Annals of Botany 91: 927-937, 2003
© 2003 Annals of Botany Company
Comparative Developmental Anatomy of the Root in Three Species of Cladopus (Podostemaceae)
1 Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Tokyo 113-0033, Japan
* For correspondence. Fax 81-3-5841-4047, E-mail ss27185{at}mail.ecc.u-tokyo.ac.jp
Received: 29 November 2002; Returned for revision: 24 January 2003; Accepted 24 February 2003
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Root meristem structure and root branching in three species of Cladopus were investigated from developmental and anatomical perspectives. Cladopus fukiensis has a compressed bell-shaped meristem at the apex of a compressed subcylindrical root, while C. javanicus and perhaps C. nymanii, with a ribbon-like root, have a half lozenge-shaped (
as seen from above) meristem composed of an apical meristem of cubic cells and a marginal meristem of rectangular cells. The dorsiventrality of the meristem results in root dorsiventrality, and a marginal meristem contributes to the broadening of the root. Comparisons of meristem structure and root morphology suggest that the ribbon-like root of, e.g. C. javanicus, evolved towards the foliose root of Hydrobryum, sister to the genus Cladopus, by loss of an indeterminate apical meristem. The lateral root of C. javanicus initiates within the meristem of a parent root. The dorsal dermal layer and inner cells of the lateral-root meristem appear endogenously under the dermal layer of the parent root, while the ventral layer is derived exogenously from a ventral dermal layer continuous with the parent-root meristem. This mosaic pattern of exogenous and endogenous root formation differs from the truly exogenous formation seen in Hydrobryum and Zeylanidium. The dorsiventral mosaic origin of the root meristem may account for root cap asymmetry.
Key words: Cladopus, evolution, meristem, morphology, root branching, root cap, Podostemaceae.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The Podostemaceae occur on rocks in waterfalls and rapids in the tropics and subtropics and have many adaptations to these extreme habitats. They grow submerged during the rainy season and are exposed to the air during the dry season. Shortly after emergence, their flowers open and fruits ripen. The roots typically creep on, and adhere to, the rock surfaces (floating in some species), and bear shoots and flowers on the dorsal or lateral surfaces. The shoots and flowers range in size and are minute in many species (e.g. in the genera Cladopus, Hydrobryum and Zeylanidium) but are considerably larger in species of Apinagia, Indotristicha, Mourera and Rhyncholacis. The Podostemaceae consist of approx. 270 species assigned to about 47 genera (Cook, 1996). Recent molecular phylogenetic analyses have suggested that this family is a close relative of Clusiaceae in the Malpighiales (Savolainen et al., 2000; Soltis et al., 2000; Gustafsson et al., 2002).
The roots of Podostemaceae deviate markedly from the radially symmetric cylindrical roots of most angiosperms. They are dorsiventral and their morphology ranges from compressed (flattened) subcylindrical to ribbon-like to foliose. It has been suggested that foliose roots evolved independently from subcylindrical or ribbon-like ones in some lineages, e.g. Hydrobryum and Zeylanidium olivaceum (Kita and Kato, 2001; Suzuki et al., 2002). The roots contain chloroplasts, and foliose roots are multifunctional as the main photosynthetic, adhering and shoot- and flower-producing organs in many species.
Podostemaceae have two patterns of root branching, endogenous and exogenous (Willis, 1902; Rutishauser, 1997; Kita and Kato, 2001). In vascular plants (except the microphyllous Lycopsida) lateral roots are generally formed endogenously from the pericycle or endodermis of a parent root (Esau, 1965; Steeves and Sussex, 1989; Fahn, 1990; Kato and Imaichi, 1997). The lateral roots of subfamilies Tristichoideae and Weddellinoideae, and American members of subfamily Podostemoideae, show an endogenous pattern, whereas the roots of most Asian–Australian Podostemoideae (except Farmeria) arise exogenously near to, or at, the apex of a parent root (Willis, 1902; Rutishauser, 1997; Imaichi et al., 1999; Ota et al., 2001; Hiyama et al., 2002). Kita and Kato (2001) suggested that the exogenous root branching pattern arose at the base of the Asian–Australian clade of Podostemoideae.
Cladopus is a genus of Asian–Australian Podostemoideae consisting of about 12 species with subcylindrical to narrow or broad, ribbon-like roots (Cusset, 1992; Kato and Hambali, 2001; Rutishauser and Pfeifer, 2002). Molecular-phylogenetically, it is sister to the Hanseniella–Hydrobryum clade, which has exclusively foliose roots (Kita and Kato, 2001; Y. Kita, unpubl. res.). The morphology of a root is determined by its meristem activity. Ota et al. (2001) described the behaviour of the meristem throughout the course of development of the foliose root of Hydrobryum japonicum, but no equivalent study has been performed for Cladopus. The roots of C. nymanii and Japanese Cladopus species branch exogenously (Rutishauser, 1997), but the development of these branching patterns has not yet been addressed in the context of the appearance of new meristems of lateral roots. This study describes the developmental anatomy of the roots of three species of Cladopus: C. fukiensis (H.-C. Chao) H.-C. Chao, C. javanicus M. Kato & Hambali and C. nymanii H. Möller, focusing on root meristems and branching. The species were chosen because they are closely related (Kita and Kato, 2001; Y. Kita, unpubl. res.) and their roots are of various types, i.e. compressed subcylindrical; slightly or broadly ribbon-like. Based on the observations presented here, the pattern of evolution of foliose roots from subcylindrical or ribbon-like ones is shown.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Materials used in this study were collected from fields in China and Indonesia (Table 1). Vouchers are deposited in the University of Tokyo Herbarium (TI).
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Whole plants were fixed in FAA (formalin : acetic acid : 50 % ethyl alcohol, 5 : 5 : 90, v/v/v). For anatomical observations, root pieces were dehydrated in an ethyl alcohol series, embedded in Historesin (glycol methacrylate; Leica, Heidelberg, Germany), cut into 2-µm thick sections, and stained in a solution of safranin, toluidine blue and Orange G (Jernstedt et al., 1992). For scanning electron microscopy (SEM), the materials were dehydrated in an ethyl alcohol and t-butyl alcohol series, freeze-dried, and coated with platinum–palladium. Observations were made using a JEOL JSM-820S microscope at 5 kV.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Cladopus fukiensis
The root of C. fukiensis is subcylindrical with the dorsal surface convex and the ventral surface flat, about 0·6 mm (0·5–0·8 mm) wide and about 0·3 mm thick (Fig. 1A and E). The root meristem is covered by a markedly asymmetrical root cap with the dorsal part greatly elongated and the ventral part not developed (Fig. 1B and C). The meristem consists of an interrupted dermal layer and (densely stained) small inner cells (Fig. 1C and D). The ventral dermal cells of the meristem continue to the outermost layer of the root cap, while the dorsal dermal layer is covered by the root cap (Fig. 1C). The root cap separates from the dorsal dermal cells of the root meristem owing to the breaking of ventral (innermost) cells of the root cap, which are thin and often detached (Fig. 1C and E). The small inner cells of the meristem divide in various planes to yield rectangular or polygonal cells. Longitudinal and paradermal sections show that, conforming to the morphology of the root apex, the meristem is a compressed bell shape. The meristem’s proximal inner cells become parenchyma ground cells and also a strand of elongate non-tracheary cells, both of which are arranged longitudinally, and differentiate earlier than the dermal meristem (Fig. 1C and D). The boundary between the meristem and the differentiating tissues is not sharp, but the meristem is roughly 500 µm in length. A marginal meristem (see description of C. javanicus) is not obviously visible.
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Lateral roots are arranged alternately along the length of a parent root, accompanied by shoots between the main root and lateral branches (Fig. 1A and D). Because the lateral root develops very slowly in the early stages, the exact site of root initiation in relation to the parent root meristem could not be determined. The lateral-root primordium appears at the proximal side of a shoot near the root apex, perhaps in the proximal part of the main root meristem (Fig. 1D). The primordium is composed of dermal and small inner cells, which stain strongly in comparison with those on the opposite lateral side where a lateral root is not formed (Fig. 2D). The dorsal dermal cells are less densely stained than the ventral cells, as seen in the main roots (compare Fig. 2D with Fig. 1C and E). Both dorsal and ventral epidermises (rhizodermises) of the lateral-root primordium are continuous with those of the main root at this stage. Subsequently, as the lateral root grows (Fig. 2A), the dorsal epidermal and subdermal cells at the distal extreme become more lightly stained, i.e. non-meristematic (Fig. 2E). These cells are continuous with the epidermal and subdermal cells of the parent root, and are only slightly stretched (Fig. 2H, arrowhead) compared with those of C. nymanii and C. javanicus (see below). In contrast the dorsal epidermal cells proximal to the lightly stained cells divide anticlinally (Fig. 2E). As the lateral root elongates (Fig. 2B), cells just under the lightly stained dorsal layers undergo predominantly anticlinal divisions and become a new dorsal dermal layer of the lateral-root meristem (Fig. 2F). Later, as the lateral root elongates further (Fig. 2C), the lightly stained cells are enlarged and the ventral cells are broken so that they are separated from the dorsal epidermis of the lateral root (Fig. 2G; compare with Fig. 1C and E). A new lateral-root epidermis is visible beneath the fissures of the old dermal layer (Fig. 2C). Therefore, the new dorsal dermal meristem is developmentally discontinuous from the existing epidermis. Subsequently, the root cap is produced distally from the root meristem and becomes enlarged and thickened (Fig. 1B and C). In the course of development of a lateral root, the ventral dermal cells as well as the inner cells of the meristem are continuous with those of the parent root (Fig. 2D–G).
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The shoot arises endogenously near the lateral edge of the root, and the leaves emerge from a pocket between the parent and lateral roots (Figs 1A, D and 2B, H). A strand of non-tracheary cells, supplying the shoot, branches from the branching point of strands of the parent and lateral roots (Fig. 2H).
Cladopus nymanii
The root of C. nymanii is ribbon-like, about 2·0 mm (1·3–2·5 mm) wide and about 0·2 mm thick (Fig. 3A and D). The root cap is very similar to that of C. fukiensis (Fig. 3B–D). The root apical meristem is about 400 µm in length and dorsiventral with nearly the same histology as that of C. fukiensis (Fig. 3C); however, paradermal sections were not available. The cells of both lateral sides are meristematic, compared with those of a central part (Fig. 3D). A strand of elongate, non-tracheary cells exists through the parenchyma ground tissue (Fig. 3C and D).
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Root branching occurs in the same pattern as that of C. fukiensis (Fig. 3A). At an early stage of development, when a lateral-root primordium is visible as a bulge near the root apex (Fig. 4A), the distal extreme of the primordium tip is composed of lightly stained cells (Fig. 4E). At this stage, the dorsal epidermis is still continuous to the distal tip, and any future dorsal dermal layer of a meristem is not yet obvious. As is evident in Fig. 4E and F, where parts of the same cross-section of a main root are shown, the opposite part to the lateral region, where the lateral-root primordium is formed, is not meristematic (Fig. 4F). In a paradermal section of a root primordium at a similar stage, the lightly stained epidermal and subdermal cells are stretched horizontally, particularly at the distal tip and along the acroscopic side, as well as along the lateral side of the parent root (Fig. 4I). These stretched layers are later torn due to lateral-root growth (Fig. 4B and C, arrowheads). As the lateral root grows (Fig. 4B), inner cells under the lightly stained cells become a new dorsal dermal layer for the meristem (Fig. 4G). As the lateral root grows further (Fig. 4C), the ventral cells of the lightly stained layers facing the young dorsal epidermis of a root are torn and consequently the layer separates completely from the dorsal dermal layer of the meristem (Fig. 4H). Meanwhile the ventral dermal layer of the meristem continues to produce root cap cells distally, and ventral epidermal cells proximally. The root cap cells are produced from the established root primordium and push up the lightly stained, stretched cells (Fig. 4D).
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Shoots arise endogenously near the lateral edge of the root between the parent and lateral roots, accompanied by lateral-root developments (Figs 3A and 4C, I).
Cladopus javanicus
The root of C. javanicus is broad ribbon-like, about 3·0 mm (2·4–4·2 mm) wide and about 0·3 mm thick (Fig. 5A). It is roughly 5- and 1·5-times wider than the roots of C. fukiensis and C. nymanii, respectively, while nearly as thick. The root apex is covered by an asymmetrical root cap as in C. fukiensis and C. nymanii (Fig. 5B) but it is much reduced in size compared with those of the other species. The meristem consists a dermal layer and small inner cells which stain densely (Fig. 5B and C). The ventral dermal layer of the root apical meristem continues to the outermost layer of the root cap (Fig. 5B). The small inner cells divide in various planes, and those at the proximal end differentiate into parenchyma ground tissue and a strand of elongate, non-tracheary cells. The apical meristem is about 300 µm long, shorter than that of C. fukiensis (500 µm) and C. nymanii (400 µm) (Fig. 5B; compare with Figs 1C and 3C). In paradermal section, a band of densely staining small cells, 150–200 µm wide (obliquely or transversely related to the length of a root), is apparent along the root margin forming a meristematic tissue (Fig. 5C). Here, it is called a marginal meristem because of the histological similarity to that of Hydrobryum japonicum (Ota et al., 2001). In contrast to the apical meristem that consists of small, cubic cells dividing in various planes (Figs 5B and 6A), the marginal meristem consists of rectangular cells that divide, usually periclinally in paradermal section and anticlinally in cross-section, to produce only a parenchyma (Fig. 6B and E). The marginal meristem is naked and not covered by a root cap. Although the boundary of the two meristems is not clear, the marginal meristem is >2 mm long on either side of the root (Fig. 5C). More proximal to the marginal meristem, there is a marginal band of parenchyma cells, which are smaller than the inner cortical cells (Fig. 6C). These bands of epidermis and outer cortex are differentiated from the marginal meristem. In surface view, the dorsal epidermal cells of the root that are produced by the marginal meristem are arranged obliquely (Fig. 6D). A similar but less obvious cell arrangement is visible in the inner parenchyma cells near the root tip (Fig. 5C), compared with the longitudinal arrangement in C. fukiensis (Fig. 1D). Thus, the root meristem of C. javanicus is half-lozenge () shaped, consisting of an apical meristem in the middle and marginal meristems on both sides. The apical meristem becomes the marginal meristem at its periphery.
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Root branching occurs alternately along the length of a parent root and each branch is accompanied by a shoot between the lateral and parent roots (Fig. 5A). A lateral root primordium is formed near the root apex, and its meristem appears within the meristem of the parent root (Figs 5C and 7D). The meristem of an initiating lateral root consists of densely stained small cubic cells and is naked (Figs 6F and 7A). The dermal cells contain somewhat large vacuoles. Slightly older lateral roots developing on a parent root were not found in the material examined. However, the pattern of lateral branch development seems to be basically the same as the pattern seen in primary lateral roots. The epidermal and subdermal cells of the ‘parent’ root (= primary branch) at the site of lateral-root formation become stretched, stain only lightly and then become partially torn (Fig. 7B). A band of the lightly stained cells extends on the acroscopic side of the ‘lateral’ root (= secondary branch) toward the apical meristem of the ‘parent’ root (Fig. 7D). Young root cap cells, which are interior to, and smaller than, the stretching epidermal and subdermal cells, are produced from the root meristem (Fig. 7B). As the lateral root becomes enlarged, the meristem widens (Fig. 7C and D). In young lateral roots about 3 mm long or longer, the meristem, like that of the parent root, is band-like consisting of two kinds of meristem, i.e. an apical meristem and marginal meristem (Fig. 7D).
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The shoot arises endogenously near the lateral edge of the root and subsequently shifts toward the interior due to the activity of the marginal meristem producing parenchyma (Fig. 7B and D). A strand of non-tracheary cells to the shoot branches from that of the lateral root. At maturity the shoots appear on the dorsal surface of the root far from the root margin (Fig. 5A).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The root apical meristem of angiosperms is usually dome-shaped and produces derivative cells radially and basipetally, resulting in a cylindrical root (Steeves and Sussex, 1989). Distally, the leading edge of the meristem (root cap initials) forms a radially symmetrical, bowl-shaped root cap. Observations show that the apical meristem of C. fukiensis has a somewhat compressed bell shape and forms a subcylindrical root. A similar root meristem and, consequently, similar root morphology are seen in the subcylindrical roots of Malaccotristicha malayana, Weddellina squamulosa, Apinagia longifolia and Podo stemum ricciiforme (Imaichi et al., 1999; S. Koi, unpubl. res.; I. Tsukamoto, unpubl. res.). The root meristem of C. javanicus and perhaps C. nymanii has a dome-tipped (
) shape, consisting of two kinds of meristem, i.e. an apical meristem and a long, band-like marginal meristem, although the apical meristem changes into a marginal meristem at the periphery along the root margin. The structure of the meristems and cell alignment of the epidermis and cortex indicate that both apical and marginal meristems contribute to an elongation of the root, while the extensive activity of the marginal meristem results in a broad ribbon-like root. That cylindrical or subcylindrical roots are a plesiomorphic character state in most angiosperms, the basal clades of Podostemaceae and some species of Cladopus suggests that the evolution of ribbon-like roots from subcylindrical roots in Cladopus involved extensive development of the marginal meristem. All species of the Hanseniella–Hydrobryum clade have foliose roots, and the clade is sister to the Cladopus clade (Kita and Kato, 2001; Y. Kita, unpubl. res.), suggesting that the different root morphologies of the two clades diverged from a common ancestor. This study suggests that the root meristem of C. javanicus is morphologically and developmentally similar to that of Hydrobryum japonicum. The meristem of the lateral root of C. javanicus at the early stage of development is similar to the young, temporarily naked meristem of a new root (lobe) of H. japonicum in that the meristematic cells are cubic early in development (Ota et al., 2001). In C. javanicus, the developed root meristem consists of an apical meristem of cubic cells and a marginal meristem of rectangular cells, the former of which continues at the root apex and becomes the latter at the periphery. In H. japonicum, the uniform and determinate marginal meristem occupies most of the margin of a root (lobe), except the proximal margin (Ota et al., 2001). Daughter roots (lobes) are formed at a few random sites in the marginal meristem of a parent root (old lobe), the rest of which then differentiates into parenchyma. In C. javanicus, lateral roots arise within the marginal meristem of a parent root. One interpretation is that evolution of the foliose root of Hydrobryum from an ancestral ribbon-like root involved a change of meristem structure from a heterogeneous, indeterminate meristem to a homogeneous, determinate meristem. In particular, loss of an indeterminate apical meristem seems to be a major aspect of the change, because the uniform, determinate marginal meristem is already acquired by the ribbon-like root of Cladopus and also that of Zeylanidium lichenoides, a member of a sister clade of the Cladopus–Hydrobryum clade (Kita and Kato, 2001; Hiyama et al., 2002).
The pattern of formation of lateral-root meristems in the Cladopus species examined is extraordinary. In vascular plants two patterns of root branching are generally found, endogenous and exogenous. In the endogenous type, a lateral root is formed in the pericycle or endodermis of a parent root far from the root apex. An adventitious root initiates in subdermal cells in some species, e.g. Ceratopteris (Hou and Hill, 2002). So the epidermises of parent and lateral roots are discontinuous (Esau, 1965; Steeves and Sussex, 1989; Fahn, 1990). If root branching is exogenous, the apical meristem of a parent root divides into two daughter meristems and future root branches, and the epidermises of both roots are continuous (von Guttenberg, 1966; Imaichi and Kato, 1989). Observations revealed that C. fukiensis, C. nymanii and C. javanicus show a dorsiventral mosaic pattern of root meristem formation. In these species, the dorsal dermal meristem of a lateral root originates from an inner tissue under the dorsal epidermal and subdermal cells of a parent root, which are lightly stained and well differentiated. This pattern of development is more similar to the endogenous origin rather than exogenous origin scheme. It is noted that these lightly stained cells are not root cap cells of a young lateral root because they are continuous with the epidermal and subdermal cells of a parent root, as seen in paradermal section. Although the dorsal epidermises of a parent root and a lateral root appear to be continuous, they are developmentally discontinuous. In comparison, the ventral dermal meristem originates exogenously from that of a parent root, so that the ventral epidermises of a parent root and a lateral root are continuous. The results show that the pattern of lateral-root branching in the species examined is not typically exogenous, as described gross-morphologically (Rutishauser, 1997), but may be called exo/endogenous.
In paradermal section, the meristem of a lateral root appears within the marginal meristem of a parent root in C. javanicus. It is uncertain whether a lateral root is formed inside or outside the meristem of a parent root in C. fukiensis and C. nymanii, although the former pattern is more likely. In Zeylanidium subulatum and Z. lichenoides, the meristem of a parent root is divided into two daughter meristems (two future root branches) indicating exogenous formation (Hiyama et al., 2002).
Both endogenous and exogenous root origins occur in the Podostemaceae. The two patterns separate the basal clades of vascular plants. Endogenous origin occurs in megaphyllous plants, i.e. ferns, Equisetum, gymnosperms and angiosperms, whereas the exogenous origin occurs in the microphyllous group of Selaginellales, Lycopodiales and Isoetales (Kato and Imaichi, 1997). In Malaccotristicha malayana (Tristichoideae) and Podostemum ceratophyllum (Podostemoideae), lateral-root primordia form endogenously close to the vascular bundle of a parent root (Hammond, 1937; Imaichi et al., 1999). Some species of American Podostemoideae also show endogenous root origins (Warming, 1881, 1888). This endogenous formation is an ancestral pattern of root formation in most vascular plants with cylindrical roots, and it is found in Tristichoideae and those New World Podostemoideae which typically have subcylindrical roots (Willis, 1902; Hammond, 1937; Rutishauser, 1997; Imaichi et al., 1999). In comparison, lateral roots are exogenous in most species of Asian Podostemoideae with varied roots from subcylindrical to foliose (Willis, 1902; Rutishauser, 1997). Kita and Kato (2001) suggested that the exogenous formation of a lateral root evolved at the base of the Asian–Australian clade in the Podostemoideae. There is variation in exogenous root formation pattern, i.e. truly exogenous formation in H. japonicum (Ota et al., 2001), Z. lichenoides, Z. maheshwarii, Z. olivaceum and Z. subulatum (Hiyama et al., 2002), and exo/endogenous formation in C. fukiensis, C. javanicus and C. nymanii (present study). The evolution of root branching can be better understood by further comparative developmental anatomical studies of the root meristem. It is possible that the evolution of exogenous root formation involved a modification of a root meristem that allowed a root to branch at or near the apex. In relation to this, the ability of endogenous root formation was lost. Compared with most angiosperms in which there is generally no organ (root) formation in the root meristem, the meristem of a daughter (lateral) root appears within, or near the periphery of, a parent root meristem in the species of Cladopus examined and in Zeylanidium species (Hiyama et al., 2002). Shoots are also initiated in the root meristem. Further root meristem modification might have facilitated the evolution of ribbon-like and foliose roots with a marginal meristem in the Asian–Australian clade of Podostemoideae, as well as in African species of the subfamily.
Cladopus fukiensis, C. nymanii and C. javanicus have remarkably dorsiventral asymmetrical root caps. The root cap separates from the dorsal epidermis by breaking of the innermost cells. This is in contrast to most angiosperms (Esau, 1965; Steeves and Sussex, 1989) and also Weddellina squamulosa (Podostemaceae, Weddellinoideae) (S. Koi, unpubl. res.), in which the oldest outermost cells of a symmetrical root cap detach, while the innermost cells remain attached to the epidermis. A similar pattern is seen in Indotristicha ramosissima, Malaccotristicha malayana and Terniopsis sessilis (Tristichoideae) (Rutishauser and Huber, 1991; S. Koi, unpubl. res.). Such differences in morphology and development of a root cap are caused by the pattern of root cap formation. In most angiosperms and W. squamulosa, root cap cells are produced distally from the apical meristem and divide periclinally and/or anticlinally, and the outermost (distal) cells are older and slough off. In Cladopus and, possibly, other species of Podostemoideae with similar asymmetrical root caps, the outermost cells of a root cap are constantly produced from the ventral dermal meristem (but see Jäger-Zürn, 2002). There is no evidence available for the rest of a root cap, particularly the innermost (proximal) cells, but two patterns are possible. One is that the root cap, except for the outermost layer, is produced from the distal end of the dorsal dermal and inner meristems. The other is that it is intermittently derived and differentiated from the dorsal dermal meristem cells, and a new dorsal dermal meristem is formed under the previous one. In other species, a new ventral dermal meristem is formed over the previous one (S. Koi, unpubl. res.).
The root meristem and root cap are dorsiventrally symmetrical in the foliose roots of H. japonicum and Z. olivaceum (Willis, 1902; Jäger-Zürn, 2000; Ota et al., 2001; Hiyama et al., 2002). Both dorsal and ventral dermal meristems are parallel to each other and produce root cap cells distally, and dorsal and ventral epidermises proximally. Both dorsal and ventral dermal meristems are similar to the ventral dermal meristem of Cladopus examined and some other species (Goebel, 1932; S. Koi, unpubl. res.; I. Tsukamoto, unpubl. res.). Taking into account the derived phylogenetic positions of H. japonicum and Z. olivaceum (Kita and Kato, 2001), it is inferred that the dorsiventral symmetry of the root meristem and root cap is derived from the dorsiventral asymmetry, which is common to many Podostemoideae (Goebel, 1932; Rutishauser, 1997; Rutishauser et al., 1999; S. Koi, unpubl. res.; I. Tsukamoto, unpubl. res.). This change may involve a modification of the dorsal dermal root meristem.
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ACKNOWLEDGEMENTS |
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We thank G. G. Hambali and J.-Q. Liu who helped us collect materials, Y. Kita for helpful discussion, and G. Kenicer for improving the English expression. This study was in part supported by Grants-in-Aid for Scientific Research from the Japan Society for the Promotion of Science.
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