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(American Journal of Botany. 2001;88:382-390.)
© 2001 Botanical Society of America, Inc.

Developmental morphology of the thalloid Hydrobryum japonicum (Podostemaceae)1

Makiko Ota 2 , Ryoko Imaichi 2, 3 and Masahiro Kato 4

2Faculty of Science, Japan Women's University, 2-8-1 Mejirodai, Tokyo 112-8681, Japan; and 4Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Tokyo 113-0033, Japan

Received for publication January 4, 2000. Accepted for publication May 18, 2000.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
We describe the unique development and branching of lobed thalli in Hydrobryum japonicum. Lobe formation begins with meristem initiation at random sites near the thallus margin fringed by protective tissues. As the protective tissues are successively peeled off particularly in the growing new lobes, the lobes become naked and then become fringed again by new protective tissues that develop from the marginal part of the new meristems. Subsequently the meristems become less active and are differentiated into parenchymatous ground tissue at maturity. The random pattern of meristem formation during the sporadic development gives rise to a nonorderly branching pattern of the thalli. Some other lobes (~10%) are regenerated from injured parts of the thalli. The vegetative shoots arise endogenously near the thallus margin and are enclosed by the nonvascular strand nets. The rudimentary shoot apices remain embedded in the thalli. The thalli, though remarkably different from typical roots of other angiosperms, might be extremely transformed roots.

Key Words: developmental morphology • homology • Hydrobryum japonicum • meristem • Podostemaceae • root • root cap • shoot


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Podostemaceae grow over waterworn rock surfaces in cascades, waterfalls, and rapids in rivers. Plants are submerged in swift-running water nearly throughout the year, but become emerged in the air during the dry season when the water level is low. Generally flowers or inflorescences mature and shed seeds after emergence. Systematically, Podostemaceae have been considered to be closely related to eudicot families including Crassulaceae, Saxifragaceae, and Hydrostachyaceae (see Les, Philbrick, and Novelo, 1997 ; Ueda et al., 1997), or have been distinguished as one of three angiosperm classes (Cusset and Cusset, 1988b ). However, recent molecular data indicate that Podostemaceae are part of a Malpighiales clade (Soltis et al., 1999 ).

Hydrobryum is one of 47 genera associated with the family (Cook, 1996 ) and belongs to the subfamily Podostemoideae (Engler, 1930 ; van Royen, 1951 ) or Podostemaceae in a narrow sense (e.g., Cusset and Cusset, 1988a ; Cusset, 1992 ). It is distributed in eastern Himalaya, southeastern Asia, and eastern Asia including Japan, which is the northernmost range in the Old World, while most other genera are tropical and subtropical (Cusset, 1992 ; Cook, 1996 ). The genus Hydrobryum consists of three to ~10 species (Cusset, 1992 ; Cook, 1996 ; see also Rutishauser, 1997 ), of which four are distributed in southern Japan (Nakayama and Minamitani, 1999 ). Like some other genera (e.g., Diplobryum, Synstylis), it has very specialized, green, liverwort (or alga)-like thalli. The thalli adhere to the rock surfaces by rhizoids on the ventral surface and have embedded short shoots with leaves and flowers on the dorsal surface. Thus, the thalli of Hydrobryum, like those of some other genera, are involved in adherence, photosynthesis, organogenesis, and reproduction.

Developmental and morphological research has been made to different extents for various genera of Podostemaceae (e.g., Warming, 1881, 1882, 1888, 1891, 1899, 1901 ; Willis, 1902 ; Hammond, 1937 ; Troll, 1943 ; Jäger-Zürn, 1970, 1992, 1995a, b, 1997 ; Rutishauser and Huber, 1991 ; Rutishauser, 1997 ; Rutishauser and Grubert, 1999 ; Rutishauser, Novelo, and Philbrick, 1999 ; Imaichi, Ichiba, and Kato, 1999 ). Many workers have argued that the creeping and branching axes or crusts of most Podostemaceae can be interpreted as roots. Exceptionally, the Dalzellia zeylanica thalli were interpreted as foliose shoots (Jäger-Zürn, 1997 ). Some workers (e.g., Cusset and Cusset, 1988a, b ; Mohan Ram and Sehgal, 1992 ) doubted the homology of the Podostemaceae roots and typical roots of other angiosperms. However, no developmental morphological study has been made of the thalloid Hydrobryum and other genera, so that the homology of the thalli remains uncertain.

This paper describes the developmental morphology of Hydrobryum japonicum Imamura and examines the homology of the thalli. The morphology and anatomy of the organs and tissues of this species were described by Imamura (1929) .


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Material of Hydrobryum japonicum sensu stricto was collected in Kaminokawa River and Ogawa River in Kagoshima Prefecture, Kyushu, southern Japan. The material examined was well developed but sterile. Voucher specimens are deposited in the University of Tokyo Herbarium (TI).

The material was fixed with FAA (formalin:acetic acid:50% ethyl alcohol = 5:5:90 v/v). For anatomical observations, most materials were dehydrated in an ethanol series, embedded in Historesin (glycol methacrylate, Leica, Heidelberg, Germany), cut at a thickness of 2 µm, and stained with a modified Sharman's staining solution (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. Observations were done using a Hitachi S-800 microscope (10 kV).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Morphology and anatomy
Our observations of developed parts of plants are in accord with Imamura's (1929) description. The external morphology of the thalli are foliose, various- sized (up to 20–30 cm in diameter), ~0.5 mm thick, and variously lobed (Figs. 1, 3, 10–13). Large lobes have up to six or seven small lobes along the margin. There is a network of strands in the thalli (Fig. 1). Pale, more or less broken, protective tissues fringe the thalli (Fig. 2). The thalli are adherent to the rock surfaces usually (~80%) by oblong, dark-brown, rhizoid-bearing areas on the ventral surface opposite the shoots (Figs. 3, 32) and by larger ones that occur independently of shoot position (~20%). The rhizoids (adhesive hairs) secrete a glutinous substance, which may also influence cyanobacteria to attach to the surface.



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  		Figs. 1–5. Surface views in light microscopy (Figs. 1, 3 ) and SEM micrographs (Figs. 2, 4, 5 ) of Hydrobryum japonicum. 1. Dorsal side of thallus. Dark spots (one of which is marked by arrow) are young shoots in strand nets. 2. Marginal portion of thallus fringed by protective tissue (P). 3. Ventral side of thallus. It is adherent to rock surface by rhizoids in oblong dark adhesive areas (R). 4 and 5. Shoot emerging from thallus surface (Fig. 4 ) and close-up figure of its basal part (Fig. 5 ). Bars = 5 mm in Figs. 1, 3 ; 50 µm in Fig. 2 ; 1 mm in Fig. 4 ; 200 µm in Fig. 5

 
The shoots are borne on the dorsal surface of the thalli ~2 mm apart from each other. They are enclosed by the strand nets but not supplied by the strands (Figs. 1, 7), as described by Imamura (1929) . The youngest are ~0.5 mm from the thallus margin. The farther the shoots are from the margin, the larger and older they are. The shoots have four to seven tufted, evascular, linear-spatulate leaves (up to 9 mm long or longer), which emerge from the thalli, and a few embedded young leaves (Figs. 4, 5; see also Fig. 33). At this stage in development there is no sign of emerging stems. Since the shoots arise endogenously, they are surrounded by broken epidermal and inner tissues of the thalli (Fig. 5).



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  		Figs. 31–34. Longitudinal sections of shoots at different stages of development in Hydrobryum japonicum, obtained from radial sections of thalli. 31. Shoot primordium just initiated in ground tissue of thallus. 32. Young shoot. Note rhizoids (R) on the ventral epidermis below the shoot and deformed cells above the shoot apical meristem, as in Fig. 34 . 33 and 34. Emerging leaves (Fig. 33 ) and its close-up (Fig. 34 ). Shoot apical meristem (SA) is embedded in thallus. Bars = 50 µm in Fig. 31 ; 100 µm in Figs. 32, 33 ; 20 µm in Fig. 34.

 
Anatomically, all cells of the epidermis and the ground tissue of the thalli contain chloroplasts, which are denser on the dorsal side. The epidermal cells are elongate in the radius of lobes, due to radial expansion of the lobe (see Figs. 2, 18). The matured ground tissue is generally 5–7 cells thick and devoid of any intercellular space (Fig. 6). The tissue is composed of parenchymatous cells and some collenchymatous cells.



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  		Figs. 6–9. Radial (Figs. 6, 8 ), paradermal (Fig. 7 ), and transverse (Fig. 9 ) sections of Hydrobryum japonicum thalli. 6 and 7. Marginal portions. Marginal meristem is covered by protected tissue, and shoot primordium and nonvascular strands are initiated proximal to the meristem. 8 and 9. Nonvascular strands. C, collenchymatous thickening; M, marginal meristem; P, protective tissue; R, rhizoid; S, shoot primordium; ST, nonvascular strand. Bars = 100 µm in Figs. 6, 7 ; 50 µm in Figs. 8, 9

 
The marginal protective tissue is composed of two to five horizontal tiers of lightly stained cells, which are often collenchymatous and, rarely, have small nuclei (Figs. 6, 7). The tier number differs with the age of the thalli: generally the older thalli have fewer tiers. The cells are elongate along the thallus margin, and the outermost cells are prone to break and peel off (Figs. 2, 7). There is a meristem composed of densely stained, small cells below and along the marginal protective tissue, which we term the marginal meristem. The meristem varies in size according with the age of the lobe, ranging from the one with three or four tiers of meristematic cells to the other with ~20 tiers, although the boundary of the meristem is rather obscure (Figs. 16, 17, 25).



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  		Figs. 10–17. Dorsal-surface views in light microscopy (Figs. 10–14 ), and paradermal (Figs. 15, 16 ) and radial (Fig. 17 ) sections of Hydrobryum japonicum thalli at different stages of development. 10. Several young, entire lobes formed from thallus margin. 11 and 12. Older, shallowly incised lobes. Arrows indicate incisions. 13. Old, deeply incised lobe. Arrows indicate the bottoms of incisions between partly overlapping sublobes. Shoots are seen scattered on thallus. 14– 16. Large lobe with new-lobe meristem just initiated below protective tissue. Double arrow in Fig. 14 indicates the site of the Fig. 15 section with meristem almost differentiated into parenchyma. Single arrow indicates the site of the Fig. 16 section with new marginal meristem below protective tissue. 17. Marginal part at nearly the same stage as that of Fig. 16 . M, marginal meristem; P, protective tissue. Bars = 2 mm in Figs. 10–12 ; 10 mm in Fig. 13 ; 5 mm in Fig. 14 ; 50 µm in Figs. 15–17

 
Each of the anastomosing strands consists of ~15 nonvascular, thin-walled, elongate, parenchymatous cells (Figs. 8, 9). They initiate as far from the thallus margin as the shoot primordia (which are described below) and differentiate acropetally toward the thallus margin (Fig. 7).

Thallus development
The thallus lobes grow nearly hemispherically (Figs. 10–13). The young, usually small lobes (0.5–8.0 mm wide from the margin to the base of a lobe in a surface view) are hemispherical and entire (Figs. 10, 18). The older lobes (2–12 mm wide) are also hemispherical and shallowly incised (Figs. 11, 12). The very old, large lobes (13–26 mm wide) are deeply incised (Fig. 13). The lobes cease growth at different stages of development. The margin at the incisions is thinner than the central part of the lobes and fringed by a thinner protective tissue than the entire parts. Incision is brought about by locally different growth of the lobes.

The submarginal tissue below the protective tissue of the mature lobes generally consists of lightly stained, relatively small parenchymatous cells, which seem to undergo no or few cell divisions (Figs. 14, 15). However, in a surface view there are different numbers of spots of initiating meristems below the marginal protective tissue (Figs. 14, 16, 17). The spots arise in random sites along the thallus margin and develop into new lobes.

As the new lobes grow, they are increasingly budded from the old thalli (Fig. 18). In this stage, the lobes are still fringed with the common protective tissue as the old thalli. The new lobes just formed are one or two cells thicker than the old tissue (Fig. 19). It reflects the difference of meristematic activity: it is greater in the young lobes than the mature. Rhizoids are formed in the central part of the young lobes (Fig. 20) and make them adherent to rock surfaces. This is followed by rhizoid production in adhesive areas related to the shoots, as described above (see Figs. 3, 6, 32). The old protective tissue in the growing new lobes peels off and thins (Fig. 20), whereas that in the neighboring thallus does not thin so greatly. Consequently new lobes are naked (Figs. 21, 22).



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  		Figs. 18–26. SEM micrograph (Fig. 18 ) and radial (Figs. 19–21, 23 ) and paradermal (Figs. 22, 24–26 ) sections of Hydrobryum japonicum thalli, showing lobe development subsequent to stages in Figs. 16 and 17 . 18. Young lobe budding from old thallus. A common protective tissue fringes both the new lobe and old thallus. 19. Lobe at almost the same stage as that of Fig. 18 . Arrow indicates the boundary between the new lobe and the old thallus. 20. Older lobe. Note protective tissue that is remnant of old thallus. 21 and 22. Further older lobe. The protective tissue is already peeled off, resulting in naked lobe. Figure 22 is a section neighboring on that of Fig. 21 of the same lobe. 23 and 24. Well-developed lobes with their own, new protective tissues. The lobe of Fig. 24 is slightly older than that of Fig. 23 . Note intact outermost protective cells. 25. Still further developed lobe than that of Fig. 24 . A protective tissue is stretched and the outermost cells are broken. 26. Entirely matured thallus without marginal meristem. M, marginal meristem; P, protective tissue; R, rhizoid. Bars = 200 µm in Fig. 18 ; 50 µm in Figs. 19–26

 
Later, a new protective tissue, about five cells thick horizontally, is differentiated from the marginal part of the meristem in a further-developing lobe (Figs. 23, 24). The outer cells of the tissue are larger than the inner, and the outermost are 65 µm long on average (N = 10). The outer protective cells of the older, larger lobes are increasingly stretched and prone to break and peel off, resulting in the thinning of the tissue (Fig. 25). In matured lobes, the protective tissue is thin and composed of a few tiers of cells in a paradermal section (Fig. 26). The cells are greatly stretched along the margin and are 110 µm long on average (N = 100), 1.7 times as long as those (65 µm) of the young protective tissue (Fig. 24). [For comparison, the meristematic cells are 12.5 µm long on average (N = 10).] Even the innermost cells are much longer than the meristematic cells. The cell elongation and tissue thinning indicate most probably that the protective tissue is produced only once during lobe development and stretches as the lobes grow hemispherically.

The marginal meristem is active until the late stage of lobe development (Fig. 25). Subsequently, most of the meristem is differentiated into parenchyma (Fig. 26), although parts of it remain meristematic as spots even though less vigorous (Fig. 14). Note that the lobe of Fig. 26 is older than that of Fig. 15, showing differentiation into parenchyma. This differentiation begins earlier at the lateral (proximal) margin of the lobes than at the central (distal) margin.

Regeneration of thalli
Most of the lobes examined (~90%) arise from the thallus margin in the developmental manner described above, but some others (~10%) are regenerated from injured parts of the thalli (Fig. 27). In such regeneration, cell divisions take place in the inner cells of the injured part, and a few cells below the ventral epidermis (Fig. 28). The new cells give rise to the meristem of a regenerating lobe. The tissue of the parental thalli covering the lobe peels off soon, and the lobe develops in the same manner as the lobes that arise from the intact margin of the thalli (Fig. 29). Lobes may also regenerate from near the base of the shoots, where the thalli are broken by emerging leaves (Fig. 30).



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  		Figs. 27–30. SEM micrographs (Figs. 27, 30 ) and radial sections (Figs. 28, 29 ) of Hydrobryum japonicum thalli showing thallus regeneration. 27–29. Regeneration from injured portion of thalli. 27. Regenerated lobe. 28. New meristem just initiated in ground tissue of thallus. 29. Developing lobe fringed by its own protective tissue. 30. Regeneration from near shoot base. L, leaf; P, protective tissue; RL, regenerated lobe. Bars = 500 µm in Figs. 27, 30 ; 100 µm in Figs. 28, 29

 
Shoot development
The shoot primordia initiate 0.1–0.3 mm or ~30 cells from the thallus margin and arise endogenously within the ground tissue. In longitudinal section, they are composed of small cells that have densely stained nuclei and cytoplasm, and are displaced below lightly stained parenchymatous cells (Fig. 31). Those small meristematic cells produce a shoot composed of a rudimentary shoot apical meristem and leaf primordia (Fig. 32). As the shoots grow, the lightly stained cells above the shoots are deformed but remain there (Fig. 32; see also Fig. 34). As the leaves grow, most of them emerge through the clefts in which the thallus tissues are broken (Fig. 33).

The shoot apex remains embedded within the thallus (Fig. 33). In a longitudinal section, the apex is a little concave, small, and composed of about four small cells in the surface layer and a small number of small inner cells (Fig. 34).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
The developmental pattern of the Hydrobryum japonicum thalli described here is the first for the Podostemaceae. A summary follows. The initiation of new lobes begins with meristem formation in random sites below the marginal protective tissue in the old lobes, which have nearly ceased development. As the new lobes grow, the new marginal meristem becomes naked due to the peeling-off of the protective tissue. Then a new protective tissue is differentiated from the marginal part of the new meristem. Later, the growth of the lobes decreases and eventually ceases accompanied by parenchymatization of the meristem. This pattern may also be found in Zeylanidium olivaceum and other species with a histologically similar thallus margin (Warming, 1891 ; Willis, 1902 ; Jäger-Zürn, 2000a ), although developmental data are lacking. It differs remarkably from the pattern of the more or less axial or ribbon-shaped roots in many other Podostemaceae, which have, or are supposed to have, continuously active apical meristems (Warming, 1881, 1882, 1888 ; Willis, 1902 ; Troll, 1943 ; Rutishauser and Huber, 1991 ; Rutishauser, 1997 ; Imaichi, Ichiba, and Kato, 1999 ).

The marginal meristem formation at random sites in old lobes during sporadic development gives rise to the nonorderly branching pattern characteristic of Hydrobryum japonicum. A similar branching seems to occur in Zeylanidium olivaceum (Willis, 1902 ; Jäger-Zürn, 2000a ). Rutishauser (1997) noted that the foliose or ribbon-shaped roots of some Podostemaceae (e.g., Polypleurum and Zeylanidium) show exogenous branching and marginal growth. Random meristem formation is much more influential in the morphogenesis of Hydrobryum. In many other Podostemaceae the roots arise endogenously and are branched in the same apparently monopodial manner as, or in a similar way to, the one described in other angiosperms (Willis, 1902 ; Rutishauser, 1997 ; Imaichi, Ichiba, and Kato, 1999 ).

There is no typical root cap in Hydrobryum japonicum. Instead, the thallus margin is fringed by a protective tissue that is differentiated once during lobe development from the marginal part of meristem. Imamura (1929) applied the term root cap for this tissue, as Warming (1891) , Willis (1902) , and Jä ger-Zürn (2000a) did in Zeylanidium olivaceum. Generally in vascular plants, the root cap is produced continuously from the root apical meristem, or the root cap initials or calyptrogen (Esau, 1965 ; Steeves and Sussex, 1989 ; Fahn, 1990 ; Webster and MacLeod, 1996 ). It is the case with many other Podostemaceae (e.g., Warming, 1881, 1882, 1888 ; Willis, 1902 ; Troll, 1943 ; Rutishauser and Huber, 1991 ; Rutishauser, 1997 ; Imaichi, Ichiba, and Kato, 1999 ). Apparently the root cap cells contain amyloplasts in axial roots of a Podostemaceae species (R. Imaichi, unpublished data), as is common in the vascular plants (Esau, 1965 ; Sievers and Braun, 1996 ).

Regeneration is known in many Podostemaceae (Warming, 1881 ; Willis, 1902 ; Hammond, 1936 ; Imaichi, Ichiba, and Kato, 1999 ; R. Imaichi, unpublished data). It seems to be adaptive for the Podostemaceae that live in swift-running river water containing soil particles and other materials, which subject the thalli to injury. In culture Podostemum ceratophyllum can generate roots from various organs (Hammond, 1936 ). In natural populations of various species, new roots (or thalli) are produced endogenously from injured parts of the roots (or thalli) (e.g., Warming, 1881 ; Willis, 1902 ; Imaichi, Ichiba, and Kato, 1999 ). It is noteworthy that in Hydrobryum japonicum new lobes are regenerated from the thallus tissues near the shoots, as well as injured parts of thalli. It suggests that tissues surrounding the shoots may be involved in regeneration in most other species of Podostemaceae with endogenous shoots.

The shoots of Hydrobryum japonicum are composed of several evascular, small leaves on the very small apex. Their endogenous origin is common in this and other Podostemaceae with axial or thalloid roots (Warming, 1881, 1882, 1891 ; Willis, 1902 ; Imamura, 1929 ; Rutishauser and Huber, 1991 ; Rutishauser, 1997 ; Jäger-Zürn, 1997, 2000a, b ; Imaichi, Ichiba, and Kato, 1999 ). The shoot apices remain embedded within the ground tissue of the thalli at maturity, as in Cladopus nymanii (R. Imaichi, unpublished data) and perhaps in Diplobryum minutale, other Hydrobryum species including H. floribundum, Synstylis micranthera, Polypleurum species, and Zeylanidium species (Willis, 1902 ; Troll, 1943 ; Cusset, 1992 ; Rutishauser, 1997 ; Jäger-Zürn, 2000a ). Such embedded shoots, often accompanied with flattened roots or thalli, are considered to be a reductive specialization. In many other Podostemaceae (van Royen, 1951, 1953, 1954 ; Cook, 1996 ; Rutishauser, 1997 ; Imaichi, Ichiba, and Kato, 1999 ), the shoot apices emerge from the thalli. The reduced shoots differ from these conspicuous emerging shoots in having no vascular tissue.

The thallus of Hydrobryum japonicum is still an enigmatic organ remarkably different from the ordinary root. It does not only lack an apical meristem and root cap typical of the root, but also has a network of nonvascular strands instead of vascular ones, although plural vascular strands are seen in the Cladopus roots (Shin, 1950 ). Nonetheless, because of the presence of a protective tissue and root-hair-like rhizoids, and the endogenous shoot development, as well as monophyly of Podostemaceae (Les, Philbrick, and Novelo, 1997 ; Ueda et al., 1997 ; Soltis et al., 1999 ), it might be likely that the thalli are extremely transformed roots. We need further comparative ontogenetic studies of the roots based on the phylogenetic relationships of the Podostemaceae.


   FOOTNOTES
 
1 Support for this study was provided by Grants-in-Aid from Scientific Research from Japan Society for the Promotion of Science and by the Foundation of River and Watershed Environment Management. Back

3 Author for reprint requests (e-mail: ryoko{at}jwu.ac.jp ) Back


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
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