Root apical meristem diversity and the origin of roots: insights from extant lycophytes

Journal of Plant Research - The independent origin of roots in lycophytes and euphyllophytes has been proposed, mainly based on paleobotanical records. However, the question of how roots evolved...     

Developmental study onHypolepis punctata (Thunb.) Mett.

The origins of the first and second petiolar buds ofHypolepis punctata were clarified in relation to the early development of the leaf primordium, which arises from a group of superficial cells of the shoot apical meristem. One of these superficial cells produces a two-sided leaf apical cell which subsequently cuts off segments to make a well-defined cell group, called here the leaf apical cell complex, on the distal part of the leaf primordium. Meanwhile, cells surrounding the leaf apical cell complex also divide frequently to form the basal part of the leaf primordium. Two groups of basal cells of the leaf primordium located on the abaxial and the adaxial sides initiate the first and the second petiolar buds, respectively. The initial cells are usually contiguous to the leaf apical cell complex, constructing the abaxial and adaxial flanks of the very young leaf primordium. However, the first petiolar bud sometimes develops from cells located farther from the leaf apical cell complex. These cells are derived from those originally situated in the peripheral region of the shoot apical meristem. This study was supported by a Grant-in-Aid for Encouragement of Young Scientists by the Ministry of Education, Science and Culture, of Japan No. 474322 in 1979.     

The outer integument and funicular outgrowth complex in the ovule of<Emphasis Type="Italic"> Magnolia grandiflora</Emphasis> (Magnoliaceae)

The development of the outer integument and funicular outgrowth in the ovule of Magnolia grandiflora was examined by microtomy and scanning electron microscopy to reveal the morphology and evolution of the outer integument, a novel angiosperm structure. Early in development the outer integument is semiannular, decurrent to the lateral sides of the funiculus, and extends downwards beyond the funicular outgrowth that forms in the gap of the outer integument, and is transverse to the funiculus. The outer integument then overgrows the funicular outgrowth perpendicularly to the funiculus to form a micropyle together. The hood-shaped outer integument and the funicular outgrowth compose an envelope complex, and the interpretation of a single cupular outer integument is not supported. This envelope complex may differ from the cupular outer integument of other angiosperms, e.g., Nymphaeaceae, suggesting independent origin of apparently cupular outer integuments and hood-shaped outer integuments. Anatropous curving is due mainly to differential growth of the chalaza. The bistomic micropyle of Magnoliaceae seems to represent a derived character state, compared to an endostomic micropyle. T. Yamada is a research fellow of the Japan Society for the Promotion of Science.     

Comparative development of heavily asymmetric-cordate gametophytes of <Emphasis Type="Italic">Anemia phyllitidis</Emphasis> (Anemiaceae) focusing on meristem behavior

Development of heavily asymmetric cordate gametophytes of Anemia phyllitidis (Anemiaceae), one of the schizaeoid ferns, was examined using a sequential observation technique; epi-illuminated light micrographs of the same growing gametophytes were taken approximately every 24 h. The apical cell-like wedge-shaped cell was produced once from the terminal cell of a germ filament, but it stopped dividing soon after production of one or two derivative cells. Without a functional apical cell, the gametophyte developed by intercalary growth until the early stage of wing formation, and then the multicellular (pluricellular) meristem arose from the lower lateral side of the gametophyte. This was in sharp contrast to the observation that the multicellular meristem forms in place of the apical cell in typical cordate gametophytes. Loss of the functional apical cell probably caused a site-shift in the multicellular meristem of the Anemia phyllitidis gametophyte during evolution from apical to lateral. The results suggest that apical cell-based and multicellular meristems are primarily independent of each other. The multicellular meristem produced cells equally in the distal and proximal directions to form wings in both directions but proximally produced cells divided much less frequently. As a result, a heavily asymmetric gametophyte was formed.     

Adventitious buds ofdryopteris sparsa complex (dryopteridaceae): Developmental anatomy and systematic implication

Adventitious buds of theDryopteris sparsa complex were examined anatomically and taxonomically. While no buds are found inD. hayatae andD. sparsa, they occur inD. sabaei, D. yakusilvicola, and in putative hybrids of which one parent seems to beD. sabaei. The buds function as a means of vegetative reproduction in the species and hybrids. The buds arise as a pair on stipes of abortive leaves without lamina. InD. sabaei the youngest bud primordium observed consists of a small group of surface and subsurface meristematic cells surrounded by differentiated tissue cells, and the meristematic cells appear to be quiescent. As the bud primordia develop, the inner and then outer parenchymatous cells below the meristematic cells divide each into several small cells, among which the procambial strands are later differentiated to connect the bud primordium to the vascular strand of the leaf. The meristematic cells also undergo cell divisions, and the bud primordium becomes larger. A shoot organization of the bud primordium is later established. The bud-bearing, uniquely abortive leaves and delayed development of the buds support the taxonomic relationship of agamosporousD. yakusilvicola having been derived from hybridization betweenD. sabaei andD. sparsa.     

Developmental anatomy of the shoot apical cell,rhizophore and root ofSelaginella uncinata

The developmental anatomy of the shoot apex, rhizophore and root ofSelaginella uncinata was examined by the semi-thin section method. The shoot apex has a single, lens-shaped apical cell with two cutting faces. Rhizophore primordia are initiated exogenously at the branching point of the second youngest lateral shoot. The rhizophore apex has a tetrahedral apical cell with three cutting faces. A pair of root primordia is initiated endogenously from inner cells of the rhizophore apex, after the rhizophore apical cell becomes unidentifiable losing its activity, and subsequently a root cap is formed from the distal face of the root apical cell. During the course of successive root branching the apical cell in an original root apical meristem becomes unidentifiable and then a new apical cell is initiated in each of the bifurcated root apical meristems. The root branching mode seems to be equivalent to the described dichotomous branching mode of fern shoots. Our results demonstrate a distinct morphogenetical difference between the rhizophore and the root, and confirm the exogenous origin of the rhizophore, as described for other species ofSelaginella. This evidence indicates that the rhizophore is not an aerial root but a leafless, root-producing axial organ.     

Taxonomic status of Monotropastrum humile, with special reference to M. humile var. glaberrimum (Ericaceae, Monotropoideae)

Taxonomic treatment of the achlorophyllous monotropoid plant Monotropastrum humile is still unclear and confusing because of the lack of detailed morphological analyses and molecular phylogeny. In particular, the taxonomic status of a glabrous variety, M. humile var. glaberrimum, is under debate. Our detailed examination of the morphological characteristics of living plants revealed that M. humile var. glaberrimum can be easily distinguished from the putative conspecific taxon M. humile var. humile by characteristics not previously recognized, namely the shape and color of the floral disc. Most morphological features characterizing Cheilotheca were also found in M. humile var. glaberrimum. Moreover, there was considerable nucleotide differentiation in the internal transcribed spacer (ITS)2 sequences of M. humile var. humile and var. glaberrimum. Molecular analysis of the phylogenetic relationship of M. humile var. humile, var. glaberrimum, and other monotropoids using ITS2 sequences showed that two varieties of M. humile formed a monophyletic clade with a member of a different genus, Monotropa L., but obvious phylogenetic relationships among these three taxa were not obtained. Thus we conclude that Monotropastrum humile var. glaberrimum should be treated as a distinct species. However, the generic affiliation of M. humile var. glaberrimum could not be determined because of its intermediate character state combination and the insufficient characterization of related species. We strongly suggest that Monotropastrum as a whole needs re-evaluation.     

Development and structure of trichotomous branching in Edgeworthia chrysantha (Thymelaeaceae)

We studied the development and structure of the unusual trichotomous branching of Edgeworthia chrysantha. Three "branch primordia" are formed sequentially on the shoot apex of a main axis and develop into trichotomous branching. The branch primordia are clearly distinguishable from the typical axillary buds of other angiosperms; they develop much more rapidly than axillary buds, and the borders between the branch primordia and shoot apex of the main axis are anatomically unclear. Furthermore, at a later stage, leaves subtending the branch primordia produce typical axillary buds. These results suggest that the trichotomous branching in this species involves the division of the shoot apical meristem. Expression analysis of genes involved in branching or maintenance of the shoot apical meristem in this species should clarify the control mechanism of this novel branching pattern in angiosperms. We also observed the phyllotactic patterns in trichotomous branching and have related these patterns to the shoot system as a whole.     

Developmental anatomy of <Emphasis Type="Italic">Terniopsis malayana</Emphasis> (Podostemaceae,subfamily Tristichoideae), with implications for body plan evolution

The developmental morphology of Terniopsis malayana, an unusual aquatic angiosperm from Thailand, was examined. A unique vegetative structure called the “ramulus” arises endogenously in the root tissue. The ramulus has an actively growing apical meristem. The ramulus branches several times to form a “ramulus complex” consisting of up to six ramuli, which are distichously arranged in almost a single plane. In a ramulus complex, the new ramulus (ramulus branch) is initiated on the adaxial side of the first (the basalmost) scale in the first ramulus, but at a site lateral to the first scale in later ramuli, suggesting that the new ramulus arises from axillary or extra-axillary buds of the immediately older ramulus. Ramulus growth is terminated in association with the loss of the apical meristem, and its axillary or extra-axillary buds begin to grow to form the next new ramulus instead. The flower occurs in place of the youngest ramulus, when reproductive. It seems likely that the Terniopsis ramulus and its scale are comparable to the shoot and leaf, and thus a ramulus complex is interpreted as a sympodially branched shoot.     

Developmental anatomy of the three-dimensional leaf ofBotrychium ternatum (Thunb.) Sw.

The ophioglossaceous leaf exhibits a unique morphology, three-dimensional constitution. This examination clarified the developmental manner of the leaf ofBotrychium ternatum (Thunb.) Sw. The leaf primordium develops as an ordinary appendicular leaf which shows a typical hyponastic growth curvature, though it soon takes a conical shape with a tetrahedral apical cell. The leaf primordium forms a sporophyll primordium first, then forms vegetative primary pinnae acting as the trophophyll primordium. The sporophyll primordium also forms sporogenous primary pinnae. The sporophyll initiation begins with establishment of a new apical cell (sporophyll apical cell) near the original leaf apical cell. Through activity of the sporophyll apical cell most of the sporophyll primordium is formed later. In contrast, the vegetative or sporogenous primary pinna begins to develop as a low mound of surface cells on the trophophyll or sporophyll primordium respectively. The apical cell is later established on the summit of each pinna primordium. In the developmental point of view, the sporophyll primordium is not equivalent to the primary pinnae on the trophophyll primordium. The sporophyll may not represent two fused basal pinnae of a leaf, but represents an organ independent of and equivalent to the trophophyll.