Satoshi Koi

Expression of SHOOT MERISTEMLESS , WUSCHEL , and ASYMMETRIC LEAVES1 Homologs in the Shoots of Podostemaceae: Implications for the Evolution of Novel Shoot Organogenesis

This work explores how organogenesis of the shoot apical meristem (SAM)-less shoots evolved from that of the typical SAM-mediated shoots in the aquatic eudicot Podostemaceae. Based on the expression patterns of STM, WUS, and ARP orthologs, the leaf in SAM-less shoot species is initiated as a SAM and differentiates into a single apical leaf, resulting in the evolution of novel shoot-leaf mixed organs in Podostemaceae. Podostemaceae (the river weeds) are ecologically and morphologically unusual angiosperms. The subfamily Tristichoideae has typical shoot apical meristems (SAMs) that produce leaves, but Podostemoideae is devoid of SAMs and new leaves arise below the base of older leaves. To reveal the genetic basis for the evolution of novel shoot organogenesis in Podostemaceae, we examined the expression patterns of key regulatory genes for shoot development (i.e., SHOOT MERISTEMLESS (STM), WUSCHEL (WUS), and ASYMMETRIC LEAVES1/ROUGH SHEATH2/PHANTASTICA (ARP) orthologs) in Tristichoideae and Podostemoideae. In the SAM-mediated shoots of Tristichoideae, like in model plants, STM and WUS orthologs were expressed in the SAM. In the SAM-less shoots of Podostemoideae, STM and WUS orthologs were expressed in the initiating leaf/bract primordium. In older leaf/bract primordia, WUS expression disappeared and STM expression became restricted to the basal part, whereas ARP was expressed in the distal part in a complementary pattern to STM expression. In the reproductive shoots of Podostemoideae with a normal mode of flower development, STM and WUS were expressed in the floral meristem, but not in the floral organs, similar to the pattern in model plants. These results suggest that the leaf/bract of Podostemoideae is initiated as a SAM and differentiates into a single apical leaf/bract, resulting in the evolution of novel shoot-leaf mixed organs in Podostemaceae.

Comparative anatomy of root meristem and root cap in some species of Podostemaceae and the evolution of root dorsiventrality

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.

Endogenous Leaf Initiation in the Apical‐Meristemless Shoot of Cladopus queenslandicus (Podostemaceae) and Implications for Evolution of Shoot Morphology

Podostemaceae are an ecologically and morphologically unusual aquatic group of angiosperms; e.g., Cladopus queenslandicus lives in rapids and waterfalls and has adventitious shoots on the subcylindrical roots prostrate on rocks. In this light and transmission electron microscopic study, we describe a peculiar organogenetic pattern of endogenous leaf initiation at the shoot tip in the absence of an apical meristem in C. queenslandicus. This pattern, like the one described previously in some other species, is in marked contrast to the general pattern seen in most angiosperms that the shoot apical meristem is essential to leaf formation on the flank. Leaf formation also involves two unique processes: (i) cell separation that occurs on the outside of the incipient leaf primordium and (ii) vertical tissue splitting in a region where a shoot apical meristem exists in other angiosperms. Comparison in the presence or absence of a shoot apical meristem, cell separation, and tissue splitting in Podostemaceae shows that this organogenetic pattern may be a defining evolutionary novelty of the Asian‐Australian lineage of the subfamily Podostemoideae.

Developmental morphology of seedling and shoot and phylogenetic relationship of Diplobryum koyamae (Podostemaceae)

We demonstrated that saltational evolution was recurrent in the body plans of seedlings of the aquatic angiosperm Podostemaceae, in contrast to other angiosperms with seedlings having almost common body plans. Diplobryum koyamae, transferred to the genus Hydrodiscus described in this paper, has long-floating shoots with an anchoring disk-like base and is rootless. Such a body plan is distinct from other members of Asian Podostemoideae comprising reduced or moderate shoots borne on the root. Here, our molecular phylogenetic analysis revealed that H. koyamae is sister to a crustose-rooted group of Hanseniella, Hydrobryum and Thawatchaia within Asian Podostemoideae. The germinating embryo was devoid of plumule and radicle, and comprised a single cotyledon and a short hypocotyl, which produced an adventitious shoot endogenously. The leaves are formed in the absence of the shoot apical meristem, accompanying the separation of lightly stained cells. Comparison with other species of Asian Podostemoideae having the plumule and the adventitious root in the seedling, along with their phylogenetic relationship, suggests that saltational evolution occurred in the seedling body plan of H. koyamae leading to the extraordinary adult body plan, as in the separate clade of Dalzellia, Indodalzellia, and Indotristicha of the subfamily Tristichoideae.

Phylogenetic Relationship and Morphology of Dalzellia gracilis (Podostemaceae, Subfamily Tristichoideae) with Proposal of a New Genus

Dalzellia gracilis, an enigmatic species of Podostemaceae, is characterized by the subcylindrical creeping roots and dorsiventral ribbonlike shoots borne on the roots. To reveal the phylogenetic relationships of D. gracilis, molecular phylogenetic and morphological analyses were performed. A matK tree indicates that it is most likely sister to a clade of its congeners and Indotristicha ramosissima. Dalzellia gracilis, like Tristicha, has subcylindrical, capless roots, and it exhibits an endogenous developmental pattern in both shoots and associated holdfasts shared by Terniopsis, Indotristicha, and Tristicha. The dorsiventral ribbonlike adventitious shoots, with the dorsiventral compressed shoot apical meristem producing dimorphic leaves on the dorsal and ventral‐lateral sides, are extremely similar to the crustose shoots of the other species of Dalzellia. Dalzellia gracilis is devoid of rosettes, although the other congeners have them. The many free leaves subtending the base of the pedicel are also unique to the species, whereas the trimerous flower is common to subfamily Tristichoideae. On the basis of these molecular and morphological results, we describe a new genus Indodalzellia for D. gracilis to draw attention to these morphological distinctions. Dalzellia, Indodalzellia, and Indotristicha have remarkable morphological differences compared to the inconspicuous morphological diversity in Tristicha and Terniopsis and between the two genera.

Developmental anatomy of the reproductive shoot in Hydrobryum japonicum (Podostemaceae)

Podostemaceae are unusual aquatic angiosperms adapting to extreme habitats, i.e., rapids and waterfalls, and have unique morphologies. We investigated the developmental anatomy of reproductive shoots scattered on crustose roots of Hydrobryum japonicum by scanning electron microscopy and using semi-thin serial sections. Two developmental patterns were observed: bracts arise either continuously from an area of meristematic cells that has produced leaves, or within differentiated root ground tissue beneath, and internal to, leaf base scars after an interruption. In both patterns, the bract primordia arise endogenously at the base of youngest bracts in the absence of shoot apical meristem, involving vacuolated-cell detachment to each bract separately. The different transition patterns of reproductive shoot development may be caused by different stages of parental vegetative shoots. The floral meristem arises between the two youngest bracts, and is similarly accompanied by cell degeneration. In contrast, the floral organs, including the spathella, arise exogenously from the meristem. Bract development, like vegetative leaf development, is unique to this podostemad, while floral-organ development is conserved.

Two new species of Hydrobryum (Podostemaceae) from Laos

SummaryTwo new species of Podostemaceae are described from a single site in northern Central Laos. Hydrobryum hapteron is characterised by the many long holdfasts in the basal area of the crustose root and the long stalks of capsules. It shares the prominent holdfasts and stalks of capsules with H. ramosum (C. Cusset) Koi & M. Kato but is distinct from it in the crustose root. Hydrobryum subcylindricoides is similar to H. subcylindricum Koi & M. Kato in the ribbon-like root but differs from it in the wider root, Y-shaped stigmas and fewer ribs on the capsule.