Motile Gametes of Land Plants: Diversity,Development, and Evolution

Referee: Professor Jeffrey Duckett, School of Biological Sciences, Queen Mary and Westfield College, University of London, Mile End Road, London, E1 4NS, UK Spermatogenesis is a morphogenetic system in plants that is unparalled in its potential to yield diverse and informative structural and developmental data. The unquestionable homology of terrestrial plant spermatozoids to each other and to gametes of related lineages allows an examination of cellular evolution and provides sound data for phylogenetic analyses. In this review we examine the architecture and ontogeny of motile male gametes among major groups of land plants. We begin with a historical perspective that emphasizes the utility of spermatogenesis in understanding cellular evolution and in determining phylogenetic relationships. A cladistic analysis of data based solely on spermatogenesis and a conceptual phylogeny based on combined morphological and molecular data serve as the basis for the comprehensive discussion of architectural and developmental features of plant spermatozoids. Spermatozoids of green plants have two fundamental architectural designs: biflagellated or multiflagellated. Biflagellated gametes vary among basal archegoniates and charophytes in degree of coiling, position, and substructure 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 staggered basal bodies. Like bryophytes, gametes of most lycophytes are biflagellated; two exceptions are Isoëtes and Phylloglossum, taxa that independently evolved multiflagellated sperm cells with approximately 20 flagella. Developmental information, especially related to the origin and development of the locomotory apparatus, are essential to determine structural homology among 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 include the arrangement of the microtubular cytoskeleton, origin of the locomotory apparatus, and structural details of the basal bodies and multilayered structure. Sperm cell development in archegoniates involves the complete transformation of virtually every cellular component. Crucial to this process are proteinaceous elements of the cytoskeleton. Complex microtubule arrays unique to these cells include the spline, basal bodies, and flagella. The discrete microtubule-organizing centers (MTOCs) that generate these cytoskeletal arrays 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. Actin plays a role in organellar shaping and positioning as well as in cytoplasmic deletion and the maintenance of spatial integrity in the mature cell. We conclude with an overview of the current and potential utility of male gametogenesis as an informative system in approaching fundamental questions relating to cellular differentiation and motility. Characterization of motility mutants will elucidate genetic control of structure-function relationships among cellular components, while biochemical and molecular investigations provide crucial data on the mechanism of development. The examination of spermatogenesis in additional taxa is essential to characterize further developmental variations. Moreover, such studies provide a more comprehensive understanding of plant biodiversity at the cellular level and lead to even greater phylogenetic resolution from this elegant morphogenetic system.