperianth in the Cymodoceaceae, except for a transient ridge that forms below the stamens in the male flower of Syringodium filiforme Kiitz. (Tomlinson and Posluszny, 1978). The male flowers consist otherwise of two stamens fused back to back, and the female flowers oftwe carpels, again in a flower-like orientatk, n. Posidoniaceae are described as having a racemose inflorescence, with branches subtended by bracts. The ultimate branches bear a few '~terile bracts below a zone with a few naked flowers which are not subtended by bracts. The flowers normally consist of three stamens with expanded connectives and a single carpel. The Najadaceae represent the ultimate in simplicity in this group. The male flower terminates a branch, and consists solely of a stamen surrounded by two raembranous involucres. The female flower is represented by an apparently terminal ovule surrounded by a single involucre, and can be described as acarpellate in the sense ofSattler (1974). Viewing these 'extra-simple' types as cases of reduction, we feel there is in general not enough evidence to speculate on what they might be reduced from. They could be reduced from a pre-floral state, but they could equally well be reduced from a condition with recognisable flowers. The former is quite possibly the case in Posidoniaceae where the ultimate branches of the inflorescence are quite reminiscent of the ultimate branches of tepaloid Alismatideae; the latter is probably the case in Zannichelliaceae where a number of flowers have a three-membered perianth.

EVOLUTION OF THE HELOBIAL F L O W E R

321

CONCLUSION We realise that the speculations presented here are likely to remain no more than speculations. Nevertheless they do provide a basis for envisaging the Alismatidae as demonstrating the results of deriving a 'flower" and an 'inflorescence' plan in different ways from a pre-floral state. This might be taken to imply that the Alismatid~e provide a key to the origin of the flower. However, we think that this general view is not justified except in a comparative sense. The Alismatidae are actually quite a specialised group of plants (Tomlinson, 1982) and consequently they may represent a special case of evolution of reproductive structures. Additionally, like any evolutionary plan, the sequence could also be taken to run in the reverse direction, in which case we have a group of plants in which the features of'flower" and 'inflorescence' are being redistributed within the reproductive shoot. Homeotic genes have been identified in some dicotyledons which can alter the distribution and nature of whorls of floral organs to various degrees (see review in Coen and Meyerowitz, 1991 ) and similar genetic changes might have been involved in some aspects of the evolution ofhelobial flowers and inflorescences. The discussion has evaded entirely the nature of the carpel: all the groups have satisfactorily carpellate gynoecia except the Hydrocharitaceae which can nevertheless be derived from such a condition, and the (presumed) reduced Najadaceae. We have, however, needed to consider the relationship between stamens, stamen fascicles, perianth segments which may represent sterilised stamens, and perianth segmen',s which may subtend stamens or stamen fascicles. If there is a unified theme in this aspect of the reproductive structures of the Alismatidae, it seems to be one of derivation from a condition resembling a gonophyll (after Melville, 1962, 1963) or, perhaps a more appropriate concept, an androclad/ bract unit (Meeuse ( 1966 ) after Neumayer, 1924).

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Charlton, W.A., 1979. Studies in the Alismataceae. VIII. Experimental modification of organogenesis in Ranalisma humile. Can. J. Bot., 57: 223-232. Charlton, W.A., 1981. Features of the inflorescence of Triglochin maritima. Can. J. Bot., 59: 2108-2115. Chaflton, W.A., 1991. Studies in the Aiismataceae. IX. Development of the flower in Ranalisma humile. Can. J. Bot., 69: 2790-2796. Charlton, W.A. and Ahmed, A., 1973a. Studies in the Alismataeeae. III. Floral anatomy of Ranalisma humile. Can. J. Bot., 51: 891-897. Chaflton, W.A. and Ahmed, A., 1973b. Studies in the Alismataceae. IV. Developmental morphology of Ranalisma humile and comparisons with two members of the Butomaceae, Hydrocleis nymphoides and Butomus umbellatus. Can. J. Bot., 51: 899-910. Charlton, W.A. and Fosluszny, U, 1991. Meristic variation in Potamogeton flowers. Bot. J. Linn. Soc., 106: 265-293. Coen, E.S. and Meyerowitz, E.M., 1991. The war of the whorls: genetic interactions controlling flower development. Nature, 353:31-37. Cook, C.D.K., 1982. Pollination mechanisms in ihe Hydrocharitaceae. In: J.J. Symoens, S.S. Hooper and P. Compare (Editors), Studies on Aquatic Vascular Plants. Royal Botanical Society of Belgium, Brussels, pp. 1-15. Den Hartog, C., 1957. Alismataceae. Flora Malesiana Ser. 1 Sperma~ophyta, 5:317-334. Emberger, A., 1950. La va!eur morphologique et i'origine de la fleur (Apropos d'un¢ theorie nouvelle). Ann6e Biol., 26: 279-296. Emberger, A., 1951. L'origine de ia fleur. Experientia, 7:161-168. Hegelmaier, F., 1870. 0ber die Entwicldung der Bliithentheile yon Potamogeton. Bot. Ztg., 18: 283-320. Hutchinson, J., 1959. The Families of Flowering Plants. II. Monocotyledons. Second Edition. Clarendon Press, Oxford, pp. 511-792. Kaul, R.B., 1967a. Development and vasculature of the flowers ofLophotocarpus calycinus and S-gittaria latifolia (Alismaceae). Am. J. Bot., 54:914-920. Kaul, R.B., i 967b. Ontogeny and anatomy of the flower of Limnocharisflava (Butomaccae). Am. J. Bot., 54: 1223-.1230. Kaul, R.B., 1968a. Floral development and vasculature in Hydrocleis nympkoides (Butomaceae). Am. J. Bot., 55: 236-242. Kaul, R.B., 1968b. Floral morphology and phylogeny in the Hydrocharitaceae. Phytomorphology, 18:13-35. Kaul, R.B., 1970. Evolution and adaptation of inflorescences in the Hydrocharitaceae. Am..I. Bot., 57: 708-715. Kaul, R.B., ! 976. Conduplicate and specialized carpels in the Alismatales. Am. J. Bot., 63:175182.

Kunth, C.S., ! 841. Enumeratio Plantarum. Vol. 3. J.G. Cotta, Stuttgart arid Tiibingen, 752 pp. Laeroix, C. and Sattler, R., 1988. PhyUotaxis theories and tepal-petal superposition in Basella rubra. Am. J. Bot., 75: 906-917. Leins, P. and Stadler, P., 1973. Entwicklungsgeschichtliche Un~ersuchungen am Androecium der Alismatales. Oesterr. Bot. Z., 121: 51-63. Lieu, S.M., 1979. Organogenesis in Triglochinstriata. Can. J. Bot., 57: 1418-1438. Markgraf, F., 1936. Bliitenbau und Verwandschaft bei den einfachsten Helobiae. Ber. Dtsch. Bot. Ges., 54: 191-229. Meeuse, A.D.J., 1966. Fundamentals of Phytomorphology. Ronald Press, New York, 231 pp. Melville, R., 1962. A new theory of the Angiosperm flower. I. The gynoeeium. Kew Bull., 16: 1-50.

Melville, R., 1963. A new theory of the Angiosperm flower. II. The androecium. Kew Bull., 17: 1-63.

Miki, S., 1937. The origin of Najas and Potamogeton. Bot. Mag. (Tokyo), 5 h 472-480. Neumayer, H., 1924. Die Geschichte der Bliite. Abh. Zooi. Bot. Ges. Wien, 14:1-112.

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Posluszny, U., 1981. UnicarpeUate floral development in Fotamogeton zosteriformis. Can. J. Bot., 59: 495-504. Posluszny, U., 1983. Re-evaluation of certain critical relationships in the Aiismatidae: floral organogenesis of Scheuchzeria palustris (Scheuchzeriaceae). Am. J. Bot., 70: 925-933. Posluszny, U. and Sattler, R., 1973. Floral development ofPotamogeton densus. Can. J. Bot., 5 l: 647-656. Posluszny, U. and Sattler, R., 1974a. Floral development ofPotamogeton richardsoniL Am. J. Bot., 61: 209-216. Posluszny, U. and Sattler, R., 1974b. Floral development of Rupp/a maritima var. maritima. Can. J. Bot., 52: 1607-1612. Posluszny, U. and Sattler, R., 1976a. Floral development ofZannichellia palustris. Can. J. Bot., 54:651-662. Posluszny, U. and Sattler, R., 1976b. Floral development of Najasflexilis. Can. J. Bot., 54: 1140-1151. Posluszny, U. and Tomlinson, P.B., 1977. Morphology and development of floral shoots and organs in certain Zannichelliaceae. Bot. J. Linn. Soc., 75:21-46. Posluszny, U., Charlton, W.A. and Jain, D.K., 1986. Morphology and development of the reproductive shoots of Lilaea scilloides (Poir.) H auman (Alismatidae). Bot. J. Linn. Soc., 92: 323-342. Sattler, R., 1965. Perianth development ofPotamogeton richardsoniL Am. J. Bot., 52:35-41. Sattler, R., 1974. A new approach to gynoecial morphology. Phytomorphology, 24: 22-34. Sattler, R. and Singh, V., 1973. Floral development of Hydroc/eis nymphoides. Can. J. Bot., 51: 2455-2458. Sattler, R. and Singh, V., 1977. Floral organogenesis of Limnocharisflava. Can. J. Bot, 55: 10761086. Sattler, R. and Singh, V., 1978. Floral organogenesis ofEchinodorus amazonicus Rataj and floral construction of the Alismatales. Bot. J. Linn. Soc., 77: 141-156. Scribailo, R.W. and Posluszny, U., 1985. Floral development of Hydrocharis morsus-ranae (Hydrocharitaceae). Am. J. Bot., 72: 1578-1589. Sculthorpe, C.D., 1967. The Biology of Aquatic Vascular Plants. Edward Arnold, London, 6 i0 PP. Singh, V., 1966. Morphological and anatomical studies in Helobiae. VI. Vascular anatomy of the flower of Alismaceae. Proc. Natl. Acad. Sci. India, R 36: 329-344. Singh, V. and Sattler, R., 1972. Floral development ofAlisma triviale. Can. J. Bot., 50: 619627. Singh, V. and Sattler, R., 1973. Nonspiral androecium and gynoecium of Sagittaria iatifolia. Can. J. Bot., 51: 1093-1095. Singh, V. and Sattler, R., 1974. Floral development ofButomus umbellatus. Can. J. Bot., 52: 223-230. Singh, V. and Sattler, R., 1977a. Development of the inflorescence and flower of Sag/ttaria cuneata. Can. J. Bot., 55:1087-1105. Singh, V. and Sattler, R., 1977b. Floral development ofAponogeton natans and A. undulatus. Can. J. Bot., 55:1106-1120. Snow, M. and Snow, R., 1942. The determination ofaxillary buds. New Phytol., 41: 13-22. Tomlinson, P.B., 1982. Anatomy of the Monocotyledons. VII. Helobiae (Alisma~idae) ed. C.R. Metcalfe (Editor), Clarendon Press, Oxford, 559 pp. Tomlinson, P.B. and Posluszny, U., 1978. Aspects of floral morphology and development in the seagrass Syringodium filiforme (Cymodoceaceae). Bot. Gaz., 139: 333-345. Uhl, N.W., 1947. Studies in the floral anatomy and morphology of certain members of the Helobiae. Unpublished Ph.D. Thesis of Cornell University, Ithaca, New York, 137 pp.

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Wilder, G.J., 1974a. Symmetry and development of B,~tomus umbellatus (Butomaceae) and Limnocharisflava (Limnocharitaceae). Am. J. Bot., 61: 379-394. Wilder, G.J., 1974b. Symmetry and development ofLimnobium spongia (Hydrocharitaceae). Am. J. Bot., 6 l: 624-642. Wilder, G.J., 1974c. Symmetry and development of pistillate Vallisneria americana (Hydrocharitaceae). Am. J. Bot., 61: 846-866. Wilder, G.J., 1975. Phylogenetic trends in the Alismatidae (Monocotyledoneae). Bot. Gaz., 136: 159-170.