Annals of Botany 89: 755-765, 2002
© 2002 Annals of Botany Company
Comparative Developmental Anatomy of Seedlings in Nine Species of Podostemaceae (Subfamily Podostemoideae)
0Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7–3-1 Hongo, Tokyo 113–0033, Japan
* For correspondence. Fax + 81 3 3818 5367, e-mail sorang{at}biol.s.u-tokyo.ac.jp
Received: 12 December 2001; Returned for revision: 30 January 2002; Accepted: 7 February 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The developmental anatomy is described for seedlings of nine Asian and Australian species of Podostemaceae, subfamily Podostemoideae. The hypocotyl is rudimentary (except in Zeylanidium olivaceum) and does not form a primary root in any of the species examined. An adventitious root forms endogenously in the hypocotyl of six species with ribbon-like or flattened subcylindrical roots, and in Z. olivaceum with foliose roots. In contrast, it forms exogenously in Hydrobryum griffithii and Synstylis micranthera with foliose roots. The juvenile root becomes flattened and dorsiventral, branches exogenously (in Polypleurum stylosum, P. wallichii and Z. lichenoides) and produces shoots endogenously (in P. stylosum, P. wallichii, S. micranthera and Z. lichenoides). The root meristem is simple, composed of surface and uniform inner cells, and is devoid of root cap initials in all species. The reduced meristem morphology of seedling roots may be primitive in the Asian–Australian Podostemoideae. A root cap or protective tissue did not form during the culture period, even in the seven species with capped adult roots, probably due to its delayed development. It was absent throughout ontogeny in the other two species. No obvious shoot apical meristem forms between the cotyledons. One to several leaves occupy the shoot apical area in species with endogenous adventitious roots, while no leaves are formed in species with exogenous roots. These differences suggest recurrent origins of foliose roots in the Asian clade. Similarities between the unique seedling morphology and mutant Arabidopsis phenotypes are discussed.
Key words: Adventitious root, developmental anatomy, evolution, hypocotyl, Podostemaceae, primary root (radicle), root cap, seedling, shoot apex.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The Podostemaceae are aquatic angiosperms that typically grow on rocks in cascades, waterfalls and rapids where there are great seasonal fluctuations in river water levels. The vegetative plants grow submerged during the rainy season, but are exposed to air during the dry season, flowering and setting fruit, dehydrating and eventually dying. They are morphologically adapted to this habitat. Their body plan deviates remarkably from the root–shoot system common in angiosperms (e.g. Rutishauser, 1995, 1997). However, the family is a member of the advanced rosid eudicots. Several families have been proposed as the putative sister family to Podostemaceae, but the matter is still under debate (Cronquist, 1981; Les et al., 1997; Ueda et al., 1997; Soltis et al., 1999, 2000; Savolainen et al., 2000).
The Podostemaceae consist of about 270 species assigned to about 47 genera, mostly monotypic or oligospecific (Cook, 1996), reflecting considerable discontinuous variation of morphological characters. The genera are usually classified into two subfamilies, Podostemoideae and Tristichoideae (van Royen, 1951), or two families Podostemaceae and Tristichaceae (Willis, 1915; Cusset and Cusset, 1988a; Cusset, 1992). A molecular phylogenetic study (Kita and Kato, 2001) supported Engler’s (1930) classification recognizing the two subfamilies along with a third subfamily Weddellinoideae (Jäger-Zürn, 1997; Rutishauser, 1997). Les et al. (1998) and Kita and Kato (2001) inferred similar and hence robust inter-generic relationships from different genes, rbcL and matK. Molecular data indicate that a group of American genera (e.g. Apinagia, Marathrum, Mourera, Oserya and Vanroyenella) is basal in the Podostemoideae clade, and that the American Podostemum, along with the Madagascan Endocaulos and Thelethylax, are sister to the rest of the subfamily consisting of all Asian and Australian genera, including those examined in this study (Kita and Kato, 2001).
The Asian–Australian Podostemoideae have two different root morphologies. Diplobryum minutale C. Cusset, Hanseniella heterophylla C. Cusset (the sole species of the genus), all of the species of Hydrobryum (approx. ten), Polypleurum filifolium (Ramamurthy & Joseph) Nagendran, Arekal & Subramanyam, Synstylis micranthera (van Royen) C. Cusset (the sole species of the genus), Willisia selaginoides (Bedd.) Warming ex Willis (the sole species of the genus), Zeylanidium maheshwarii Mathew & Satheesh and Z. olivaceum (Gardn.) Engler have foliose (i.e. liverwort or lichen-like) roots (Cusset, 1992; Cook, 1996; Schnell, 1998). Their roots cover rock surfaces, are chlorophyllous and have extremely short, leafy and floral shoots scattered on their dorsal surface; they play major roles in adherence, photosynthesis, organogenesis and reproduction. The other species of Diplobryum, Polypleurum and Zeylanidium, like many other genera, have variously flattened subcylindrical or ribbon-shaped roots. Kita and Kato (2001) analysed Asian–Australian Podostemoideae and found them to be monophyletic and divided into two clades. One clade consists of two subclades, the Hydrobryum–Synstylis subclade and the Cladopus–Torrenticola subclade, in which Torrenticola is nested within Cladopus, and the other is the Zeylanidium–Polypleurum clade (see Fig. 5). In the Zeylanidium–Polypleurum clade, Z. olivaceum forms a clade with Z. maheshwarii, which in turn is sister to Z. lichenoides (Kurz) Engler. This phylogeny indicated that the foliose roots of the Hydrobryum–Synstylis clade and Z. maheshwarii and Z. olivaceum were derived independently from the ribbon-like roots common in the Podostemaceae (Kita and Kato, 2001).
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The foliose roots, as well as the flattened subcylindrical or ribbon-like ones, are usually considered to be homologous with the roots of other angiosperms (e.g. Warming, 1881, 1882, 1888, 1891, 1899, 1901; Willis, 1902; Engler, 1930; Troll, 1941; Rutishauser and Huber, 1991; Jäger-Zürn, 1992, 2000a, b; Rutishauser, 1997; Imaichi et al., 1999; Rutishauser and Grubert, 1999; Rutishauser et al., 1999; Ota et al., 2001). Some workers (e.g. Cusset and Cusset, 1988a, b; Mohan Ram and Sehgal, 1992) doubted the homology of the Podostemaceae roots and the typical roots of other angiosperms. Mohan Ram and Sehgal (1997) stressed that it is premature to discuss the homology of the roots given the diverse origins of adventitious (secondary) roots in seedlings.
Studying seedling development could lead to a better understanding of the morphology and evolution of Podostemaceae roots. Seedling development has been studied in field-collected seedlings of several species, although seedlings were observed at limited stages of development (e.g. Warming, 1882; Willis, 1902; Philbrick, 1984; Jäger-Zürn, 1995, 2000a; Rutishauser, 1997; Rutishauser and Grubert, 1999). To overcome such limitations, germination experiments have been performed to obtain seedlings (e.g. Grubert, 1976; Philbrick and Novelo, 1994; Mohan Ram and Sehgal, 1997; Oropeza et al., 1998). Mohan Ram and colleagues (Mohan Ram and Sehgal, 1997, and references cited therein; Uniyal and Mohan Ram, 2001) cultured seeds of Indian species and grew them until they flowered. In gross-morphological studies, these authors observed that adventitious roots usually develop from hypocotyls and also sometimes from epicotyls, cotyledons and early foliage leaves. However, few anatomical data on Podostemaceae seedlings are available (Schnell and Cusset, 1963). This paper describes the developmental anatomy of cultured seedlings of three species with foliose roots and six related species with ribbon-like or flattened subcylindrical roots in the Asian and Australian Podostemoideae (Table 1). Based on data obtained, the evolution of foliose roots is discussed.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Fruits were collected from wild plants in the field (Table 1). Voucher specimens are deposited in the University of Tokyo Herbarium (TI).
For seedling culture, the methods of Mohan Ram and Sehgal (1997) were followed. Their methods were generally applicable with good results, particularly for seed germination and early development. Fruits were surface sterilized in 1·6 % sodium hypochlorite/0·1 % Triton X100 for 4 min. Seeds removed from the fruits were allowed to germinate on thermocole cubes floating in a liquid medium (pH 7·0) containing 1/40–1/5 strength MS salts (Murashige and Skoog, 1962) and 2 % sucrose at 26 °C in a 14/10 h light/dark regime. When adventitious roots had developed to a certain extent, seedlings were transferred to agar medium containing 1/20 strength MS salts and 1·5–3·0 % agar and were covered with liquid medium. Non-aseptic culture was also used for species when the above aseptic culture did not result in good seedling development. Seeds removed from untreated fruits were put in Petri dishes (9 cm in diameter) containing appropriate volumes of 0·01–0·1 % (v/v) HYPONeX (Hyponex Japan Ltd, Tokyo).
For anatomical observations, material was fixed with FAA (formalin : acetic acid : 50 % ethyl alcohol, 5 : 5 : 90 v/v), dehydrated in an ethanol series, embedded in Historesin (glycol methacrylate; Leica, Heidelberg, Germany), cut into 2-µm thick sections, and stained with a solution of safranin, toluidine blue and Orange G (Jernstedt et al., 1992).
To investigate the evolution of foliose roots, character-state mapping of four morphological traits onto a modified Kita and Kato’s (2001) matK phylogenetic tree of subfamily Podostemoideae was made using MacClade version 4 (Maddison and Maddison, 2000). The traits were the pattern of origin of lateral roots from parental roots in adult plants (endogenous vs. exogenous); the pattern of origin of adventitious roots from hypocotyls in seedlings (endogenous vs. exogenous); plumular leaves between cotyledons in seedlings (present vs. absent); and root morphology (ribbon-like or flattened cylindrical vs. foliose). The traits were treated as unpolarized characters. Data were not available for the two seedling traits in some Asian species and were thus coded as ‘unknown’ (missing). Mourera fluviatilis Aublet does not form an adventitious root in the hypocotyl (Rutishauser and Grubert, 1999; K. Suzuki, unpubl. res.) so the origin of lateral roots and root morphology were coded as ‘unknown’ (missing). American and African taxa, for which data for the two seedling traits were also not available, were excluded from analysis. The matK tree was calculated anew for Cladopus javanicus (DDBJ accession no. AB066175) and Polypleurum stylosum (AB066174), using the maximum parsimony method in the same tree search strategy as Kita and Kato’s (2001) analysis. In the three most parsimonious trees obtained, C. javanicus and P. stylosum were nested in clades Cladopus–Torrenticola and Polypleurum–Zeylanidium, respectively (results not shown). Topological differences among the trees did not affect each of the scenarios of character evolution, which are shown with a strict consensus tree of the three (see Fig. 5). Optimization conducted by ACCTRAN and DELTRAN yielded a single parsimonious reconstruction for each trait.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The seedlings of all species examined were similar. Shortly after germination they were small and consisted of two cotyledons and a hypocotyl (Fig. 1A). The cotyledons were filiform, and the hypocotyl was several cells long, as wide as it was long (sometimes narrower), and bore rhizoids at the tip (Figs 1A, 2A, E, F, 3A and 4A). The hypocotyl was composed of an epidermis and parenchymatous cortex (Figs 1B, 2E, F, 3B and 4A). Exceptionally, the hypocotyl in Zeylanidium olivaceum was long and had a non-vascular strand composed of elongated cells (Fig. 1I and J). A primary root or radicle was not formed at the tip of the hypocotyl in any species examined (Figs 1C, E, J, 2E, F, 3B, C and 4A, C).
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Serial sections showed that an obvious shoot apical meristem was not formed between the cotyledons in any species examined. Some illustrations (e.g. Figs 1H, I and 3B) show sections of very young leaf primordia that look like shoot apical meristems. In all species except Hydrobryum griffithii and Synstylis micranthera, one to several leaves occupied the area where a shoot apex is formed in other dicot angiosperms (Figs 1B, H, I, 2E, F and 3B). It is uncertain whether there is no shoot apical meristem at all or if a reduced meristem disappears during plumular leaf formation. In Z. olivaceum, a number of leaves formed later at the apex of the elongated thick hypocotyl. This result is in accordance with Willis (1902) and Jäger-Zürn (2000a). In Z. subulatum (synonym: Podostemum subulatum Gardn.), the leaves, like those of adults, had sheath-like bases covering younger leaves (Fig. 1H). In H. griffithii and S. micranthera, no shoot apical meristem and no leaf formed between the cotyledons, which were tightly appressed (Fig. 4A and B).
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An adventitious root was formed from the hypocotyl in all species examined, although a primary root or radicle is not formed at the tip of the hypocotyl. The term ‘adventitious’ follows Willis (1902), Esau (1977), Fahn (1990) and Bell (1991) who used it in a broad sense for roots (and stems) that arise in various extraordinary positions. It has sometimes been described as secondary (e.g. Rutishauser, 1997). In some seedlings of Cladopus javanicus and Z. lichenoides, a few roots were formed from a single hypocotyl (Fig. 3C). Initiation was endogenous in C. javanicus, Polypleurum stylosum, P. wallichii, Torrenticola queenslandica, Z. lichenoides, Z. olivaceum and Z. subulatum (Figs 1B, E, J, 2E, F, 3A and C). A similarly endogenous origin of an adventitious root in a hypocotyl was described in a plant erroneously identified by Mohan Ram and Sehgal (1997) as Dalzellia zeylanica (Gardn.) Wight, which may in fact be Z. lichenoides (Jäger-Zürn, 2000a, pers. comm.). The root primordium arose a few cells below the surface in cortical parenchyma on the lateral side of the hypocotyl. It arose in the upper (close to the cotyledons) to middle of the hypocotyl in C. javanicus, P. stylosum, P. wallichii, T. queenslandica and Z. lichenoides (Figs 1B, 2E, F, 3B and C), as described by Mohan Ram and Sehgal (1997) for C. hookerianus (Tul.) C. Cusset [syn.: Griffithella hookeriana (Tul.) Warm.] and P. stylosum. In Z. olivaceum, the root arose near the tip of the hypocotyl (Fig. 1J). In some seedlings of P. stylosum, the adventitious roots were formed at the position of a shoot apex between the cotyledons, as described by Mohan Ram and Sehgal (1997). Serial sections showed that the root primordia were hemispherical and nearly as thick as they were wide while they were embedded in the hypocotyl in all species with endogenous hypocotylary roots. In Z. olivaceum, it remains uncertain whether the root initiates before or after the non-vascular strand is differentiated in the hypocotyl. Subsequently, the root primordia enlarged and emerged by rupturing hypocotyl tissue. By contrast, in H. griffithii and S. micranthera, root initiation was exogenous, involving the epidermal and cortical tissues of the hypocotyl (Fig. 4A and C).
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Shortly after emergence or branching from the hypocotyls, the root primordia developed into spatulate roots, which then became ribbon-like (Fig. 2B–D) or flattened subcylindrical. However, later development could not be observed in the present culture conditions in Z. olivaceum, S. micranthera and H. griffithii with foliose roots, which may be considerably transformed from the juvenile roots. Therefore, no data were available in these species for the developmental transition of meristem from the juvenile to the mature foliose root, which probably has a marginal meristem along the root lobe, as does that of H. japonicum (Ota et al., 2001). In all species examined, the root meristem was simple and composed of surface and uniform inner cells (Figs 1D, G, K, 4A and C). The surface layer entirely covers the inner cells, and there is no root cap initial. No root cap or protective tissue was formed, so the root meristem was naked during the period in which plants were cultured, i.e. for about 3 months after germination in Zeylanidium lichenoides and less in the other species (Fig. 1D, F, G and K). Roots consisted of an epidermis (rhizodermis) with root hairs on the ventral surface, parenchymatous cortex without intercellular spaces and non-vascular strands of elongate cells (Fig. 1D, F, G and K). The epidermis was differentiated from the surface initial layer, the cortex from the inner cells, and the non-vascular tissue from the provascular tissue derived from the inner cells. The shoots or tufts of leaves occurred near the lateral margin of the juvenile roots (Fig. 2B–D). The shoots were initiated near the root apex and endogenously, a few cells below the surface, in P. stylosum, P. wallichii, S. micranthera and Z. lichenoides (Fig. 4B).
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The roots were usually branched in a similar manner to those in adult plants, and gross-morphological observations showed that the lateral roots arose exogenously from the parental adventitious root in P. stylosum, P. wallichii and Z. lichenoides (Fig. 2C and D). In Z. lichenoides, root branching was always accompanied by shoots located between the main and lateral roots, as in the adult root, but the shoots also occurred in the roots between successive branchings. In P. stylosum and P. wallichii, there was no regular association between shoots and root branching (Fig. 2C and D). Well-grown roots meandered and were often detached from the substrate (agar) in P. wallichii and Z. lichenoides.
Analysis of the character-state evolution of the four traits yielded a single most parsimonious reconstruction for each trait. The reconstruction indicates that transition from an endogenous to exogenous origin of lateral roots and root-lobes from parental ones in adult plants occurred at the base of the Asian–Australian clade (Fig. 5A). In the scenarios of the seedling traits, transition from an endogenous to exogenous origin of adventitious roots from hypocotyls and the loss of plumular leaf formation between cotyledons occurred at the base of the Hydrobryum–Synstylis subclade (Fig. 5B and C). Transformation from ribbon-like or flattened cylindrical to foliose roots occurred at the base of the Hydrobryum–Synstylis subclade and in a clade of Z. maheshwarii and Z. olivaceum in the Polypleurum–Zeylanidium subclade in the Asian–Australian Podo stemoideae (Fig. 5D).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The in vitro cultured seedlings described here are generally similar to those reported previously (Mohan Ram and Sehgal, 1997), and to seedlings grown naturally (Willis, 1902), in their fundamental organ morphology, indicating that data from seedling culture are useful to investigate the specialized morphology and evolution of Podostemaceae. However, there are differences between cultured and naturally grown seedlings, mainly in the extent of development of organs. The number of plumular leaves varies among seedlings and can also be influenced by the concentration of constituents in the culture medium (Mohan Ram and Sehgal, 1997). The roots of Poly pleurum wallichii and Zeylanidium lichenoides meandered and often became detached from the substrate (agar). This may be due in part to poorly developed adhesive root hairs, compared with the tightly adhering roots of naturally grown plants. In P. stylosum and Z. lichenoides, adventitious roots varied in their number per hypocotyl and in the organs from which they arose (Willis, 1902; Mohan Ram and Sehgal, 1997; this study).
In contrast to dicotyledonous angiosperms in general, a primary shoot apex (plumule) with an obvious meristem is not formed between the cotyledons, and no primary root (radicle) is formed at the tip of the hypocotyl in the nine species examined, as noted by Mohan Ram and Sehgal (1997) and others. The adventitious (secondary) root arises from the hypocotyl in all species examined including P. stylosum, Z. lichenoides and Z. subulatum (Willis, 1902; Mohan Ram and Sehgal, 1997). However, not all members of the family Podostemaceae have such a seedling morphology. Rutishauser (1997) noted that a seedling has a plumule and two cotyledons in all members of the Podostemaceae whose germination has been studied, but that the morphology of the plumule needs to be described in detail. Mohan Ram and Sehgal (1997) described seedlings of Indotristicha ramosissima (Wight) van Royen (subfamily Tristichoideae) as having both a shoot and roots, which are relatively short-lived. Gross-morphological observations showed that in some New World Podostemaceae, such as Apinagia, Mourera, Rhyncholacis and Weddellina, a vigorous shoot with a number of leaves develops from the plumule, whereas an adventitious root arises in seedlings of Apinagia and Weddellina but not in Mourera and Rhyncholacis (Grubert, 1976; Rutishauser and Grubert, 1999; K. Suzuki, unpubl. res.). A variety of body plans of the Podostemaceae should be investigated by comparative developmental anatomy of seedlings and adults.
Our results indicate that there are two types of initiation of an adventitious root from the hypocotyl in the three species studied with foliose roots, namely endogenous or exogenous, while roots are endogenous in the six species studied with ribbon-like or flattened subcylindrical roots (Table 2). Although the difference between endogenous and exogenous origins is obvious in the seedlings examined, both types of development have been described as occurring together, e.g. in Indotristicha ramosissima shoots (Rutishauser and Huber, 1991), Dalzellia zeylanica shoots (Jäger-Zürn, 1995), Zeylanidium olivaceum roots (Jäger-Zürn, 2000a) and Hydrobryum japonicum Imamura roots (Ota et al., 2001). In the latter three species, and also perhaps in the first, new shoots or root lobes arise exogenously from unwounded parental shoots or roots, while regenerated ones arise endogenously. Regeneration is known in many taxa of Podostemaceae which are often subject to injury while submerged in swift-running water (Warming, 1881; Willis, 1902; Hammond, 1936; Imaichi et al., 1999; Ota et al., 2001). Endogenous regeneration may result in the coexistence of different means of organ initiation.
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Shortly after emergence or branching from the hypocotyl, the juvenile adventitious roots enlarge, become flat and dorsiventral, and form adventitious (secondary) shoots or tufts of leaves endogenously on both lateral sides, as described by Willis (1902) for several species, including some of the species examined in this study. Thus, the adventitious roots begin to express features of adult roots very early in development. Being composed of surface and uniform inner cells, and devoid of root-cap initials, the meristem is simple compared with the histologically well-organized root apical meristem of other angiosperms (Esau, 1977; Steeves and Sussex, 1989; Barlow, 1996). In Z. subulatum seedlings, the extreme root tip is formed by a collenchymatous layer beyond the initial meristem (inner cells in this paper), and the epidermis is continued by the collenchyma (Willis, 1902). However, the surface cells, considered to be identical to Willis’ (1902) collenchyma, are meristematic. It is noteworthy that such a seedling root meristem is fundamentally identical in all species examined, regardless of whether they have flattened subcylindrical, ribbon-like or foliose roots, or are assigned to different subclades of the Asian Podostemoideae. A similar meristem morphology occurs temporarily in adult roots of H. japonicum, which belongs to the Hydrobryum–Synstylis subclade (see Fig. 5). Ota et al. (2001) showed that in H. japonicum, the meristem is also simple and is composed only of surface cells and uniform inner cells in the early stage of root lobe development when it is temporarily capless. It may be that this perhaps reduced meristem morphology of seedling roots is widespread and primitive in the Asian–Australian Podostemoideae.
The roots of most Podostemaceae have dorsiventral root caps or protective tissues covering the meristem. In contrast, the roots are capless in a few Asian species (Podostemoideae) including Z. lichenoides (I. Tsukamoto, unpubl. res.) and Z. subulatum (Willis, 1902), as well as in Tristicha trifaria (Bory ex Willd.) Sprengel (Tristichoideae) (Rutishauser, 1997). Although Jäger-Zürn (2000b) described Z. subulatum as having a thin root cap, the capless root meristem was verified (Y. Hiyama, pers. comm.). Given that these species are not basal in Podostemoideae or Tristichoideae and are distantly related to each other (Kita and Kato, 2001), we suggest that phylogenetically the root cap disappeared in some of the Podostemaceae. Regardless of the presence or absence of a root cap in adult plants, the root cap was not formed in any species during the period in which the plants could be cultured, although other features of adult roots, e.g. root branching and formation of adventitious (secondary) shoots and root hairs, were expressed. This result does not indicate that culture conditions were inappropriate for root cap development because a cap was formed in Apinagia and Podostemum (Podostemoideae), Weddellina (Weddellinoideae) and Malaccotristicha (Tristichoideae) under the same conditions (K. Suzuki and Y. Kita, unpubl. res.). It is likely that the root cap or protective tissue arises in a later stage of development in the capped species examined of the Asian–Australian Podostemoideae. In comparison, the capless root meristem continues up to the adult stage in Z. lichenoides and Z. subulatum. The markedly delayed formation or absence of a root cap contrasts strongly with the situation in a true root, and raises the question of whether the root cap or protective tissue of Asian–Australian Podostemoideae is homologous with a true root cap.
Deviation from a true root cap is also seen in H. japonicum with foliose roots. Ota et al. (2001) described the developmental anatomy of its marginal meristem and root cap-like protective tissue. Initiation of daughter meristems at random sites in the parental marginal meristem, which later differentiates in the other parts, results in root lobing. The parental protective tissue is entirely sloughed off from the daughter meristem of a growing lobe, followed by the production of a new protective tissue from the meristem. Thus the meristem is temporarily capless. Further comparative studies of the ontogeny of the root cap in juvenile plants and its differentiation from the root meristem may provide useful data to understand better the homology of Podostemaceae root caps.
In adult plants of Z. lichenoides, Z. subulatum and some others (e.g. Cladopus), root branching is associated exclusively with shoots, which occur at every point of root branching (Willis, 1902; Mathew and Satheesh, 1997; Rutishauser, 1997; Jäger-Zürn, 2000b). In both Z. lichenoides and Z. subulatum, a mother meristem divides into two daughter meristems at the site of an initiating shoot and the daughter meristems become unequal in size, resulting in anisotomously dichotomous root branching (Y. Hiyama, pers. comm.). In juveniles of Z. lichenoides and Z. subulatum, such association does not always occur and some shoots occur between successive root branchings. This result suggests that shoots may not contribute to division of a root meristem, possibly because they arise near the lateral end of a smaller root meristem than in mature roots, or may be too small to influence meristem division. It is likely that the association is established during the course of development when the root meristem becomes enlarged.
The character-state evolution of the morphological traits, particularly the two seedling traits, was analysed for some members of the Podostemoideae, but many other taxa, including African members with foliose roots (Cook, 1996), remain to be analysed. Therefore, the character evolution hypothesis (Fig. 5) is still preliminary, although close phylogenetic relationships and morphological similarities indicate that it is perhaps also valid for Asian species with such data unavailable. We infer that an exogenous origin was derived from an endogenous origin for the adventitious roots of seedlings (Fig. 5B), as well as the lateral roots of adults (Fig. 5A; Kita and Kato, 2001). This is also supported by the fact that an endogenous origin of roots is common in vascular plants, irrespective of the type of organs from which roots arise. In angiosperms, the adventitious root usually arises from the pericycle of stems (Esau, 1977; Fahn, 1990; Bell, 1991) and even hypocotyls (Steffen, 1952; Celenza et al., 1995). This is also the case with ferns and horsetails, whose roots also originate from the endodermis (Fahn, 1990; Kato and Imaichi, 1997). Exceptionally, in an aquatic fern Ceratopteris, the adventitious root is initiated from a subdermal cell at the base of the leaf (Lachmann, 1907; Pal and Pal, 1962), in a manner very similar to exogenous origination. Our results indicate that the manner of exogenous initiation of lateral roots from parental roots in adults perhaps evolved at the basal node of the Asian–Australian clade of subfamily Podostemoideae, and then that of adventitious roots from hypocotyls in seedlings evolved at the base of the Hydrobryum–Synstylis subclade (Fig. 5A and B). The difference in the development of adventitious roots in seedlings supports the independent evolution of foliose roots in Z. olivaceum and the Hydrobryum–Synstylis subclade (Fig. 5B and D), as suggested by a phylogenetic analysis (Kita and Kato, 2001). This recurrent evolution hypothesis is consolidated by a correlation between the manner of root developmental and the presence or absence of leaves in the area of a shoot apex in seedlings (Table 2; Fig. 5B and C). It remains uncertain whether the foliose roots of the other Asian members, e.g. Diplobryum minutale and Hanseniella heterophylla, are derived independently of those studied or from those of common ancestor(s).
Despite being a member of the eudicots, the Podostemaceae evolved unique body plans that deviate remarkably from those common in angiosperms, and which are adapted to the aquatic habitat in swift-running water. Some species have roots with a number of adventitious shoots and may or may not have primary shoots, and others consist of shoots and lack primary roots (Willis, 1902; Engler, 1930; Troll, 1941; Cook, 1996; Rutishauser, 1997; Schnell, 1998). The body plans are established from the beginning of the life history and, in the Asian–Australian clade, embryos and seedlings lack a primary shoot and root. The seedlings show noteworthy similarities with arabidopsis mutants. First, in the Podostemaceae examined, no primary root develops from the hypocotyl, which is rudimentarily short and lacks a conducting strand connecting the area of a shoot apex and the hypocotyl tip. The absence of a primary root is compensated by an adventitious (secondary) root. A similar arabidopsis mutant is monopteros (mp), in which a provascular strand is not produced and a hypocotyl and primary root (radicle) are lacking; weak phenotypes of monopteros have short hypocotyls and adventitious roots (Berleth and Jürgens, 1993; Hardtke and Berleth, 1998). The MP gene is considered to have an early function in the establishment of vascular and body (apical–basal axis) patterns in embryonic and postembryonic development. It is likely that the gene governs auxin signalling (Hardtke and Berleth, 1998). Secondly, in the Podostemaceae examined, no obvious shoot apical meristem is formed between the cotyledons. No leaves arise in H. griffithii or S. micranthera, while in the other seven species small numbers of leaves are formed in the area where a shoot apex is formed in other angiosperms. Similar phenotypes are expressed by the shoot meristemless (stm) mutant of Arabidopsis (Barton and Poethig, 1993; Clark et al., 1996; Endrizzi et al., 1996). The STM gene, along with other genes, is considered to play a role in keeping the central meristem cells undifferentiated. Therefore, it is possible that mutations that result in the reduction or absence of embryonic organs (primary shoot and root) have been partly involved in the evolution of the unique Podostemaceae body plan.
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ACKNOWLEDGEMENTS |
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We thank H. Akiyama, D. Darnaedi, G. G. Hambali, R. Imaichi, P. Mathew, H. Okada, A. K. Pradeep, T. Santisuk, D. B. Sumithraarachchi, T. Wongprasert and S. -G. Wu for their assistance with material collection, and A. Kuwabara for her useful suggestion with regards culturing. We are indebted to reviewers for their useful suggestions. This study was supported in part by Grants-in-Aid for Scientific Research from the Japan Society for the Promotion of Science, the Foundation of River and Watershed Environmental Management, and the Nissei Life Insurance Foundation.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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