Motile gametes of land plants: Diversity, development, and evolution

Spermatogenesis is a morphogenetic system in plants that is unparalled in i ts potential to yield diverse and informative structural and developmental data. The unquestionable homology of terrestrial plant spermatozoids to eac h other and to gametes of related lineages allows an examination of cellula r evolution and provides sound data for phylogenetic analyses. In this revi ew we examine the architecture and ontogeny of motile male gametes among ma jor groups of land plants. We begin with a historical perspective that emph asizes the utility of spermatogenesis in understanding cellular evolution a nd in determining phylogenetic relationships. A cladistic analysis of data based solely on spermatogenesis and a conceptual phylogeny based on combine d morphological and molecular data serve as the basis for the comprehensive discussion of architectural and developmental features of plant spermatozo ids. Spermatozoids of green plants have two fundamental architectural designs: b iflagellated or multiflagellated. Biflagellated gametes vary among basal ar chegoniates and charophytes in degree of coiling, position, and substructur e of the basal bodies and number of organelles. Hornwort spermatozoids are simple, bilaterally symmetrical, and uniquely exhibit a right-handed coil. An autapomorphy among setaphytes (a clade containing mosses and liverworts) is the production of coiled biflagellated sperm cells with dimorphic stagg ered basal bodies. Like bryophytes, gametes of most lycophytes are biflagel lated; two exceptions are Isoetes and Phylloglossum, taxa that independentl y evolved multiflagellated sperm cells with approximately 20 flagella. Deve lopmental information, especially related to the origin and development of the locomotory apparatus, are essential to determine structural homology am ong these taxa. Evaluation of the more complicated multiflagellated gametes of other vascular plants reveals similarities that support a monophyletic fern, Equisetum and Psilotum assemblage. Autapomorphies of this clade inclu de the arrangement of the microtubular cytoskeleton, origin of the locomoto ry apparatus, and structural details of the basal bodies and multilayered s tructure. Sperm cell development in archegoniates involves the complete transformatio n of virtually every cellular component. Crucial to this process are protei naceous elements of the cytoskeleton. Complex microtubule arrays unique to these cells include the spline, basal bodies, and flagella. The discrete mi crotubule-organizing centers (MTOCs) that generate these cytoskeletal array s are equally complex and enable the examination of molecular constituents and ontogenetic modifications. The protein centrin is found in a variety of structures, including the diverse MTOCs and the locomotory apparatus. Acti n plays a role in organellar shaping and positioning as well as in cytoplas mic deletion and the maintenance of spatial integrity in the mature cell. We conclude with an overview of the current and potential utility of male g ametogenesis as an informative system in approaching fundamental questions relating to cellular differentiation and motility. Characterization of moti lity mutants will elucidate genetic control of structure-function relations hips among cellular components, while biochemical and molecular investigati ons provide crucial data on the mechanism of development. The examination o f spermatogenesis in additional taxa is essential to characterize further d evelopmental variations. Moreover, such studies provide a more comprehensiv e understanding of plant biodiversity at the cellular level and lead to eve n greater phylogenetic resolution from this elegant morphogenetic system.