AOBPreview originally published online on April 18, 2005
Annals of Botany 2005 96(1):51-58; doi:10.1093/aob/mci148
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Leaf Development in the Absence of a Shoot Apical Meristem in Zeylanidium subulatum (Podostemaceae)
1 Department of Chemical and Biological Sciences, Faculty of Science, Japan Women's University, 8-1, Mejirodai 2-chome, Tokyo 112-8681, Japan and 2 Department of Biological Sciences, Graduate School of Science, University of Tokyo, 3-1, Hongo 7-chome, Tokyo 113-0033, Japan
* For correspondence. E-mail ryoko{at}fc.jwu.ac.jp
Received: 24 November 2004 Returned for revision: 12 January 2005 Accepted: 2 March 2005 Published electronically: 18 April 2005
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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• Background and Aims The Podostemaceae are a family of unusual aquatic angiosperms that live in rapids and waterfalls. To adapt to such extreme habitats, the family shows unusual morphologies. This study investigated the developmental anatomy of the shoot of Zeylanidium subulatum borne on the prostrate root attached to submerged rock surfaces.
• Methods Shoots of Z. subulatum were observed under the microscope using resin-sections.
• Key Results The shoot has no shoot apical meristem (SAM) and, without it, forms leaves distichously dorsiventrally facing the immediately older leaf. A new leaf forms on the adaxial side of a pre-existing leaf and also on the abaxial side of a leaf on flowering shoots. In both cases, the young leaf is endogenous below the older leaf and maintains histological continuity with it. Shortly after internal initiation, the leaf primordia become separate from each other due to cleavage between adjacent leaves of opposite ranks. The cleavage is caused by intercellular separation as well as by degeneration of vacuolated cells. Loss of the SAM is probably linked with the speculated shift of the site of leaf formation to the root.
• Conclusions The ‘shoot’ of Z. subulatum is characterized by the absence of a SAM, endogenous leaf formation in the absence of a SAM, cleavage between leaf primordia, and adventitious leaf formations. These innovations occur in some Podostemaceae that have become increasingly adapted to extreme aquatic habitats.
Key words: Adventitious leaf, developmental anatomy, dorsiventrality, endogenous leaf, Podostemaceae, shoot apical meristem (SAM), Zeylanidium subulatum
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Due to their peculiar ecology and morphological features, species in the Podostemaceae have long fascinated biologists (Arber, 1920
). Members of the family are unusual aquatic angiosperms growing on rocks in rapids and waterfalls in the world's tropics and subtropics. The plants grow submerged in fast-running streams during the rainy season and subsequently are exposed to air, where they flower, before drying during the dry season. The roots are prostrate and adhere tightly to the rock surface; the shoots endure violent whipping motions while submerged. Morphologically, the Podostemaceae are so unusual (moss-, alga- or lichen-like) and adapted to such extreme habitats that the family is described as a good example of a misfit (Bell, 1991), or to exhibit ‘fuzzy morphology’ (Rutishauser, 1995). Despite their peculiarities, recent molecular phylogenies suggest that the Podostemaceae are most closely related to the Clusiaceae (Hypericaceae), a family of the higher eudicot Malpighiales (Savolainen et al., 2000; Soltis et al., 2000; Gustafsson et al., 2002). The marked contrast between the morphology and phylogeny of the family suggests that conspicuous changes have occurred to allow the Podostemaceae to adapt to such harsh habitats.
The prostrate roots of members of the Podostemaceae bear adventitious shoots and reduced flowers. The shoot of the subfamily Podostemoideae is extraordinary (Rutishauser, 1997); an anatomical study revealed no shoot apical meristem (SAM) in Podostemum ceratophyllum (Hammond, 1936) and gross anatomical observations suggest its absence in some other species (Warming, 1888; Matthiesen, 1908; Rutishauser and Grubert, 1999, 2000). Other work has reported the presence of a SAM in other species (Jäger-Zürn, 1999, 2002a, b). Due to a lack of conclusive evidence, the presence or absence of the SAM in this subfamily is controversial, although Koi et al. (2005) described the absence of a SAM in Cladopus queenslandicus. The subfamily Tristichoideae has a SAM (Jäger-Zürn, 1970; Cusset and Cusset, 1988; Rutishauser and Huber, 1991; Imaichi et al., 1999, 2004). Therefore, it seems likely that loss of the SAM—if true—appeared during the evolution of the Podostemaceae.
Another peculiarity of the Podostemaceae is the correlated shoot branching pattern and leaf (sheath) morphology. Unlike the common angiosperm pattern where lateral shoot branches are borne in axils (i.e. on the adaxial side) of the leaf, in the Podostemaceae they occur on the abaxial side of double-sheathed (dithecous) leaves (Fig. 1; Jäger-Zürn, 1994, 1999; Rutishauser and Grubert, 1999; Rutishauser et al., 2003). Such shoot branching has been interpreted as heterotopy (Jäger-Zürn, 1999, 2002a), and by a ‘2-L module’ hypothesis for American species where a module consists of two leaves, one of which is terminal and the other is double-sheathed with a flower borne between them (Rutishauser and Grubert, 1999; Rutishauser et al., 1999).
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In the shoot of Z. subulatum, Jäger-Zürn (1999)
described a rudimentary SAM and a shoot-branch borne on the abaxial (wrong) side of a leaf associated with a flower. A lateral branch, usually comprising a flower and a single-sheathed (monothecous) leaf, is embraced by the abaxial sheath of a double-sheathed leaf, which is inserted below a terminal flower (Fig. 1). Although the organographic relationships of the shoots and flowers were examined (Jäger-Zürn, 1999), the development underlying the unusual branching remains uncertain. We investigated the developmental anatomy of the shoot of Z. subulatum with special attention to the presence or absence of the SAM and, if absent, the leaf development. |
MATERIALS AND METHODS |
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Shoots borne on the roots of Zeylanidium subulatum were collected in Mahaweli Ganga, Kandy District, Central Province, Sri Lanka. A voucher specimen is deposited in the University of Tokyo Herbarium (TI).
For anatomical observations, materials were fixed in FAA (formalin : acetic acid : 50 % ethanol = 5 : 5 : 90 v/v) in the field. The fixed material was dehydrated in an ethanol series, embedded in Historesin (glycol methacrylate; Leica, Heidelberg, Germany), cut into 2-µm thick sections, and stained with modified Sharman's staining solution (Jernstedt et al., 1992).
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RESULTS |
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Shoot development
Leafy shoots, 2–8 mm long, are borne adventitiously on the dorsal side of the compressed, long, creeping root (Fig. 2A). The leaves on the vegetative shoot are single-sheathed with an adaxial (ventral) sheath. The adaxial epidermal cells are much smaller than the abaxial cells (Fig. 2B). Although observations show that the shoot is unusual, we still refer to it as a ‘shoot’ hereafter and discuss its morphological nature below.
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The shoot or first leaf initiates endogenously within an area of the root apical meristem and a group of meristematic cells becomes obvious in association with division of the root meristem (see Hiyama et al., 2002
, fig. 2). The first leaf develops as the subsurface cells of the root become lightly stained due to large vacuoles and eventually separate from the leaf primordium to generate a void (Figs 2C, D; 3A). The second leaf initiates endogenously from densely stained meristematic cells adjacent to the first-leaf primordium and is most likely of root origin, as is the first leaf (Fig. 2D). No SAM is visible. The second leaf is acroscopic (relative to the root apex) to the first leaf, indicating that the adaxial surface of the first leaf faces the root apical meristem. Leaf development is accompanied by vacuolation of some cells in the future boundary between the first and second leaves, and, as the second leaf develops, the vacuolated, lightly stained cells increase in size (Fig. 3A, B). The future adaxial surface of the second leaf is histologically continuous with the first leaf, partly via vacuolated cells (Fig. 3A–E). The cells degenerate later when the third-leaf primordium has initiated. There is no space between leaves, but darkly stained degenerated cell residues are sandwiched in some places (Fig. 3D; these cells are seen commonly in different samples, e.g. Fig. 4K). The adaxial surface of the leaf faces the immediately older leaf. (The terms adaxial and abaxial are used conventionally, although there is no evidence of a shoot apex between the distichous leaves.)
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The SAM is never formed through shoot development. Instead, a region comprising small, densely stained cells similar to those of the leaf primordia occurs below the two youngest leaves and is retained in subsequent leaf formation (Fig. 3A, C, F, I). Such an internal meristematic region is absent at the base on the adaxial side of the leaf when a flower is present and no more leaves form (Fig. 4B).
Consequently, leaf production occurs in the absence of the SAM. Leaves form in opposite ranks of a roughly 
phyllotaxis (Figs 1; 2A, B). The third leaf initiates in the meristematic region below the base on the adaxial side of the second-leaf primordium (Fig. 3C). The second- and third-leaf primordia are continuous and demarcated by a line of cell walls (in section) between their future adaxial surfaces (Fig. 3C, E). Cell proliferation occurs at different rates in adjacent leaf primordia, and consequently the wall line elongates and curves. Divisions of cells adjacent to the line are predominantly perpendicular to the line. Comparison with an earlier stage (Fig. 3A) shows that the future surface of the third leaf appears in the region of the SAM in other angiosperms (except for internal location) and connects to the future surface of the second leaf above the third. Subsequently, the future adaxial surface of the second-leaf primordium is continuous to both the future abaxial and adaxial surfaces of the developing third-leaf primordium (Fig. 3F, G; see also Fig. 3C and I for other leaf primordia). As the leaf grows, the vacuolated cells stretch further along the wall line (Fig. 3H). The third-leaf primordium arises opposite and close to the procambium (middle) of the second leaf, which may be oblique to the first-leaf primordium (Fig. 3E, H). The fourth leaf forms below the third similarly to the third-leaf development, while the second and third leaves partly separate (Fig. 3I). Thus, since the leaves develop at different rates, cleavage occurs along the line of cell walls so that the leaves ultimately become entirely separate.
The sheath develops in close association with the leaf it embraces (Figs 2B; 3D). As the leaf grows and becomes terete, the older leaf embraces it by the increasingly curved sheath (Fig. 3B, D, E, H). These processes occur while the two adjacent leaves are still histologically continuous.
Leaf development of double-sheathed leaves
The double-sheathed leaf is associated with a flower on the adaxial side, i.e. at the site equivalent to that of leaf formation (Fig. 4A; see also Fig. 4G, J). The young flower primordium is recognized by its convex-truncate shape in longitudinal section (Fig. 4B). Flower development was not examined in detail. However, it would be useful to understand the developmental relationships of the flower and leaf—or organs of different orders. When the flower bud and the future double-sheathed leaf are very young, meristematic cells at the base on the abaxial side stain more densely than the surrounding tissue (Fig. 4B). Subsequently, cells just above the meristematic cells become vacuolated and an adventitious leaf primordium forms from the meristematic cells (Fig. 4C–F). The adventitious leaf becomes dorsiventral to the double-sheathed leaf from which it is formed (Fig. 4F, K). Even when the leaf primordium shows a conspicuous bulge, it is still histologically continuous with the double-sheathed leaf for a considerable length (Fig. 4F, I, K). Interfoliar continuation continues to the late stages of leaf development. The developing first adventitious leaf is barely connected to the double-sheathed leaf by cell-wall residues extending from a thickened cell wall of the double-sheathed leaf (Fig. 4F, arrowheads; for the thickened wall, see also Figs 3I and 4H). Comparison of cross- and longitudinal sections of the leaf primordia at equivalent stages of development shows that the abaxial sheath develops from the terete (abaxially round) base of the leaf in close association with development of its subtended leaf (compare Fig. 4I with Fig. 4B–F). The leaves separate from each other later by cell degeneration and intercellular separation.
The second adventitious leaf forms on the adaxial side of the first adventitious leaf and below it, in association with cell vacuolation (Fig. 4J, K). It develops while the first adventitious leaf is still continuous with, but partially separated from, the double-sheathed leaf (Fig. 4K). The older second leaf becomes dorsiventral to the first (Fig. 4A, ‘DL’ in square). A flower may form instead of the second leaf, resulting in a double-sheathed leaf and a flower borne on the older double-sheathed leaf (Fig. 4G).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Previous studies concerning the presence or absence of a SAM using different species in the subfamily Podostemoideae have been controversial (Warming, 1888
; Matthiesen, 1908; Hammond, 1936; Jäger-Zürn, 1999, 2002a, b; Rutishauser and Grubert, 1999, 2000; Rutishauser et al., 2003). Zeylanidium subulatum has been described as having a rudimentary SAM (Jäger-Zürn, 1999). However, this study demonstrated the absence (at least in the histological sense) of a SAM. Similarly, there is no SAM in Cladopus queenslandicus with long shoots (Koi et al., 2005). Some American Podostemoideae are thought to lack a SAM (Warming, 1888; Matthiesen, 1908; Hammond, 1936; Rutishauser and Grubert, 1999, 2000), but close observations are needed to verify its absence. By contrast, there is a SAM in the subfamily Tristichoideae (Jäger-Zürn, 1970; Cusset and Cusset, 1988; Rutishauser and Huber, 1991; Imaichi et al., 1999, 2004). Results of this study and other available data suggest that the absence of a SAM, and consequently the absence of a typical shoot, is an innovation of the subfamily Podostemoideae.
In the absence of a SAM in Z. subulatum, a leaf forms within an internal meristematic region below the youngest leaf primordium. Remarkably, a new leaf is endogenous and histologically continuous with the adjacent older leaf in early development. Subsequent cleavage by intercellular separation and cell vacuolation and degeneration separates the leaves (Fig. 5). A similar pattern of leaf formation occurs in Cladopus queenslandicus, although intercellular separation is less extensive (Koi et al., 2005). To our knowledge, this pattern of leaf development is unknown in any other plant group. The cell degeneration described here is a kind of programmed cell death (PCD), and its contribution to early leaf development is an organ-level example added to a wide spectrum of PCD involvement in plant development and morphogenesis (Gray, 2004; Noodén, 2004).
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The cleavage occurs between the youngest leaf primordia, i.e. at the position of the SAM in other angiosperms (except in internal locations). These features (absence of a SAM, and endogenous development and cleavage of leaves) may indicate that the leaves develop in an adventitious meristematic region within the root. Similar adventitious shoots arising from roots occur in a number of species, including ferns and angiosperms (Bell, 1991
). Shoots of Ophioglossum species and Platycerium bifurcatum are comparable to adventitious buds in the Podostemaceae roots only in that they are initiated in adventitious meristematic regions within the root apex (Peterson, 1970; Richards et al., 1983). Unlike in the Podostemoideae, their SAMs are formed before leaf initiation and hence the leaf primordia arise at the flank of the SAM. Therefore, the adventitious shoot with no SAM of the Podostemoideae is in remarkable contrast to ordinary adventitious bud formation with a SAM. This comparison raises the question as to whether the adventitious meristem in the Podostemaceae root includes an extremely modified and anatomically invisible SAM, or is a truly novel leaf- (and flower-) producing region.
In angiosperms in general, the shoot apical meristem is morphologically conspicuous and takes an obvious cytohistological, or tunica-corpus, zonation. The meristem is also described as comprising the central, peripheral and rib zones (Steeves and Sussex, 1989). Gene expression analyses show that the cytohistology and leaf organogenetic pattern are governed by particular genes that are expressed in the stem cell population and apical initials located in the central and adjacent zones (Fletcher, 2002). This correlation of meristem histology, gene expression and organogenesis (and also histogenesis) is not seen in Z. subulatum and Cladopus queenslandicus (Koi et al., 2005). In these, and perhaps some other species of Podostemoideae, leaf organogenesis occurs where the shoot apical meristem is histologically absent, although genetic regulation operates for leaf organogenesis.
In the Podostemaceae, the endogenous leaf formation associated with cell degeneration and cleavage is also found in Cladopus queenslandicus (Koi et al., 2005). Zeylanidium subulatum and C. queenslandicus share a unique characteristic, i.e. Y-shaped exogenous root branching accompanied by shoot formation in the forking point of the root (Rutishauser, 1997; Hiyama et al., 2002). Many other members of the Podostemoideae (e.g. Cladopus spp., Polypleurum spp.) also probably have such branching (S. Koi, unpubl. data). This is in marked contrast to the ordinary subapical root branching by endogenous lateral root formation. A recent paper on Hydrobryopsis sessilis with thalloid exogenously branching roots stressed that its root apex structure resembles the ordinary shoot apex in tunica-corpus organization, and hence the Podostemoideae have lost their classical morphological connotations like stem, leaf and root (Sehgal et al., 2002). However, the figure presented (fig. 9 in Sehgal et al., 2002) is too obscure to show convincingly that the root apex displays the tunica-corpus configuration typical of the ordinary angiosperm SAM. The Z. subulatum root apex has no tunica-corpus configuration (Hiyama et al., 2002). Nevertheless, it is noteworthy that two very peculiar characteristics—exogenous root branching similar to shoot branching and endogenous leaf development from other leaf bases—seem to be closely connected, although the underlying mechanism is unknown. Recent molecular developmental genetic analyses have shown that the RAM (root apical meristem) and SAM are controlled by similar genetic programs, reflecting duplication of developmental modules (Friedman et al., 2004). The fuzzy morphology of the root and shoot in the Podostemaceae merits molecular developmental analysis.
The adventitious leaf forms on the unusual abaxial (dorsal) side of the young double-sheathed leaf, under the influence of a developing flower borne regularly on the adaxial side of the leaf. This is a site where angiosperms in general have no SAM. Such a positional relationship was interpreted as heterotopy by Jäger-Zürn (1999). The leaf forms endogenously and in association with leaf cleavage, as does a leaf on the adaxial side of a leaf on the sterile shoot (Fig. 5). Adventitious leaf formation and the resulting extra-axillary branching compensate for loss of the SAM. Earlier reports of non-axillary branching of the shoot in some Podostemoideae (Jäger-Zürn, 1999; Rutishauser and Grubert, 1999; Rutishauser et al., 2003) need re-examination with special attention to whether the branching involves the non-axillary appearance of the SAM.
The new leaf is not dorsiventral to the shoot apex, which is absent, but to the youngest leaf primordium, which is opposite and meristematic. The first leaf is orientated toward the root apex, which has the only meristem when it forms. The leaf-to-leaf pattern of development seems to be causally linked with leaf dorsiventrality. A similar leaf organogenesis and dorsiventrality is seen in the Ophioglossaceae ferns. The leaf in Ophioglossaceae consists of a sporophore borne on the adaxial side of a trophophore, which is in turn dorsiventral to the shoot apex (Kato, 1990). The apical meristem of the initiating sporophore is dorsiventral to the trophophore (Imaichi and Nishida, 1986). Furthermore, in Z. subulatum, the leaf dorsiventrality is correlated with the apparently phyllotaxis (see Figs 1, 2A and 4G). It seems that in successive leaf formation, the positioning of a new leaf is influenced predominantly by the youngest (meristematic) leaf primordium in the absence of a SAM. Notably, phyllotaxis determination occurs while the incipient leaves are histologically continuous with the older leaves and not yet covered by the epidermis. In Arabidopsis, the epidermis controls auxin flux, which regulates phyllotaxis (Reinhardt and Kuhnemeier, 2002; Reinhardt et al., 2003).
In conclusion, the shoot of Z. subulatum (subfamily Podostemoideae) is characterized by endogenous leaf formation in the absence of a SAM, accompanied by cleavage between leaf primordia and adventitious leaf formation in an ectopic position. It is a remarkable deviation from the shoot of the Clusiaceae, the eudicot sister family to the Podostemaceae (Gustafsson et al., 2002), and is even more specialized than the shoot with exogenous leaf development of the subfamily Tristichoideae of the Podostemaceae (Jäger-Zürn, 1970; Cusset and Cusset, 1988; Rutishauser and Huber, 1991; Imaichi et al., 1999, 2004). In Malaccotristicha (Tristichoideae; Imaichi et al., 1999) the shoot has a small SAM from its inception when it develops within the root in a very similar manner to that of the Podostemoideae (Ota et al., 2001; Hiyama et al., 2002; present study). Based on the phylogeny (Savolainen et al., 2000; Soltis et al., 2000; Kita and Kato, 2001; Gustafsson et al., 2002), and if other members of the subfamily Podostemoideae really do lack a SAM, perhaps the SAM was lost during Podostemoideae evolution, with the site of leaf formation shifting concomitantly to the leaf base within the root, the boundary of which is absent. Such borderless and adventitious shoot development, subsequent to unusual early postembryonic development in the absence or reduction of the plumule and radicle (Mohan Ram and Sehgal, 1997; Suzuki et al., 2002; Imaichi et al., 2004), may have radically altered the Podostemaceae body plan during their adaptive evolution in extreme aquatic habitats. Leaf embedding forced by the histological integration of the shoot into the root would protect fragile juvenile leaves more effectively from damage by turbulent water than leaf formation at the shoot apex. This adaptive advantage may have contributed to diversification of the largest subfamily Podostemoideae, with some 260 of about 270 confamilial species compared with the small subfamily Tristichoideae with about ten species and the monospecific Weddellinoideae.
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ACKNOWLEDGEMENTS |
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We thank H. Akiyama, H. Okada and D. B. Sumithraarachchi for help with the fieldwork and S. Koi and D. E. Boufford for reading the manuscript. This study was supported in part by Grants-in-Aid for Scientific Study from the Japan Society for the Promotion of Science.
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