The origin of plants: body plan changes contributing to a major evolutionary radiation.

نویسندگان

  • L E Graham
  • M E Cook
  • J S Busse
چکیده

P lants (land plants, embryophytes) are of monophyletic origin from a freshwater ancestor that, if still extant, would be classified among the charophycean green algae. Plants, but not charophyceans, possess a life history involving alternation of two morphologically distinct developmentally associated bodies, sporophyte and gametophyte. Body plan evolution in plants has involved fundamental changes in the forms of both gametophyte and sporophyte and the evolutionary origin of regulatory systems that generate different body plans in sporophytes and gametophytes of the same species. Comparative analysis, based on molecular phylogenetic information, identifies fundamental body plan features that originated during radiation of charophycean algae and were inherited by plants. These include, in probable evolutionary order: cellulosic cell wall, multicellular body, cytokinetic phragmoplast, plasmodesmata, apical meristematic cell, apical cell proliferation (branching), threedimensional tissues, asymmetric cell division, cell specialization capacity, zygote retention, and placenta. Body plan features whose origin is linked to the dawn of plants include: multicellular sporophyte body, histogenetic apical meristem in the gametophyte body, and capacity for tissue differentiation in both sporophyte and gametophyte. Origin of a well-defined sporophytic apical stem cell and a system for its proliferation, correlated with capacity for organ production and branching, occurred sometime between the divergence of modern bryophytes and vascular plant lineages. Roots and their meristem and a multilayered tunica-corpus shoot apical meristem arose later. Regulatory genes affecting shoot meristems, which have been detected by analysis of higher plant mutants, may be relevant to understanding early plant body plan transitions. Fundamental aspects of the plant body plan are remarkably consistent within the plant kingdom and are different from metazoans. All plants exhibit at least one form of apical meristem consisting of one or more cells that are functionally analogous to metazoan stem cells because they are histogenetic, i.e., able to generate specialized tissues. Plants differ from animals in that the plant apical meristem has the additional capability to generate organs (leaves and stem) and reproductive organ systems (cones or flowers) throughout the life of the plant, whereas the number and form of metazoan organs are embryonically determined. Plants are often described as having a ‘‘modular construction’’ that allows flexibility in organ production in response to changes in environmental conditions. Plants also differ from animals in that the plant sexual life history involves an alternation of two multicellular bodies (sporophyte and gametophyte) that are morphologically different and have changed differently through time. Thus the body plans of these two life history phases have taken separate evolutionary pathways (Fig. 1). That a simple single-celled histogenetic apical meristem (Fig. 2) appeared very early in plant evolution is suggested by the fact that this type of meristem occurs in modern plants that are considered to be early divergent and not in the green algal ancestors of plants. Early divergent plant forms include bryophytes (liverworts, hornworts, mosses), simple rootless plants considered to lack specialized food and lignified water conducting cells (vascular tissue), as well as simple vascular plants that produce spores rather than seeds. Later-appearing vascular plant groups are characterized by multicellular shoot and root apical meristems. Vascular plants differ from bryophytes in possessing two types of apical meristem, those of the shoot and root. Woody vascular plants possess two additional forms of meristematic tissues, the vascular and cork cambia. Comparative morphology and developmental studies suggest that the apical meristems of gametophytesysporophytes, bryophytesyvascular plants, and organsyorgan systems may be homologous, and that the more complex meristems are derived from simpler forms. Emerging data on genetic control of apical meristem development and function, derived from the study of higher plant mutants that exhibit disruption in meristems (some of which are later described) are expected to allow rigorous testing of these hypotheses. This article focuses on: (i) the earliest stages in the origin of the plant body, including origin of an apical meristem, histogenesis, and essential precursor characters such as the cellulosic cell wall, phragmoplast cytokinetic system, and asymmetric cell division, all of which originated in the ancestors of plants, the charophycean green algae, and (ii) transition to the simplest plant body plan. The origin of the plant embryo and other early reproductive innovations have been reviewed separately (1). Higher plant meristems are also covered elsewhere (2).

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عنوان ژورنال:
  • Proceedings of the National Academy of Sciences of the United States of America

دوره 97 9  شماره 

صفحات  -

تاریخ انتشار 2000