Intermediate evolutionary state of motile sperm and pollen tubes in the extant gymnosperm Cycas revoluta

Résumé fourni par la source

Evolutionary transitions in land plant fertilization from zooidogamy to siphonogamy were characterized by transformations of male reproductive cells. Basal land plants such as bryophytes and pteridophytes have motile sperm, whereas most seed plants have nonmotile sperm, delivered by a pollen tube. Despite being seed plants, gymnosperm cycads and ginkgo uniquely form highly multiflagellated and large motile sperm within pollen tubes. However, the evolutionary state of these male reproductive cells remains unknown. We clarified the gene expression profiles of Cycas revoluta pollen tubes and motile sperm swimming toward female reproductive cells. Male cycad cells expressed fewer genes associated with transcription, translation, and related processes, which is consistent across land plants. We compared the distinctive orthologous groups (OGs) of the genes specifically expressed in sperm and pollen tubes with those in other plants. Cycad pollen tubes shared several OGs with angiosperms but possessed significantly fewer gene copies and lacked cell wall remodeling and plasma membrane-localized receptor genes that contribute to rapid and guided growth. The growth mechanism of cycad pollen tubes might be largely different from angiosperm pollen tubes. In contrast, despite their morphological uniqueness, cycad sperm shared representative OGs with angiosperm sperm cells to the same extent as egg cells. In addition, a sperm-specific histone variant may contribute to transcriptional regulation via chromatin condensation like other male gametes. As an extant gymnosperm that retains zooidogamy with pollen tubes, the cycad represents a molecular intermediate state in the transition from zooidogamy to siphonogamy, providing insight into the evolution of land plant fertilization.

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