AOBPreview originally published online on October 24, 2002
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Annals of Botany 90: 735-744, 2002
© 2002 Annals of Botany Company
Developmental Anatomy and Branching of Roots of Four Zeylanidium Species (Podostemaceae), with Implications for Evolution of Foliose Roots
1 Department of Chemical and Biological Sciences, Faculty of Science, Japan Women’s University, 2-8-1 Mejirodai, Tokyo 112-8681, Japan and 2 Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Tokyo 113-0033, Japan
* For correspondence. Fax 03 5981 3658, e-mail ryoko{at}fc.jwu.ac.jp
Received: 25 June 2002; Returned for revision: 21 August 2002; Accepted: 16 September 2002 Published electronically: 24 October 2002
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Podostemaceae have markedly specialized and diverse roots that are adapted to extreme habitats, such as seasonally submerged or exposed rocks in waterfalls and rapids. This paper describes the developmental anatomy of roots of four species of Zeylanidium, with emphasis on the unusual association between root branching and root-borne adventitious shoots. In Z. subulatum and Z. lichenoides with subcylindrical or ribbon-like roots, the apical meristem distal (exterior) to a shoot that is initiated within the meristem area reduces and loses meristematic activity. This results in a splitting into two meristems that separate the parental root and lateral root (anisotomous dichotomy). In Z. olivaceum with lobed foliose roots, shoots are initiated in the innermost zone of the marginal meristem, and similar, but delayed, meristem reduction usually occurs, producing a parenchyma exterior to shoots located between root lobes. In some extreme cases, due to meristem recovery, root lobing does not occur, so the margin is entire. In Z. maheshwarii with foliose roots, shoots are initiated proximal to the marginal meristem and there is no shoot–root lobe association. Results suggest that during evolution from subcylindrical or ribbon-like roots to foliose roots, reduction of meristem exterior to a shoot was delayed and then arrested as a result of inward shifting of the sites of shoot initiation. The evolutionary reappearance of a protective tissue or root cap in Z. olivaceum and Z. maheshwarii in the Zeylanidium clade is implied, taking into account the reported molecular phylogeny and root-cap development in Hydrobryum.
Key words: Branching, developmental anatomy, exogenous vs. endogenous origin of root, meristem, Podostemaceae, root, root cap, shoot, Zeylanidium.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Members of Podostemaceae are aquatic angiosperms that grow on water-worn rocks in waterfalls and rapids which are subject to seasonal fluctuations in water level. The plants grow submerged during the rainy season and are usually exposed to the air during the dry season. They flower shortly after exposure to air and set fruits whilst drying. The family has evolved specialized morphologies that appear to have adaptive significance. Within the family, considerable discontinuous morphological variation is reflected by the current classification in which approx. 270 species are classified into about 47 genera, mostly monotypic or oligospecific (Cook, 1996).
The extensively modified plant body of the Podostemaceae is difficult to interpret using the ordinary root–shoot concept. A seedling of subfamily Podostemoi deae either has a rudimentary primary shoot (plumule) or lacks one, and may or may not have a relatively short-lived primary root (radicle) (Mohan Ram and Sehgal, 1997; Suzuki et al., 2002). The mature plant usually consists of an adventitious (secondary) root, which arises from various parts of the seedling with the exception of the hypocotyl tip, and root-borne adventitious shoots. The morphological nature of the diversely structured roots is controversial, and they have been variously termed a thallus, root–thallus or crust, as well as a root (Rutishauser and Huber, 1991). In Asian Podostemoideae species, roots are flattened subcylindrical, ribbon-shaped or foliose (thalloid) (Willis, 1902; Engler, 1930; Troll, 1943; Cusset, 1992; Cook, 1996; Schnell, 1998; Jäger-Zürn, 2000a; Uniyal and Mohan Ram, 2001). In Z. subulatum (Gardn.) C. Cusset and Z. lichenoides (Kurz) Engl., as in many other Podo stemoideae, the root is subcylindrical or ribbon-shaped, respectively, and alternately branched. Unusually, there is a shoot at every point of root branching (Warming, 1888; Willis, 1902; Mathew and Satheesh, 1997; Rutishauser, 1997; Jäger-Zürn, 2000a). The pattern is as regular as that commonly seen in shoots of most angiosperms where shoots occur in the axil of each subtending leaf. The shoot emerges on the dorsal surface of the root near the lateral edge between the main axis and lateral root. This association between root branching and shoots is also seen in Cladopus, a species of Polypleurum and Asian members of Podostemoideae, whereas there is no such association in other related species of Polypleurum (S. Koi et al., unpubl. res.).
The foliose root is chlorophyllous, with extremely reduced vegetative and reproductive adventitious shoots scattered on the dorsal surface, and root hairs (adhesive hairs) on the ventral surface. Such roots are seemingly multifunctional. A molecular phylogeny shows that Asian Podostemoideae are monophyletic and divided into two clades, one consisting of Zeylanidium and Polypleurum, and the other consisting of Cladopus, Torrenticola, Hydrobryum and Synstylis (Cook and Rutishauser, 2001; Kita and Kato, 2001). This suggests that the foliose roots of Z. olivaceum (Gardn.) Engl. and Z. maheshwarii C. J. Mathew & Satheesh, and of Hydrobryum and Synstylis are derived independently from subcylindrical or ribbon-like roots in the two clades. This proposed parallel evolution is also supported by the developmental morphology of seedlings (Suzuki et al., 2002). However, no attention has been paid to a possible association between root lobing and shoot formation in Z. olivaceum and Z. maheshwarii in which the shoots are scattered irregularly over the dorsal surface of the root (Willis, 1902; Mathew and Satheesh, 1997; Jäger-Zürn, 2000b), although they are phylogenetically close to Z. subulatum and Z. lichenoides.
This paper describes the developmental anatomy of roots of Z. subulatum and Z. lichenoides, and Z. olivaceum and Z. maheshwarii, with emphasis on the development of the root meristem, which is associated with shoot initiation, during the course of root branching. Anatomical data are compared for the four species to clarify the evolution from subcylindrical to foliose roots and the evolution of the developmental relationships of root branching or lobing with such a regular association with shoots.
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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 in Sri Lanka and India (Table 1). Vouchers are housed in the herbarium of the University of Tokyo (TI). For anatomical observation, materials were 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). For scanning electron microscopy (SEM), the material was dehydrated in an ethanol series, critical-point dried and coated with platinum–palladium. SEM observations were made using a Hitachi S-800 microscope (10 kV).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Zeylanidium subulatum and Z. lichenoides
The root in Z. subulatum is somewhat flattened with an oval shape in transverse section (approx. 0·8 mm wide and 0·5 mm thick), whereas that in Z. lichenoides is more flattened and wider, with a ribbon shape (0·8–1·5 mm wide, approx. 0·2 mm thick) (Fig. 1A–D). The root is branched alternately at intervals of 7–9 mm in Z. subulatum and 1–2 mm in Z. lichenoides (Fig. 1A and B). It consists of an epidermis and a parenchymatous ground tissue that is roughly seven to nine cells thick in Z. subulatum and five to seven cells thick in Z. lichenoides. The ground tissue is devoid of intercellular spaces and possesses only a rudimentary vascular bundle (Fig. 1C and D). In both species, the vascular bundle is single and consists of elongated cells. There are no apparent tracheary elements with helical thickenings except in the endogenously developed shoot. Adhesive root hairs are borne densely on the ventral surface, mostly along the vascular bundles (dark bands in Fig. 1A and B).
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The root has an apical meristem that is slightly flattened and consists of a single surface layer and small, densely stained inner cells (Fig. 1E and F). Surface cells are approx. 21 and 14 µm thick in Z. subulatum and Z. lichenoides, respectively, whereas the inner cells are approx. 14 and 10 µm thick, respectively. Surface cells are nucleated near the inner walls in both species (Fig. 1E and F). The surface cells undergo anticlinal divisions exclusively, so the surface layer does not rupture even at root branching but continues to the epidermis in the proximal portion (Fig. 1E–G). The root apex does not produce a root cap or any similar protective tissue.
Since the shoots occur between main and lateral roots at every branching point, root branching is always associated with shoot formation (Fig. 1A, B, G and H). The root apical meristem widens prior to branching (Fig. 2A and B). Within the further-widened root meristem a shoot primordium is formed accompanied by a group of vacuolated cells exterior (distal) to it (Fig. 2C). Consequently, the meristem splits into two. In a section of Fig. 2C, the heavily stained cells that constitute the smaller meristem are distinguishable from the adjacent, lightly stained cells, although the smaller meristem is less clear than the larger one. The larger daughter meristem will become the apical meristem of a future main root axis, whereas the smaller meristem becomes that of a future lateral root. As the shoot develops, the lightly stained vacuolated cells just above the shoot primordium die, and a void is formed (Fig 2D–F). As the growing shoot emerges, the root tissues covering the shoot expand and eventually rupture (Figs 1H and 2E, F).
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Since shoots occur alternately on either side of the root apex, the main root appears zigzagged with alternate lateral branches (Fig. 1A and B). In Z. subulatum, the lateral root develops more slowly than the main root, and is rarely branched. In Z. lichenoides, the young lateral root does not branch due to its very slow growth, but mature roots with floral shoots commonly have branched lateral roots.
Zeylanidium olivaceum
The roots of Z. olivaceum are foliose, lobed, and usually 5–8 mm wide and 0·3 mm thick (Fig. 3A–C). The shoots are scattered over the dorsal surface of the root with no obvious pattern (Fig. 3A). The youngest shoots occur near the root margin, whereas the larger and older shoots are further from the outer root margin (Figs 3A–C, 4A and 5A). Most shoots occur interior to shallow or deep incisions in the root margin (Fig. 3A and B), which, in many cases, are deeper in more developed roots, resulting in lobing. However, in some cases, there is no lobe incision exterior to the shoot, resulting in an entire root margin (Figs 3A, C and 5A).
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The root is composed of a dorsal and ventral epidermis between which are sandwiched about six parenchymatous layers without intercellular spaces, and an anastomosing provascular strand (Fig. 3D and E). The strand consists of elongated parenchymatous cells (Fig. 3E), except in old shoots, which are supplied by tracheary elements with helical thickenings. The unicellular root hairs are borne in patches on the ventral epidermis. Young shoots are supplied by one or two provascular strands from an anastomosing network of strands spreading in the root (Fig. 3A and C). By contrast, there is no provascular strand in the area exterior to very young shoots, although the area is not incised (Figs 3A and 5A).
There is a meristem along the margin of the foliose root covered by protective tissue (Fig. 3A and F). In this paper this meristem is referred to as a marginal meristem; its appearance is similar to that found in Hydrobryum japonicum (Ota et al., 2001). The marginal meristem is seven to eight cells wide (in the proximo-distal direction) and four to five cells thick (in the dorso-ventral direction) including the surface layers, and has a moderately layered structure. The protective tissue is composed of large, lightly stained cells that are five to eight cells wide and four to five cells thick. It is produced from the meristem as shown by cell alignment: the inner cells of the protective tissue are younger and smaller while the outer cells are older, larger and more stretched tangentially due to root growth (Fig. 3F). Pieces of protective tissues consisting of very old brown cells are often retained outside the outermost protective cells and are scattered along the margin (Fig. 3B). This suggests that formation of a protective tissue from the marginal meristem is quite discontinuous.
The shoot is initiated endogenously in the innermost zone of the meristem (Fig. 3G). As in Z. subulatum and Z. lichenoides, cells obliquely above a shoot primordium become enlarged, lightly stained, and eventually die to create a void (Fig. 4B and D). Growing shoots protrude from the root after rupturing the dorsal epidermis (Fig. 4F). As the root grows, the shoots shift to the interior from the root margin (Figs 3A–C and 4A). The marginal meristem area exterior to the shoots narrows (three to four cells wide in a proximo-distal direction), and the inner zone of the meristem begins to differentiate into parenchyma (Fig. 4B). In contrast, the neighbouring meristem area, which is not associated with shoots, remains wide (seven to eight cells; Fig. 4C). It seems probable that activity of the marginal meristem decreases under the influence of the initiating shoot. As the meristem gradually becomes less active, the derived root tissue exterior to a shoot becomes thinner, although it is only one cell layer thinner vertically than that in actively growing neighbouring parts (Fig. 4D and E). The epidermal and ground-tissue cells exterior to the shoot are stretched radially, possibly due to tension from the growing neighbouring parts (Fig. 4D and E). Finally, the meristem area exterior to the shoot differentiates into parenchyma, completing the splitting of the meristem (Fig. 4F). No marginal meristem or protective tissue remains although the parenchyma cells at the margin are slightly larger than the meristem cells (Fig. 4F).
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In a small number of cases the root margin remains entire (not incised), even exterior to a shoot (Fig. 5A). The exterior part is very elongated and retains the marginal meristem, although this is as thin and stretched as that in incised parts (Fig. 5A and B). This part also lacks a network of strands. There is also another extreme case: once reduced, the marginal meristem may return to a vigorous meristem, resulting in a markedly elongated area with the distal part being supplied by a provascular-strand network (Fig. 3C). Serial longitudinal sections of the elongated area show that the proximal portion is thin and consists of fewer cell layers and stretched cells, while the distal portion is thicker and consists of more layers and small cells (Fig. 5C and D). The distal portion is probably derived from a recovered marginal meristem, which is as vigorous as that in the neighbouring portion (Fig. 5D and E).
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Zeylanidium maheshwarii
The roots of Zeylanidium maheshwarii are foliose and irregularly lobed but the incisions are not associated with shoots (Fig. 6A). The roots examined here are stacked up and grow on other roots with shoots, resulting in irregular lobing. The young root lobe has a proximo-distally narrow marginal meristem and a very narrow layer of protective tissue composed of slightly tangentially elongate cells (Fig. 6B). As in Z. olivaceum, the mature lobe has a well-developed meristem and protective tissue (Fig. 6C and D). The shoot is initiated in young parenchyma just proximal to, and probably derived from, the root marginal meristem (Fig. 6E). As in Z. lichenoides, Z. olivaceum and Z. subulatum, root parenchyma cells distal to the shoot primordium are vacuolated, weakly stained, and eventually die, creating a void (Fig. 6E and F). The meristem distal to the shoot is as vigorous as that prior to shoot formation and in neighbouring parts. It continues to produce root tissues, so that the root is as thick as neighbouring parts (Fig. 6F and G). Consequently, the margin of the foliose root exterior to the shoots is entire (Fig. 6A).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The Podostemaceae show two patterns of root formation: endogenous and exogenous. Endogenous formation has been described in Indotristicha ramosissima, Malaccotristicha malayana, Tristicha trifaria (assigned to subfamily Tristichoideae), Apinagia multibranchiata, Farmeria (= Maferria) indica, F. metzgerioides and Podostemum ceratophyllum (Podostemoideae) (Warming, 1881; Willis, 1902; Hammond, 1937; Rutishauser and Huber, 1991; Rutishauser, 1997, 2000; Imaichi et al., 1999). Endogenous root formation is common in other angiosperms (Esau, 1977), and many other species probably exhibit this pattern of formation. In M. malayana and P. ceratophyllum, lateral root primordia arise far from the apical meristem and close to the vascular bundle of a main root (Hammond, 1937; Imaichi et al., 1999). This proximity to the vascular bundle is reminiscent of the proximity to the pericycle of a parental root commonly seen in angiosperms in general.
By contrast, exogenous root formation occurs in most Asian species of Podostemoideae with subcylindrical or ribbon-like roots, e.g. Zeylanidium subulatum, Polypleurum stylosum, P. wallichii, P. elongatum, Griffithella (= Cladopus) hookeriana and Cladopus nymanii s.l. (Willis, 1902; Rutishauser, 1997). We have provided developmental anatomical evidence that root branching is initiated exogenously in Z. lichenoides and Z. subulatum, and that root lobing in Z. olivaceum is equivalent to exogenous branching. The meristem of a root branch or lobe arises from that of a parental root or root lobe, so that the root branches apically or becomes lobed marginally. This result is not in accord with that of Jäger-Zürn (2000b) who noted that in Z. subulatum, ‘the lateral root does not arise at the root tip, but at a certain distance from it’. The evolutionary course from endogenous to exogenous root origin (Kita and Kato, 2001) is an interesting issue that requires a phylogeny-based comparative study of meristems.
Our observations show that the exogenous origin of root branches in Z. subulatum and Z. lichenoides is associated developmentally with shoot formation. Surprisingly, a similar association is often found in the foliose root of Z. olivaceum (noted below). The root apical meristem widens prior to branching and is split into two daughter meristems because the meristem exterior to a shoot, which is initiated within the root meristem, becomes parenchyma (Fig. 7A). Initiation of a shoot within a root meristem is highly unusual compared with the situation in other angiosperms in which new organs are initiated in the peripheral zone of, or at some distance from, the apical meristem of a shoot or root (Esau, 1977). In Z. subulatum and Z. lichenoides, the meristems for future main and lateral roots become dissimilar in size (Fig. 7A). This branching pattern can be described as anisotomous dichotomy (Gifford and Foster, 1989), and is very unusual in angiosperm roots. Such meristem behaviour may be seen in other Asian Podostemoideae with a regular association of root branching and shoots.
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The divisional pattern of the marginal meristem associated with shoots in Z. olivaceum and resulting in root lobing is almost identical to that in Z. subulatum and Z. lichenoides. However, shoots are initiated in the innermost zone of the meristem, in a more internal position than those in Z. subulatum and Z. lichenoides; the subsequently produced root tissues are exterior to the shoots between root lobes (Fig. 7B, left-hand side). Such a lobing pattern is sometimes absent when the once-reduced meristem is recovered (Fig. 7B, right-hand side). In Z. maheshwarii, roots are not lobed exterior to shoots, which are initiated in young parenchyma that is produced inwardly from the marginal meristem, and hence they do not have a significant effect on the meristem (Fig. 7C). Consequently, the meristem behaves differently in Z. olivaceum and Z. maheshwarii. Phylogenetic relationships strongly suggest that the foliose roots of Z. maheshwarii and Z. olivaceum evolved from subcylindrical or ribbon-like roots common in the other species of Zeylanidium (e.g. Z. subulatum, Z. lichenoides) and Polypleurum (Kita and Kato, 2001; Suzuki et al., 2002). To some extent the meristem is already flattened and widened in Z. lichenoides and Z. subulatum, suggesting extensive widening of a meristem (into a marginal meristem) and establishment of prolonged and uniform meristem activity over the course of root evolution from subcylindrical or ribbon-like roots to foliose roots. We speculate that the effect of shoot formation on root meristem splitting was reduced by shifting the shoot initiation site from the extreme apex (e.g. Z. subulatum, Z. lichenoides) to the innermost zone of the meristem (Z. olivaceum) and then to the parenchymatous area just proximal to the meristem (Z. maheshwarii) (Fig. 7).
The foliose root of Hydrobryum and Synstylis is derived from the flattened subcylindrical root found in a group including Cladopus and Torrenticola independently of the evolution of that of Zeylanidium (Kita and Kato, 2001). It is probable that the change of meristem development involved in evolution of the foliose root of Hydrobryum and Synstylis is different from that for Zeylanidium although the genera have similar marginal meristems. In H. japonicum, Ota et al. (2001) noted that the formation of a root lobe begins with daughter-meristem initiation at random sites in the reducing parental marginal meristem, while the parental meristem disappears later in the other areas. As a result, the meristem is split and the root is lobed. Thus, H. japonicum differs from Z. olivaceum and is perhaps similar to Z. maheshwarii in that root lobing is not apparently associated with initiating shoots.
The combination of the exogenous origin of roots and meristem widening (into a marginal meristem) seems to be related to the derivation of flattened and widened roots and, eventually, foliose roots from subcylindrical roots (Rutishauser, 1997). Kita and Kato (2001) implied that the evolution of exogenous roots from endogenous roots occurred at the base of the Asian Podostemoideae clade and that foliose roots evolved subsequently in some of Asian genera and species. By contrast, the root is subcylindrical (not foliose) in clades with endogenous roots, e.g. Tristichoideae, Weddellinoideae and American Podo stemoideae (Kita and Kato, 2001). To determine whether the foliose roots of African species (Engler, 1930; Taylor, 1953; Cusset, 1987) are exogenous will require developmental and anatomical studies.
As described by Willis (1902) and Rutishauser (1997), Z. subulatum and Z. lichenoides lack a root cap. In all the material at various stages of root development examined here, the surface layer at the root tip was part of the apical meristem that produces the epidermis and was never sloughed off. Our result is not in accord with that of Willis (1902) who described the surface layer as a collenchymatous layer in both species, nor is it in accord with that of Jäger-Zürn (2000b) who described an apparently unusual root cap in Z. subulatum. Seedlings and young plants of some species of Asian Podostemoideae, including Z. subulatum and Z. lichenoides, whether or not they have root caps, always lack root caps in the culture period (up to 3 months) (Suzuki et al., 2002). Thus root cap development is delayed or missing in such species.
The root meristem of young plants of some Asian Podostemoideae is relatively simple and is composed of a surface layer and inner cells, like those of adult roots of Z. subulatum and Z. lichenoides. In contrast, seedlings of some species of Tristichoideae and American Podostemoideae form root caps under the same culture conditions (K. Suzuki and Y. Kita, pers. comm.). In Hydrobryum japonicum, Ota et al. (2001) showed that a protective tissue covers the root margin and is sloughed off in the early stage of development of a new root lobe, resulting in a temporarily naked meristem; new protective tissue is produced subsequently from the daughter meristem. The naked meristem is very similar to that of Z. subulatum and Z. lichenoides. A similar protective tissue occurs in Z. olivaceum although it is persistent. In Z. maheshwarii, which is closely related to Z. olivaceum, the protective tissue is thin and probably continuous. Rutishauser (1997) proposed root cap reduction toward capless roots in the Podostemaceae as a whole. A molecular phylogeny (Kita and Kato, 2001) suggests that the marginal protective tissue or root cap may have reappeared in Z. olivaceum and Z. maheshwarii.
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ACKNOWLEDGEMENTS |
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We thank H. Okada, H. Akiyama, P. Mathew, A. K. Pradeep and D. B. Sumithraarachchi for their help during field trips. This study was supported, in part, by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science, and by the Takahashi Industrial and Economic Research Foundation.
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S. KOI and M. KATO Comparative Developmental Anatomy of the Root in Three Species of Cladopus (Podostemaceae) Ann. Bot., June 1, 2003; 91(7): 927 - 937. [Abstract] [Full Text] [PDF]
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