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Anatomy and Morphology |
2Department of Botany, National Science Museum, Amakubo, Tsukuba 305-0005, Japan; 3Department of Chemical and Biological Sciences, Faculty of Science, Japan Women's University, Mejirodai, Tokyo 112-8681, Japan
Received for publication July 3, 2005. Accepted for publication February 24, 2006.
ABSTRACT
In the unusual aquatic Podostemaceae, the root is the leading organ of the plant body and is variously compressed and submerged as it adheres to rock surfaces in rapid water. In an anatomical comparison of the root apical meristems and root caps of 33 species that represent the major lineages of the family, the dorsiventrality of root meristems varied and was classified into four patterns: (1) The root cap is produced outward from a nearly radially symmetrical meristem. (2) The meristem and root cap are markedly dorsiventral; the outermost cells of the hood-shaped cap are acroscopic derivatives from bifacial initials on the ventral side, while the pattern on the dorsal side is similar to pattern 1. (3) Bifacial initials are on both the dorsal and ventral sides. (4) No root cap is present. An evolutionary polarity may be evident from pattern 1 to 2 and then to 3. Pattern 2 arose in the early evolution of the subfamily Podostemoideae and subsequently, pattern 3 arose in species with crustose roots, while the least specialized pattern 1 is retained in Tristichoideae and Weddellinoideae. Pattern 4 characterized by caplessness may have appeared recurrently in Tristichoideae and Podostemoideae. These evolutionary changes in the meristem preceded the specialization of external root morphologies.
Key Words: dorsiventrality • evolution • Podostemaceae • root • root cap • root apical meristem
Podostemaceae are a family of ecologically and morphologically unusual aquatic angiosperms. They occur on rocks in rapids and waterfalls in the tropics and subtropics of the world. Vegetative plants grow submerged in swift-running water during the rainy season and subsequently emerge and eventually dry during the dry season when the water level drops. Generally flowers open and seeds are set shortly after emergence. Except for a few rootless species, the roots creep on and adhere to rock surfaces (in some species floating except the base) and are dorsiventral and variously flattened into shapes ranging from subcylindrical to ribbon-like or crustose (Fig. 1) (Willis, 1902
; Troll, 1941
; Rutishauser, 1997
). The roots bear adventitious shoots, both vegetative and reproductive, on the lateral flanks or dorsal side and root hairs (rhizoids) on the ventral surface. Thus, the root is the leading organ in the body plan of most Podostemaceae and is a remarkable adaptation to its unique environment, i.e., the border between hard rock surfaces and fast-running water. Molecular analyses place Podostemaceae in the eudicot rosid Malpighiales, particularly close to Clusiaceae (Hypericaceae) (Savolainen et al., 2000
; Soltis et al., 2000
; Gustafsson et al., 2002
). The results of these analyses suggest that such unique roots of Podostemaceae were derived from cylindrical, capped roots common in Clusiaceae and other angiosperms, and that the epilithic roots were derived from underground roots that penetrate soil.
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described that in three species of Cladopus with either narrow or broad ribbon-like roots covered by hood-shaped dorsiventral root caps, the outermost layer of the root cap is an acroscopic extension from the ventral dermal layer of the root meristem. The crustose roots of Hydrobryum japonicum and Zeylanidium olivaceum have a moderately layered structure of the meristem along the margin of the root lobe, which is framed by a root cap (protective tissue) (Ota et al., 2001
; Hiyama et al., 2002
). The root of Indotristicha ramosissima appears to have a meristem of the closed type, which is demarcated from the root cap (Rutishauser and Huber, 1991
). Thus, the results of previous studies differ considerably in the organization of the root meristem and cap. However, very little information is available to consider the evolution of the root in Podostemaceae. The goal of this study was to define the dorsiventrality of the root meristem and its derivative cap in the diverse Podostemaceae and infer the evolutionary scenario that led to their unique roots. MATERIALS AND METHODS
Plant materials
Plants examined are shown in Table 1. Species were selected to represent major clades of Podostemaceae (Kita and Kato, 2001
, 2004
; Kato, 2004
). They include species that may be in need of systematic and nomenclatural revision or have very recently been revised (see footnote a, Table 1). Vouchers are deposited in the Forest Herbarium, Department of National Parks, Wildlife and Plant Conservation, Bangkok (BKF), the University of Tokyo Herbarium (TI), and National Science Museum Herbarium (TNS).
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). We cut sagittal-, frontal-longitudinal, and cross sections (Fig. 2). For scanning electron microscopic (SEM) observations, fixed roots of Podostemum rutifolium var. ricciforme and Marathrum schiedeanum were dehydrated in an ethyl alcohol series, critical point dried, coated with platinum-palladium, and observed with a Hitachi S-800 microscope at 10 kV. Roots of Polypleurum stylosum and Vanroyenella plumosa were similarly prepared and observed with a KEYENCE VE-8800 SEM at 5 kV. Roots of Weddellina squamulosa and Terniopsis malayana were dehydrated in an ethyl alcohol and t-butyl alcohol series, freeze-dried, coated with platinum-palladium, and observed with a JEOL JSM-820S SEM at 5 kV.
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, 2004
), Kato et al. (2003)
, Kato (2004)
, and Y. Kita (University of Tokyo, unpublished data), using MacClade version 4 (Maddison and Maddison, 2005
). Trees with added taxa (Kato et al., 2003
; Kato, 2004
; Kita and Kato, 2004
; Y. Kita, unpublished results of Dalzellia gracilis, Diamantina lombardii, Jenmaniella ceratophylla, and Rhyncholacis palmettifolia var. palmettifolia) are in consistency with Kita and Kato's (2001)
tree of the whole Podostemaceae.
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The root apical meristem and the root cap varied structurally among the species of Podostemaceae examined. Root morphologies were classified into four histological patterns with two subpatterns, based on the presence or absence and the place of bifacial meristems and the presence or absence of the root cap (Table 1, Fig. 3).
Pattern 1
The roots of Indotristicha ramosissima, Terniopsis australis, T.malayana, T. sessilis, Weddellina squamulosa, and Vanroyenella plumosa are variously compressed, subcylindrical or narrow ribbon-like (Figs. 4–10). In W. squamulosa the distal part of the root is almost cylindrical (Fig. 4). The apical meristem is dome-shaped in sagittal and frontal-longitudinal sections (Figs. 5, 6). As seen in an open type of root meristem (Barlow, 2002
), the central portion of the meristem is not well delimited from the root cap, due to the absence of predominant periclinal cell walls, while the periphery is demarcated by cell walls formed by anticlinal divisions of the epidermal cells below the inner root cap. Vanroyenella plumosa has a similar pattern. In comparison, in Terniopsis malayana, T. australis, T. sessilis, and Indotristicha ramosissima, the distal part of the root is compressed and conical (Figs. 7–9). In relation to this, the apical meristem in the Terniopsis species is a somewhat compressed dome and is separated from the root cap by periclinal cell walls, except in the smaller central part of the root. Such cell walls on the dorsal side are close to or apparently connected with those on the ventral side in I. ramosissima (Fig. 10; Figs. 7, 8, 11 in Rutishauser and Huber, 1991
). The meristem of all the species is located in or below the center of the root apex and supplied by the procambial strand running in or below the center.
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Pattern 2A
The roots of Diamantina lombardii, Endocaulos mangorense, Marathrum schiedeanum, Oserya coulteriana, and Polypleurum elongatum are compressed and subcylindrical, and the apical meristem is located near the ventral side, as also indicated by the procambial strand close to the ventral side (Figs. 11–15). Unlike pattern 1, cell wall residues are either absent or scant on the root cap surface in species with patterns 2A and 2B, indicating that the outermost cells did not break (Figs. 13, 15, 21, 24, 25). Compared to the larger dorsal part of the dorsiventral root cap, the ventral part is very small and one or two cells thick (Figs. 13, 15). In Oserya coulteriana the ventral root cap has a more or less layered structure with the outer layer of cells longer than the inner layer, indicating that the outer cells are older than the inner (image not shown). The periphery of the dorsal side of the root cap separates from the root proper as the innermost cell walls break in association with the differential growth of the root cap and root epidermis (Figs. 13, 15); similar to the case in pattern-1 roots (images not shown).
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In Marathrum schiedeanum the lateral root arises endogenously near the vascular strand of a parent root. The young root produces a root apical meristem and a dorsiventral root cap while developing within the parent root (Fig. 14). The root cap unevenly covers the root tip very much like that in pattern 2A in the adult or pattern 1.
The broad ribbon-like roots of Polypleurum stylosum and P. wallichii may have unusual forms of pattern 2A. The root cap is very small compared to the root width (Fig. 16). In P. stylosum there is no sharp histological difference between the root apical meristem and cap, except in cell size and stainability. The root cap comprises 2–4 cell layers, the innermost of which lies in roughly the same row as the dorsal and ventral epidermis (Fig. 17). The outermost meristem layer on the ventral side is located under a broken cap cell. In another material, the outermost meristem layer is placed under a unilayered cap and partly exposed because cap cells are ruptured (data not shown). In P. wallichii, the outermost meristem layers on both dorsal and ventral sides, as in pattern 4, form a single, continuous layer enveloping the inner meristem cells. The root cap is one cell thick and vestigial. It may be intermittently differentiated from the outermost meristem layer.
Pattern 2B
Apinagia longifolia, Cladopus austro-osumiensis, C. taiensis, Paracladopus chiangmaiensis, Podostemum rutifolium var. ricciforme, and Thelethylax minutiflora, like most other species of Podostemaceae, have subcylindrical or ribbon-like roots (Figs. 18–21, 24, 25). Rhyncholacis is usually described as lacking roots, so that the plant is interpreted as being composed of a "stem" and leaves (Royen, 1951
; see also Engler, 1930
). However, in our field observations we noted that Rhyncholacis palmettifolia has adventitious roots at the base of shoots. The roots of those species including such adventitious roots have similar structures in the meristem and root cap, so they are described together.
Their root meristem is dorsiventral and composed of a convex layer on the dorsal side, usually a less convex layer on the ventral side, and the inner cells (Figs. 21, 24, 25). The meristem is located near the ventral side of the root and supplied by a procambial strand also close to the ventral surface. The dorsiventrality is verified by cross sections of the root tip (Figs. 19, 20). The ventral epidermis is a basiscopic derivative of the bifacial meristem, whereas particular initials that produce the dorsal epidermis are not obvious. The dorsal cortex is thicker than the ventral, comprising the outer cortex of smaller cells and the inner cortex of larger cells, while the inner cortex is slightly developed in the ventral cortex (Figs. 21, 24, 25), the same as in pattern 2A (Figs. 13, 15).
The root cap is hood-shaped with its apical part covering the hemispheric root tip and is remarkably dorsiventral with the dorsal part long, gutter-like and free (Fig. 18). Cladopus taiensis has a small root cap with the dorsal part barely free. In most species with pattern 2B examined, the root cap is a few to eight cells thick and composed of smaller cells near the root apex and larger cells away from the apex. The root cap is the thickest (thicker than the root proper) in Thelethylax minutiflora among the species examined, mainly due to larger cells. The outermost cells of the root cap on the ventral side lie in the same row as the outermost layer of the root meristem (Figs. 21, 25). In Apinagia longifolia cells of the second to fourth outer layers also are aligned this way (Fig. 24). Hence, those cap cells are most likely acroscopic derivatives from the initials. These cap-producing initials are one to several cell layers thick; the thinnest is in Cladopus austro-osumiensis and the thickest in Apinagia longifolia. The dorsal root cap, along with the dorsal epidermis and cortex, is a basiscopic derivative from the dorsal meristem. Proximal to the tip, the innermost root cap cells on the dorsal side are distorted from the different growth rates between the root cap and epidermis and are eventually broken so that the root cap is detached proximally (Figs. 19–21, 24, 25).
In Podostemum rutifolium var. ricciforme the lateral root arises endogenously near the vascular strand of a parent root (Fig. 22). The root cap of the young root developing within the parent root unequally covers the root tip, a structure similar to pattern 1 or 2A. Shortly after emerging from the parent root, the apical meristem and the root cap become similar to those of the mature root, but the meristem is still covered by the root cap on the ventral side as well as on the dorsal (Fig. 23). New ventral initials seem to arise under the root cap and produce root cap cells and epidermal cells bidirectionally, and in a further elongating lateral root, the outermost root cap cells are acroscopic derivatives of the ventral bifacial meristem, the same 2B pattern as in the adult (Fig. 21).
Pattern 3
The root is crustose and lobed in Hanseniella heterophylla and Thawatchaia trilobata, which, together with the similarly crustose-rooted Hydrobryum, form a clade in the subfamily Podostemoideae (Kita and Kato, 2001
, 2004
; Kato et al., 2004
). The uniform marginal root meristem occurs along the root lobe margin. Re-examination of materials used by Ota et al. (2001)
and Kato et al. (2004)
shows that the meristem is composed of dorsal and ventral layers that sandwich the more or less layered inner cells. The band-like root cap (protective tissue) of collenchymatous cells also has a similar structure with less obvious layering because of cell enlargement. Cell alignment suggests that the dorsal and ventral layers of the root cap are acroscopic derivatives from the dorsal and ventral initials of the root meristem via anticlinal cell divisions (Fig. 3).
Pattern 4
Although Dalzellia gracilis, Tristicha trifaria, and Jenmaniella ceratophylla are assigned to different subfamilies (Tristichoideae and Podostemoideae), their root morphology is simple and quite similar. The root is compressed subcylindrically and does not have a root cap (Figs. 26, 27). The naked apical meristem is located near the center of the root and is composed of inner cells coated by a dermal layer of rectangular cells. The dermal cells divide anticlinally to proliferate initials and epidermal cells and less frequently periclinally to produce inner cells.
Root meristem evolution
In addition to the four patterns described, there is a fifth rootless state in Dalzellia zeylanica (Willis, 1902
; Imaichi et al., 2004
; Kato, in press), Mourera fluviatilis Aublet (Rutishauser and Grubert, 1999
), and Rhyncholacis (Royen, 1951
). Adventitious roots may arise from the shoot in M. fluviatilis (Jäger-Zürn, 2005
) and R. palmettifolia. The reconstructed evolution of the root apical meristem and its derived root cap in the species examined here and reported (Table 1, Fig. 3) shows that in the family, pattern 1 of Tristichoideae and Weddellinoideae is plesiomorphic, while pattern 2 is apomorphic (Fig. 28). Tristichoideae also include the apomorphic pattern 4 and rootless pattern. Within Podostemoideae, pattern 2 is plesiomorphic, and patterns 1, 3, 4 and the rootless pattern are apomorphic. Patterns 3 and 4 are likely to have arisen recurrently. Subpatterns 2A and 2B are distributed in phylogenetically unrelated clades and each subpattern occurs in African, American, and Asian species.
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In our comparison among species representing most major clades of Podostemaceae, we found four cellular patterns, with two subpatterns, of the root meristem and cap (Table 1, Fig. 3). Pattern 1 occurs in Tristichoideae and Weddellinoideae, while pattern 2 is widely distributed in Podostemoideae, with the exception of Vanroyenella plumosa (Table 1, Fig. 28). Pattern 3 is exclusive to Asian Podostemoideae with crustose roots. Differences among the patterns are obvious in development of the root cap, which is a product of the root meristem. In pattern-1 roots, the root cap develops outward and toward the proximal end, like in most angiosperms (Barlow, 2002
). In contrast, cells of root caps with pattern 2 have an age gradient along the length of the root cap with older cells toward the free proximal end on the dorsal side of the root, while pattern-3 roots have a proximodistal gradient. The diversification in root meristem organization is likely to have preceded changes of external morphology except for the root cap, because the subcylindrical or ribbon-like roots do not appear very different in the subfamilies. Nonetheless, pattern 2, which is plesiomorphic in Podostemoideae, is possibly partly involved in the diversification of the subfamily with ca. 260 or more of in total ca. 270 species or more.
Among the four patterns, pattern 1 is the most similar to the pattern in ordinary angiosperm roots with radially symmetrical apical meristems (Esau, 1965
). Pattern 1 of Indotristicha ramosissima and species of Terniopsis may be called intermediate-open type (Groot et al., 2004
) and that of Weddellina squamulosa and Vanroyenella plumosa with the largest region of cap-producing initials, open type (Barlow, 2002
) or basic-open type (Groot et al., 2004
). Most other Podostemoideae also have similar types with respect to the dorsal half of the meristem, although the ventral half differs from that of pattern 1. Groot et al. (2004)
proposed that the root apical meristem of the closed type evolved in the Malpighiales. Podostemaceae are sister to Hypericaceae assigned to the Malpighiales (Savolainen et al., 2000
; Soltis et al., 2000
; Gustafsson et al., 2002
). Because Hypericaceae are likely to have a closed-type meristem, the patterns of Podostemaceae may have been derived from the type, as a result of a change in the orientation of root cap production.
Although the patterns differ in the presence or absence and the distribution of the unique bifacial meristem as well as the presence or absence of the root cap, there are developmental transitions. In Podostemum rutifolium var. ricciforme with pattern 2B, a young lateral root has a poorly dorsiventral meristem similar to that of pattern 1 or 2A. In Marathrum schiedeanum with pattern 2A, a young root has either pattern 1 or 2A. These changes may imply that pattern 2 is derived from pattern 1, or pattern 2B is derived from pattern 2A, although the polarity is only partially consistent with the phylogenetic relationship. Furthermore, transitions between patterns 2 and 3 are seen in some Asian species. Both patterns exist in Hydrobryum japonicum in which, compared with the mature root of pattern 3, a young regenerating root has pattern 2B (Fig. 29 in Ota et al., 2001
).
There is another similarity in root development between Cladopus of pattern 2 and Hydrobryum of pattern 3. In Cladopus the lateral root forms exogenously from the marginal meristem of a parent root where there is no root cap, involving its young dorsal and ventral epidermises (Koi and Kato, 2003
). Then the dorsal epidermal cells of the developing root apex differentiate into the root cap, while the hypodermal cells become the dorsal meristem. In contrast, the ventral meristematic dermal cells become a bifacial meristem in a developmental mode similar to that of Hydrobryum with crustose roots. In H. japonicum a new meristem initiates exogenously in a certain part of the nearly differentiated meristem of a parent lobe, and then gives rise to bifacial meristem layers on both dorsal and ventral sides (Ota et al., 2001
).
Along with the comparative morphology among the three patterns and the general angiosperm root meristem organization, the inferred evolution of the root meristem and cap suggests that pattern 1 is the least specialized and preserves a radially symmetrical apical meristem typical of cylindrical roots, that pattern 2 is derived from it, and that the most specialized pattern 3 is derived from pattern 2 (Figs. 3, 28). Pattern 2, seen only in Podostemaceae, appeared early in the evolution of the subfamily Podostemoideae. The suggested specialization is consistent with that of other morphologies. For example, in contrast to the seedling of Terniopsis malayana of Tristichoideae that forms both a primary shoot and a radicle, seedlings in Podostemoideae lack the radicle and have a reduced primary shoot, and sometimes lack both (Suzuki et al., 2002
; Kita and Kato, 2004
). The shoot apical meristem is present in the adult of Tristichoideae and Weddellinoideae, but absent from Podostemoideae (Imaichi et al., 2005
; Koi et al., 2005
; references cited therein).
In regard to the unique bidirectional histogenesis of the root meristem, we speculate that the evolution from pattern 1 to pattern 2 involved the appearance of the bifacial meristem on the ventral side of the root, and the subsequent evolution from pattern 2 to pattern 3 involved the addition of such a meristem on the dorsal side. The pattern-2 meristem is one-sided; it is located much closer to the ventral side of the root than the meristem of pattern 1. Along with the establishment of a bifacial meristem, a reduction of the ventral portion of the ancestral dome-shaped meristem may have been involved in the evolution of pattern 2, with a subsequent reduction of the dorsal portion during the evolution of pattern 3 (Fig. 3).
The evolution from pattern 2 to pattern 3 took place in close association with the transformation from the subcylindrical or ribbon-like root to the crustose root, which is caused by modification of the organization of the meristem. The rather broad, ribbon-like root of Cladopus javanicus with pattern 2B (Koi and Kato, 2003
) is formed by the prominent marginal meristem located proximolateral to, and derived from, the apical meristem. The marginal meristem is similar to that of pattern 3 in being long, uniform, and more differentiated than the apical meristem, although it is capless. An increase in the marginal meristem and a reduction in the apical meristem are likely to have contributed to the appearance of the crustose root.
Pattern 4, characterized by the absence of the root cap, is seen in Dalzellia gracilis, Tristicha trifaria (Rutishauser, 1997
; this study), Zeylanidium lichenoides, Z. subulatum (Hiyama et al., 2002
), and Jenmaniella ceratophylla. Ameka et al. (2003)
described the absence of the root cap in Ledermanniella browlingii (J. B. Hall) C. Cusset. Organography (Rutishauser, 1997
) and phylogeny (Kita and Kato, 2001
) indicate that, even though caplessness is unusual, the organ observed is comparable with a root. Their root meristems, coated with a single dermal meristem layer, are very similar due to their structural simplicity, although they belong to different subfamilies or clades of the subfamily Podostemoideae. Rare occurrences of pattern 4 in a few remote, nonbasal clades of Podostemaceae and also other angiosperms (Guttenberg, 1968
) suggest that pattern 4 is derived recurrently from the capped roots of pattern 1 or 2 (Fig. 28). Although the character state of the common ancestor to the species of Polypleurum and Zeylandium is equivocal, the derivation from pattern 2 is more likely than from pattern 3, because the crustose root, which is tightly linked with pattern 3, is a derivative relative to the subcylindrical or ribbon-like roots (Suzuki et al., 2002
). Dalzellia gracilis is sister to a clade of D. zeylanica and Indotristicha ramosissima, and all are sister to Tristicha trifaria. Therefore, the root cap may have either been regained later in the evolution of Indotristicha ramosissima or recurrently lost in Tristicha trifaria and Dalzellia gracilis. Similarly, a regain (Hiyama et al., 2002
) or a loss may have occurred in the Polypleurum-Zeylandium lineage.
Temporary absence of the root cap is often visible during capped-root development in Podostemaceae. In seedling culture experiments on nine capped species, the secondary root developing from the hypocotyl is capless early in development and has an apical meristem quite similar to that of these capless species (Suzuki et al., 2002
). In the crustose-rooted Hydrobryum japonicum, the young root lobe is capless, then the root cap (protective tissue) is derived from the differentiated distal portion of the marginal root meristem (Ota et al., 2001
). The same case may hold for Zeylanidium maheshwarii (Hiyama et al., 2002
). Our observations suggest that in Polypleurum wallichii cap formation may temporarily cease in pattern 2, much like that in pattern 4. Taking into account all these results (Ota et al., 2001
; Suzuki et al., 2002
) and the aforementioned development of lateral roots from a capless portion of a parent root in Cladopus species (Koi and Kato, 2003
), a likely scenario for root cap disappearance is that, compared to the delayed cap formation in capped species, cap formation is suppressed or lost at maturity in some species that are remotely related phylogenetically. The root cap plays a central role in the perception of environmental signals such as gravity, water gradients, mechanical impedance, and pathogens (Sievers et al., 2002
). This significant role in perception is probably not played or transferred to an unidentified tissue in the capless species of Podostemaceae.
In conclusion, there is variation in the root apical meristem and cap organization in Podostemaceae. The least specialized organization (pattern 1) is present in Tristichoideae and Weddellinoideae. In the remarkably dorsiventral, one-sided root apical meristem (pattern 2) of Podostemoideae, the ventral layer is bifacial to yield the root cap acroscopically. The crustose root of some Podostemoideae has bifacial meristem layers on both dorsal and ventral sides (pattern 3) so that the root cap is an acroscopic derivative from the meristem. A root meristem with pattern 1 may have become specialized to pattern 2 and then to pattern 3 and may have caused a specialization of the root morphology in the evolution of Podostemaceae. A few species are devoid of the root cap, representing another extreme specialization (pattern 4).
FOOTNOTES
1 The authors thank T. Santisuk, T. Wongprasert, A. K. Pradeep, P. Mathew, D. B. Sumithraarachchi, F. Montata, J.-Q. Liu, S.-J. Lin, D. Darnaedi, G. G. Hambali, R. Lilwah, T. Kajita, M. Hasebe, T. Yamada and Y. Kita for help during field trips and collections and Y. Kita for unpublished phylogenetic data. This study was supported in part by Grants-in-Aid for Scientific Research from the Japan Society for the Promotion of Science. 
4 Author for correspondence (sorang{at}kahaku.go.jp
)
LITERATURE CITED
Ameka G. K. Clerk G. C. Pfeifer E. Rutishauser R.. 2003. Developmental morphology of Ledermaniella bowlingii (Podostemaceae) from Ghana. Plant Systematics and Evolution 237: 165-183.[CrossRef][Web of Science]
Barlow P. W.. 2002. Cellular patterning in root meristem: its origin and significance. In Y. Waisel, A. Eshel, and U. Kafkafi [eds.] Plant roots: the hidden half, 3rd ed 49-82 Marcel Dekker, New York, New York, USA.
Engler A.. 1930. Reihe Podostemonales. In A. Engler and K. Prantl [eds.] Die natürlichen Pflanzenfamilien, 2nd ed., vol. 18a 1-68 Verlag von Wilhelm Engelmann, Leipzig, Germany.
Esau K.. 1965. Plant anatomy, 2nd ed John Wiley, New York, New York, USA.
Groot E. P. Doyle J. A. Nichol S. A. Rost T. L.. 2004. Phylogenetic distribution and evolution of root apical meristem organization in dicotyledonous angiosperms. International Journal of Plant Sciences 165: 97-105.[CrossRef]
Gustafsson M. H. G. Bittrich W. Stevens P. F.. 2002. Phylogeny of Clusiaceae based on rbcL sequences. International Journal of Plant Sciences 163: 1045-1054.[CrossRef]
Guttenberg H. von.. 1968. Der primäre Bau der Angiospermenwurzel Verlag von Gebrüder Borntraeger, Berlin, Germany.
Hiyama Y. Tsukamoto I. Imaichi R. Kato M.. 2002. Developmental anatomy and branching of roots of four Zeylanidium species (Podostemaceae), with implications for evolution of foliose roots. Annals of Botany 90: 735-744.
Imaichi R. Hiyama Y. Kato M.. 2005. Leaf development in the absence of a shoot apical meristem in Zeylanidium subulatum (Podostemaceae). Annals of Botany 96: 51-58.
Imaichi R. Maeda R. Suzuki K. Kato M.. 2004. Developmental morphology of foliose shoots and seedlings of Dalzellia zeylanica (Podostemaceae) with special reference to their meristems. Botanical Journal of the Linnean Society 144: 289-302.[CrossRef]
Jäger-Zürn I.. 2005. Morphology and morphogenesis of ensiform leaves, syndesmy of shoots and an understanding of the thalloid plant body in species of Apinagia, Mourera and Marathrum (Podostemaceae). Botanical Journal of the Linnean Society 147: 47-71.[CrossRef]
Jernstedt J. A. Cutter E. G. Gifford E. M. Lu P.. 1992. Angle meristem origin and development in Selaginella martensii. Annals of Botany 69: 351-363.
Kato M.. 2004. Taxonomic studies of Podostemaceae of Thailand. 1. Hydrobryum and related genera with crustaceous roots (subfamily Podostemoideae). Acta Phytotaxonomica et Geobotanica 55: 133-165.
Kato M.. 2006. Taxonomic studies of Podostemaceae of Thailand. 2. Subfamily Podostemoideae with ribbon-like roots and subfamily Tristichoideae. Acta Phytotaxonomica et Geobotanica 57: 1-54.
Kato M. Kita Y. Koi S.. 2003. Molecular phylogeny, taxonomy and biogeography of Malaccotristicha australis comb. nov. (syn. Tristicha australis) (Podostemaceae). Australian Systematic Botany 16: 177-183.
Kato M. Koi S. Kita Y.. 2004. A new foliose-rooted genus of Podostemaceae from Thailand with a note on root evolution. Acta Phytotaxonomica et Geobotanica 55: 65-73.
Kita Y. Kato M.. 2001. Infrafamilial phylogeny of the aquatic angiosperm Podostemaceae inferred from the nucleotide sequences of the matK gene. Plant Biology 3: 156-163.[CrossRef][Web of Science]
Kita Y. Kato M.. 2004. Molecular phylogeny of Cladopus and Hydrobryum (Podostemaceae, Podostemoideae) with implications for their biogeography in East Asia. Systematic Botany 29: 921-932.[CrossRef][Web of Science]
Koi S. Imaichi R. Kato M.. 2005. Endogenous leaf initiation in the apical-meristemless shoot of Cladopus queenslandicus (Podostemaceae) and implications for evolution of shoot morphology. International Journal of Plant Sciences 166: 199-206.[CrossRef]
Koi S. Kato M.. 2003. Comparative developmental anatomy of the root in three species of Cladopus (Podostemaceae). Annals of Botany 91: 927-937.
Maddison D. R. Maddison W. P.. 2005. MacClade 4: analysis of phylogeny and character evolution, version 4.07 Sinauer, Sunderland, Massachusetts, USA.
Ota M. Imaichi R. Kato M.. 2001. Developmental morphology of the thalloid Hydrobryum japonicum (Podostemaceae). American Journal of Botany 88: 382-390.
Royen P. van.. 1951. The Podostemaceae of the New World. Mededelingen van het Botanisch Museum en Herbarium van de Rijksuniversiteit te Utrecht 107: 1-151 pl. 1–16.
Rutishauser R.. 1997. Structural and developmental diversity in Podostemaceae (river-weeds). Aquatic Botany 57: 29-70.[CrossRef]
Rutishauser R. Grubert M.. 1999. The architecture of Mourera fluviatilis (Podostemaceae): developmental morphology of inflorescences, flowers, and seedlings. American Journal of Botany 86: 907-922.
Rutishauser R. Huber K. A.. 1991. The developmental morphology of Indotristicha ramosissima (Podostemaceae, Tristichoideae). Plant Systematics and Evolution 178: 195-223.[Web of Science]
Savolainen V. Fay M. F. Albach D. C. Backlund A. Van Der Bank M. Cameron K. M. Johnson S. A. Lledó M. D. Pintaud J.-C. Powell M. Sheahan M. C. Soltis D. E. Soltis P. S. Weston P. Whitten W. M. Wurdack K. J. Chase M. W.. 2000. Phylogeny of the eudicots: a nearly complete familial analysis based on rbcL gene sequences. Kew Bulletin 55: 257-309.[CrossRef]
Sievers A. Braun M. Monshausen G. B.. 2002. The root cap: structure and function. In Y. Waisel, A. Eshel, and U. Kafkafi [eds.] Plant roots: the hidden half, 3rd ed 33-47 Marcel Dekker, New York, New York, USA.
Soltis D. E. Soltis P. S. Chase M. W. Mort M. E. Albach D. C. Zanis M. Savolainen V. Hahn W. H. Hoot S. B. Fay M. F. Axtell M. Swensen S. M. Price L. M. Kress W. J. Nixon K. C. Farris J. S.. 2000. Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Botanical Journal of the Linnean Society 133: 381-461.[CrossRef]
Suzuki K. Kita Y. Kato M.. 2002. Comparative developmental anatomy of seedlings in nine species of Podostemaceae (subfamily Podostemoideae). Annals of Botany 89: 755-765.
Troll W.. 1941. Vergleichende Morphologie der höheren Pflanzen, Band 1, Teil 3 Verlag von Gebrüder Borntraeger, Berlin, Germany.
Willis J. C.. 1902. Studies in the morphology and ecology of the Podostemaceae of Ceylon and India. Annals of the Royal Botanic Gardens, Peradeniya 1: 267-465 pl. IV–XXXVIII.
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