Root apical meristem diversity in extant lycophytes and implications for root origins

Abstract

Root apical meristem (RAM) organization in lycophytes could be a key to understanding the early evolution of roots, but this topic has been insufficiently explored. We examined the RAM organization of lycophytes in terms of cell division activities and anatomies, and compared RAMs among vascular plants. RAMs of 13 species of lycophytes were semi-thin-sectioned and observed under a light microscope. Furthermore, the frequency of cell division in the RAM of species was analyzed using thymidine analogs. RAMs of lycophytes exhibited four organization types: type I (Lycopodium and Diphasiastrum), II (Huperzia and Lycopodiella), III (Isoetes) and RAM with apical cell (Selaginella). The type I RAM found in Lycopodium had a region with a very low cell division frequency, reminiscent of the quiescent center (QC) in angiosperm roots. This is the first clear indication that a QC-like region is present in nonseed plants. At least four types of RAM are present in extant lycophytes, suggesting that RAM organization is more diverse than expected. Our results support the paleobotanical hypothesis that roots evolved several times in lycophytes, as well as in euphyllophytes.

Evolution of root apical meristem structures in vascular plants: plasmodesmatal networks

“…b of Fujinami et al. (), we were able to recognize a QC‐like area that corresponded to a cluster of cells immediately inside the radially arranged cell files (Fig. E).…”

“…pseudojaponica (not shown) had obvious layered structures, but unlike H . serrata , a distinct layer of epidermal initial cells was not evident, and both the epidermis and root cap tissues were derived from the common initial cells (outer initials, sensu Yi and Kato, ; Ogura, ; Fujinami et al., ). The maximum and mean PD densities of I .…”

“…Using earlier autoradiographic images of Zea and Pisum (plates 23, 25 of Clowes, ), we were able to draw rough boundaries of probable QC areas and found that there was no difference in PD density between the cells of the probable QC area and initial cells in the surrounding tissue in the RAMs of (at least) Zea mays and Pisum sativum . The occurrence of a “QC‐like area” has recently been reported in the lycophyte RAM of Lycopodium (Lycopodiaceae) through cell‐division analysis (Fujinami et al., ). By comparing our Fig.…”

“…The apical meristem terminates the shoot and the root: the shoot apical meristem (SAM) and the root apical meristem (RAM). Shoot apical meristems and RAMs of extant vascular plants exhibit diversified structures among major taxa (Clowes, ; Esau, ), and at least in the case of RAMs, this structural diversity may reflect the multiple origins of the root after the phylogenetic split of the two major lineages, lycophytes and euphyllophytes (Fujinami et al., ). However, the origins and evolutionary courses of the SAM and the RAM remain unresolved.…”

“…The Selaginella RAM has a prominent apical cell that is similar to those of monilophyte RAMs (Imaichi and Kato, ), but the RAMs of Isoetes and Huperzia are layered structures reminiscent of the closed‐type RAM of angiosperms (e.g., Guttenberg, ; Ogura, ). Furthermore, some species of Lycopodium have nonlayered structures with a cluster of initial cells, reminiscent of the open‐type RAM of angiosperms (Imaichi, ; Fujinami et al., ).…”