AOBPreview originally published online on April 27, 2007
Annals of Botany 2007 99(6):1121-1130; doi:10.1093/aob/mcm065
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INVITED REVIEW |
Developmental Morphology of the Shoot in Weddellina squamulosa and Implications for Shoot Evolution in the Podostemaceae
Department of Botany, National Science Museum, 4-1-1 Amakubo, Tsukuba, Ibaraki 305-0005, Japan
* For correspondence. E-mail skoi{at}kahaku.go.jp
Received: 25 November 2006 Returned for revision: 20 December 2006 Accepted: 16 February 2007 Published electronically: 27 April 2007
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Background and Aims: In angiosperms, the shoot apical meristem produces a shoot system composed of stems, leaves and axillary buds. Podostemoideae, one of three subfamilies of the river-weed family Podostemaceae, have a unique ‘shoot’ that lacks a shoot apical meristem and is composed only of leaves. Tristichoideae have been interpreted to have a shoot apical meristem, although its branching pattern is uncertain. The shoot developmental pattern in Weddellinoideae has not been investigated with a focus on the meristem. Weddellinoideae are in a phylogenetically key position to reveal the process of shoot evolution in Podostemaceae.
Methods: The shoot development of Weddellina squamulosa, the sole species of Weddellinoideae, was investigated using scanning electron microscopy and semi-thin serial sections.
Key Results: The shoot of W. squamulosa has a tunica–corpus-organized apical meristem. It is determinate and successively initiates a new branch extra-axillarily at the base of an immediately older branch, resulting in a sympodial, approximately plane branching pattern. Large scaly leaves initiate acropetally on the flanks of the apical meristem, as is usual in angiosperms, whereas small scaly leaves scattered on the stem initiate basipetally in association with the elongation of internodes.
Conclusions: Weddellinoideae, like Tristichoideae, have a shoot apical meristem, leading to the hypothesis that the meristem was lost in Podostemoideae. The patterns of leaf formation in Podostemoideae and shoot branching in Weddellinoideae are similar in that these organs arise at the bases of older organs. This similarity leads to another hypothesis that the ‘branch’ in Weddellinoideae (and possibly Tristichoideae) and the ‘leaf’ in Podostemoideae are comparable, and that the shoot apical meristem disappeared in the early evolution of Podostemaceae.
Key words: Anatomy, development, evolution, Podostemaceae, shoot, shoot apical meristem, Weddellina squamulosa
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Podostemaceae are a family of unusual aquatic angiosperms that live in rapids and waterfalls in the tropics and subtropics. The plants grow on submerged rock surfaces and are exposed to strong torrential stress during the rainy season. With the fall in the water level during the dry season, the plants emerge above the water to flower and fruit. Such extreme habitat conditions do not allow most vascular plants to survive, with the exception of Podostemaceae and Hydrostachyaceae (Van Steenis, 1981). The morphology of Podostemaceae is extremely deviated from that of terrestrial plants. Most species lack the radicle at the base of the hypocotyl and instead have an adventitious root on the lateral side (Mohan Ram and Sehgal, 1997; Suzuki et al., 2002). These roots are prostrate on and adhere to the rock surface and bear sterile and fertile shoots on the upper or lateral sides. The roots vary from subcylindrical to foliose.
The shoot is one of the most enigmatic organs in Podostemaceae. Angiosperms have a shoot apical meristem at the shoot tip to yield precursor cells that divide and differentiate into all shoot tissues and leaves (Steeves and Sussex, 1989). However, some species of subfamily Podostemoideae have no obvious shoot apical meristem (Hammond, 1936; Rutishauser, 1995, 2000; Rutishauser and Grubert, 1999). Based on close anatomical observations, Imaichi et al. (2005) and Koi et al. (2005) recently revealed that leaf formations occur in the absence of the shoot apical meristem in Cladopus queenslandicus and Zeylanidium subulatum, which belong to the Asian–Australian clade. In their shoots, the youngest and second-youngest leaves are so close to each other that there is no space between them. The dermal and subdermal cells on the adaxial side of the second-youngest leaf separate from the leaf tissue, followed by the initiation of a new leaf primordium below the cells. Some or perhaps all species of subfamily Podostemoideae lack a shoot apical meristem.
The evolutionary process of the loss of the shoot apical meristem in Podostemaceae is uncertain. Hypericaceae, which are suggested to be the sister group of Podostemaceae (Savolainen et al., 2000; Soltis et al., 2000; Gustafsson et al., 2002), have an ordinary shoot morphology. Subfamily Tristichoideae, which are basally diverged in Podostemaceae (Kita and Kato, 2001), have short shoots, called ramuli, with many photosynthetic scaly leaves consisting of a single cell layer except along the midrib (Imaichi et al., 1999). Some species of this subfamily are interpreted to have a shoot apical meristem at the tip of the ramulus, although there have been some interpretations for the branching pattern of ramuli (Jäger-Zürn, 1970, 1992; Rutishauser and Huber, 1991). However, it is uncertain whether the shoot apical meristem is present in Weddellina squamulosa, the sole species of the subfamily Weddellinoideae. The phylogenetic relationship of Weddellinoideae, i.e. sister to Podostemoideae (Kita and Kato, 2001), places Weddellinoideae in a key position to reveal the evolution of the Podostemaceae shoot.
Weddellina squamulosa has creeping subcylindrical roots with adventitious shoots on the lateral sides. The shoots appear dimorphic depending on the vegetative and reproductive phases. The reproductive shoot is unbranched (2–12 cm long) and bears 2–10 scaly leaves helically and a single terminal flower (Goebel, 1893). In contrast, the vegetative shoot is branched many times to grow up to 80 cm long and has a number of scaly leaves and tufts of filaments (Goebel, 1893; Wächter, 1897). The scaly leaves are dimorphic, either large or small. Developmental data for the shoots of W. squamulosa are too poor for comparison with those of Tristichoideae and Podostemoideae. The only interpretation available is that the shoot consists of a monopodial axis with lateral branches borne in the axil of subtending leaves, an organization similar to that of most angiosperms (Cusset and Cusset, 1988).
The aim of this study was to reveal the organogenesis of the shoot in Weddellina squamulosa and to compare shoot organogenesis patterns among the three subfamilies to speculate on the evolutionary process of the shoot in Podostemaceae.
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MATERIALS AND METHODS |
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Plants and fruits of Weddellina squamulosa were collected from Head Falls, Essequibo River, and from the Potaro River at Tumatumari and Konawaruk, Guyana. Voucher specimens are deposited in the University of Tokyo Herbarium (TI) and National Science Museum Herbarium (TNS).
For seedling culture, seeds collected from fruits were moistened and placed on Petri dishes. The seeds were left overnight to dry and adhere to the surface of the dishes, and were then cultured aquatically in appropriate volumes of 0·05 % (v/v) HYPONeX (Hyponex Japan, Tokyo, Japan) at 26 °C under 14 h light/10 h dark.
Whole plants, juvenile or mature, were fixed in FAA (formalin : acetic acid : 50 % ethyl alcohol, 5 : 5 : 90, v/v/v). For anatomical observations, shoot pieces were dehydrated in an ethyl alcohol series, embedded in Historesin Plus (glycol methacrylate; Leica, Heidelberg, Germany), cut into 2 µm thick sections using a glass knife on a microtome (LEICA RM 2155; Leica, Vienna, Austria), and stained in a solution of safranin, toluidine blue and orange G (Jernstedt et al., 1992). Six and 12 replicates of seedlings and root-borne shoots were examined, respectively. For scanning electron microscope (SEM) observations, the fixed materials were dehydrated in an ethyl alcohol series, after which the ethyl alcohol was replaced by isoamyl acetate. The samples were dried using a critical point dryer (HCP-2, Hitachi, Tokyo, Japan) and coated with platinum–palladium using a sputter coater (Ion Sputter E-1030, Hitachi, Tokyo, Japan). Observations were made using a JSM-820S SEM (Jeol, Tokyo, Japan) at 5 kV. Four and five replicates of seedlings and root-borne shoots were examined, respectively.
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RESULTS |
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Root-borne shoot
The developing shoot of Weddellina squamulosa consists mainly of two orders of branches, primary and secondary. The primary branches are alternate in two opposite orthostichies, showing a sympodial appearance (Fig. 1A), and the secondary branches are arranged alternately in two orthostichies on the primary branch (Fig. 1B). The primary and the secondary branches are up to approx. 24 cm and approx. 15 cm long, respectively, in the materials examined. The secondary branches give rise to small tertiary branches, and all branches are arranged in approximately the same plane. The other organs on the shoot are digitate large and small scaly leaves containing silica bodies and tufts of terete filaments (Figs 1E, F, H and 2K, L), as described (Goebel, 1893; Wächter, 1897; Cusset and Cusset, 1988).
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The youngest primary branch (PB1) occurs near the base of the second-youngest primary branch (PB2) on the side facing the third-youngest primary branch (PB3; Fig. 1B–F). The youngest primary branch is completely covered by two large scaly leaves that are borne on the immediately older primary branch (Fig. 1C, asterisks). The youngest primary branch has large scaly leaves in four orthostichies and small-scaly-leaf primordia between the large ones (Fig. 1C, two of four orthostichies are behind the stem). During growth, the primary branch continues to form large scaly leaves and also small scaly leaves (Fig. 1D–F). Secondary branches arise near the bases of large scaly leaves (Fig. 1E, F, H). Numerous filaments are borne near the primary- and secondary-branch apices (Fig. 1G) and formed in tufts arranged in two orthostichies in approximately the same plane as the primary and secondary branches (Fig. 1H).
The apex of the primary branch is dome-shaped and exhibits a tunica–corpus organization with cells in the dermal layer dividing exclusively in anticlinal planes and inner cells dividing in randomly oriented planes (Fig. 2A, B, D, H). In cross-section, the apical meristem of the primary branch is terete (Fig. 2E). The secondary branches and large scaly leaves arise acropetally on the flanks of the apical meristem (Fig. 2B, D, H). The procambium differentiates acropetally in the centre of the branch. The young secondary branch consists of the frequently cell-dividing dermal layer and meristematic inner cells, and the large scaly leaves consist of the dermal layer and differentiated parenchymatous cells (Fig. 2B, D, H). The secondary branch is supplied by a procambium, whereas the large scaly leaf lacks a vascular strand (Fig. 2D, H). The basal secondary branches arise on the primary branch at the same level as the sandwiching large scaly leaves lateral to them (Fig. 2F). At the early stage of development, the large scaly leaves, like the secondary branches, are longitudinally close to each other, with scarcely visible internodes (Fig. 2D, H). The epidermal cells in the internode are smaller and younger than those of the large scaly leaves above and below (Fig. 2H). The internodes elongate by cell divisions and subsequent tissue expansion, and then the inner cells differentiate to parenchyma; consequently, the stem elongates (Fig. 2K, L). There is no small-scaly-leaf primordium between the large scaly leaves before internode elongation (Fig. 2H). Small scaly leaves form basipetally in the elongating internode (Fig. 2K, L). The differentiated large and small scaly leaves have silica bodies in the abaxial epidermal cells (Fig. 2K, L). The apical meristem in the further developing primary branch becomes reduced, forms filaments on the flanks, and finally differentiates into epidermis and ground parenchyma tissue (Fig. 2J).
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The primary-branch primordium of a low dome (PB1) initiates at the base of the next youngest primary branch (PB2) on the side facing the adjacent primary branch (PB3; called the adaxial side here; Fig. 2A). Slight bulges of lateral organ primordia (secondary branch and scaly leaf) soon become visible above PB1 (Fig. 2B, C). PB1 is very close to the surface of PB3, with no space between them. While PB2 grows and forms secondary branches and large scaly leaves, PB1 becomes an increasingly tall dome without forming any organs (Fig. 2D, I). Two large scaly leaves occur on primary branch PB2 laterally at the base of PB1 in developmental and positional manners similar to the upper ones on PB2 at the bases of its secondary branches (compare F and G in Fig. 2). Although the initiation of primary branch PB1 precedes the formation of secondary branches, the PB1 and two associated large scaly leaves develop more slowly than the secondary branches and the more distal large scaly leaves (Fig. 2D, F–I). No leaves subtending PB1 and borne on its abaxial side are formed. As the primary branch develops further, cell divisions in the dermal layer and cell growth in the inner tissue occur, and additional small scaly leaves arise in the proximal part of the primary branch (PB2 in Fig. 2A, B, D, H). This morphogenesis and the stem elongation of the immediately older primary branch contribute to the separation of the primary branch from the adjacent second-older primary branch (e.g. PB2 and PB4 in Fig. 1B).
Seedling
The primary shoot (plumule) appears between the cotyledons, although its earliest development was not observed (Fig. 3A). This primary shoot is small and simple compared with the later-formed primary branches (compare A and B in Fig. 3). The shoot develops, forming lateral organs and branches. The primary branches on the primary shoot are arranged alternately in nearly two opposite orthostichies in a pattern similar to that of the root-borne shoot (compare Figs 3B and 1A). These primary branches are simpler than those of the root-borne shoots and bear fewer secondary branches, fewer large scaly leaves, and fewer tufts of filaments (compare Figs 3D, G and 1B, F). The secondary branches are accompanied by two scaly leaves laterally at their bases and arranged alternately in two orthostichies (Fig. 3D). In the upper part of the primary branch, tufts of filaments are borne between the two scaly leaves in place of the secondary branches (Fig. 3D). Small scaly leaves form below the basal secondary branches and large scaly leaves (Fig. 3D, asterisks). Eventually, many filaments are borne at the tip of the stem (Fig. 3C). The youngest primary branch (PB1) appears between the second and third youngest ones (PB2 and PB3; Fig. 3D). The formation of large scaly leaves and secondary branches precedes the elongation of the primary branch (Fig. 3E, F). As the shoot develops, the internodes elongate (Fig. 3G).
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The processes of shoot development and branching in the seedling and the juvenile plant are the same as in the root-borne shoot, although the shoot and leaves are smaller. The primary branch on the primary shoot has an apical meristem with a tunica–corpus organization (Fig. 4A). A new primary-branch primordium (PB1) occurs in the basalmost region of the youngest primary branch (PB2) on the side facing the second youngest primary branch (PB3; Fig. 4B). A small bulge of the secondary branch is visible above the primary-branch primordium (PB1) on the developing PB2 (Fig. 4C), and subsequently secondary branches and large scaly leaves arise on the flanks of the apical meristem of the primary branch (Fig. 4D). These two organs are easily recognizable: the secondary branches are five or six cell layers thick, whereas the large scaly leaves have fewer cell layers. A provascular strand runs in the centre of the primary branch, whereas the scaly leaves are avascular (Fig. 4C–F). The secondary branch and the primary branch are accompanied by two large scaly leaves laterally at their bases (Fig. 4E, F).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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The results of our observations, like those of Grubert (1976), show that the plumule exists in Weddellina squamulosa seedlings and has the same morphogenetic pattern as the root-borne shoot. Four species of Tristichoideae (Dalzellia zeylanica, Indotristicha ramosissima, Terniopsis brevis and Tristicha trifaria) and most species of Podostemoideae also have plumules, although they are rudimentary in the latter, which perhaps grow in the same developmental pattern as the root-borne shoots (Mohan Ram and Sehgal, 1997; Suzuki et al., 2002; Kita and Kato, 2005; and references cited therein). Therefore, the plumule was persistent in the early evolution of Podostemaceae, may have become ephemeral, and eventually disappeared in some species of Podostemoideae (Suzuki et al., 2002; Kita and Kato, 2005).
In the present study it has been demonstrated that in Weddellina squamulosa the apical meristem exists in the shoot branch and forms large scaly leaves acropetally on the flanks. This morphogenetic pattern, along with the tunica–corpus histology of the apical meristem, corresponds with the pattern common in other angiosperms (Steeves and Sussex, 1989). However, there are some significant differences from the typical shoot apical meristem in the pattern of small-scaly-leaf development and that of branching, as discussed below.
The Weddellina squamulosa shoot has two kinds of leaves that are distinct in organogenesis. The large scaly leaves form acropetally: acropetal initiation is a primary characteristic of the shoot. In contrast, the small scaly leaves arise basipetally in the elongating internodes and are not formed directly from the apical meristem. The small scaly leaves may be interpreted as ectopic leaves or scaly-leaf-like emergences (spines), and the basipetal sequence of their formation may simply reflect the possible basipetal differentiation of the internode. Although such basipetal leaf inception is rare in vascular plants, this pattern is found in a few angiosperm species, e.g. Acacia verticillata in which additional leaves arise in the meristematic regions between and below leaves already present that arise acropetally from a shoot apical meristem (Rutishauser, 1999). Moreover, another explanation may be possible. In contrast to the shoot apical meristem, a determinate meristem sometimes exhibits organogenesis in a nonacropetal sequence (Steeves and Sussex, 1989). In the tomato unipinnate compound leaf, which has an apical meristem, lateral large leaflets initiate basipetally, but minor lateral leaflets initiate nonbasipetally between the large leaflets, and marginal lobes of the large leaflets develop acropetally (Coleman and Greyson, 1976; Dengler, 1984; Janssen et al., 1998). The small scaly leaves of W. squamulosa may be comparable to the leaflets of a compound leaf, and the acro- and basipetal leaf organogeneses may be products of the determinate growth of the primary branch.
The key finding of the present study is the extraordinary developmental mode of shoot branches in Weddellina squamulosa. Consistent with Wächter (1897), it was found that its shoot branching system is sympodial with extra-axillary branches, i.e. no leaves subtending the shoot branches. Instead of a single subtending leaf, pairs of large scaly leaves are formed on the lateral sides of the branch (and not on the abaxial side). Furthermore, the small scaly leaves initiate later than the primary and secondary branches and consequently occur below the branches, as well as between the large scaly leaves. Cusset and Cusset (1988) interpreted the W. squamulosa shoot as monopodial with lateral branches borne in the axils of subtending leaves and bearing single pairs of stipules. It is most likely that the small scaly leaf was misinterpreted as a subtending leaf.
In the shoots of the seedlings of Weddellina squamulosa, tufts of filaments occur between the large scaly leaves on the primary branch in positions equivalent to those of the secondary branches. This result coincides with the description by Wächter (1897) based on root-borne shoots, like the present observations, and supports his interpretation that the tuft of filaments (‘Kiemenbüschel’) is homologous to the secondary branch.
Species of subfamily Tristichoideae and Weddellina squamulosa of Weddellinoideae have the tunica–corpus-organized apical meristem in the ramulus and the shoot-branch, respectively. The leaves of Terniopsis malayana, like the large scaly leaves of W. squamulosa, initiate acropetally on the flanks of the apical meristem (Imaichi et al., 1999). The leaves of other species of Tristichoideae, e.g. Indotristicha ramosissima and Tristicha trifaria, may have a similar developmental pattern (Rutishauser and Huber, 1991; Rutishauser, 1995). The branching pattern of Tristichoideae shoots has been interpreted differently: one interpretation is that in I. ramosissima and T. trifaria the ramuli branch in a sympodial pattern (Jäger-Zürn, 1997), and another is that they branch monopodially in the two species (Rutishauser and Huber, 1991; Rutishauser, 1995). However, ramulus branching in I. ramosissima, T. malayana and T. trifaria occurs accompanied with no subtending leaf on the adaxial side (facing the second youngest ramulus) of the base of the youngest ramulus (R. Fujinami, Japan Women's University, Tokyo, Japan, unpubl. data; S. Koi, unpubl. data), as in W. squamulosa. These common developmental features suggest that the ramulus of Tristichoideae and the primary branch of W. squamulosa are comparable, although the organogeneses of the small scaly leaves and the secondary branches are unique to W. squamulosa.
There is a large gap in morphogenesis between Weddellinoideae and Podostemoideae. The shoot of Weddellina squamulosa has an apical meristem, whereas the shoots of the Podostemoideae examined lack the meristem and consist only of leaves, either compound or simple (Imaichi et al., 2005; Koi et al., 2005). Nevertheless, Weddellinoideae and Podostemoideae (and also Tristichoideae) share the organogenetic pattern in which new organs initiate at the base of older organs, irrespective of differences in the kinds of organs, i.e. shoots or leaves. Furthermore, the determinate nature of the shoot branches and leaves is shared. These common developmental features provide an interpretation that the ‘shoot branch’ of Weddellinoideae and the ‘leaf’ of Podostemoideae (and also ‘ramulus’ of Tristichoideae) may be comparable organs (see Hypothesis B, discussed below).
From the above comparisons in the development and organography of the shoot in Weddellina squamulosa, the leaf in Podostemoideae, and the ramulus in Tristichoideae, two hypotheses are proposed for the evolution of the Podostemaceae shoot (Fig. 5). These hypotheses differ in the time of the loss of the shoot apical meristem. In Hypothesis A, reduction of subtending leaves and apical dominance at the appearance of the family Podostemaceae resulted in the extra-axillary sympodial shoot-branches, which have remained in Weddellinoideae and Tristichoideae (Fig. 5A). It is noted that cryptic subtending leaves occur in the inflorescence of Arabidopsis thaliana. Although its flower primordia are not subtended by bracts, results of expression analyses of KNOX and AINTEGUMENT genes and the role of JAGGED gene indicate that the floral primordium is subtended by a ‘cryptic’ leaf (Long and Barton, 2000; Dinneny et al., 2004; Ohno et al., 2004). In subfamily Podostemoideae, the shoot lost its apical meristem and became much reduced. Concomitantly, the leaves acquired a competence to form leaves. Finally, endogenous development was added to this leaf-forming-leaf organogenesis in the evolution of Asian–Australian Podostemoideae (Fig. 5A; Imaichi et al., 2005; Koi et al., 2005).
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In Hypothesis B, the shoot apical meristem was lost in the early evolution of family Podostemaceae. The apical meristem of the primary branch in Weddellinoideae and that of the ramulus in Tristichoideae (as well as that of a foliose, leafy shoot in Dalzellia; R. Fujinami, unpubl. data) may be homologous with the leaf apical meristem of a compound leaf (Fig. 5B). As Podostemoideae specialized further, the leaf apical meristem and consequently leaf complexity were reduced, resulting in small simple leaves, particularly in Asian species. This hypothesized compound leaf is similar to the leaf of Marathrum rubrum, a species of American Podostemoideae, which has an apical meristem that forms primary leaflets acropetally in two orthostichies (Rutishauser, 1995). Compound leaves of some plants have an apical meristem that produces leaflet primordia acropetally (Gifford and Foster, 1989). The compound leaves of Chisocheton and Guarea (Meliaceae) grow apparently indeterminately due to the persistent activity of the leaf apical meristem, which has a tunica–corpus-like structure and forms leaflet primordia acropetally (Steingraeber and Fisher, 1986; Fisher and Rutishauser, 1990; Fukuda et al., 2003). The large scaly leaves associated with the primary and the secondary branches in Weddellina squamulosa could be interpreted as stipules and stipels (i.e. secondary stipules of leaflets on a compound leaf), respectively. In Hypothesis B, the whole shoot of W. squamulosa may be interpreted as a chain of leaves (= primary branches). This organization is an apparent analogy with a chain of phytomers in the typical shoot of angiosperms. However, the indistinctness of shoot and leaf in W. squamulosa, as noted by Goebel (1893), may allow a possibility that the incipient bulge of the primary branch is a shoot apical meristem, all or most of which is used up for production of the compound leaf (= primary branch). In this case, the shoot apical meristem was apparently lost. The present data give no evidence for the presence of such a rudimentary shoot apical meristem, although close examination is necessary to solve the question of the presence or absence of the shoot apical meristem.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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We thank H. Okada, R. Imaichi, Y. Kita and K. Suzuki for their help during collecting trips in Guyana. We also thank J. Murata and A. Iwamoto for their help and for allowing us to use a critical point dryer. This study was supported by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science.
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LITERATURE CITED |
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