Regulation of Fertilization and Early Seed Development Evolutionarily conserved mechanisms of male germline development in flowering plants and animals

Abstract Sexual reproduction is the main reproductive strategy of the overwhelming majority of eukaryotes. This suggests that the last eukaryotic common ancestor was able to reproduce sexually. Sexual reproduction reflects the ability to perform meiosis, and ultimately generating gametes, which are cells that carry recombined half sets of the parental genome and are able to fertilize. These functions have been allocated to a highly specialized cell lineage: the germline. Given its significant evolutionary conservation, it is to be expected that the germline programme shares common molecular bases across extremely divergent eukaryotic species. In the present review, we aim to identify the unifying principles of male germline establishment and development by comparing two very disparate kingdoms: plants and animals. We argue that male meiosis defines two temporally regulated gene expression programmes: the first is required for meiotic commitment, and the second is required for the acquisition of fertilizing ability. Small RNA pathways are a further key communality, ultimately ensuring the epigenetic stability of the information conveyed by the male germline. Male germline establishment and development The life cycle of plants alternates between two morphologically distinct generations: the sporophyte and the gametophytes. During the course of evolution, the sporophytic phase became dominant, with the short-lived gametophytes arising, at the end of ontogeny, within structures on the sporophyte. It is during the development of the gametophytes that the plant germline is specified. Animals also display considerable variation in the timing of germline specification; this lineage can be established during early or late embryogenesis or even throughout adult life, as seen in plants (for a review, see In flowering plants, male gametophytes are formed in specialized reproductive organs of the flower: the anthers. Archesporial cells in the stamen primordium divide periclinally to produce an outer PPC (primary parietal cell) and an inner PSC (primary sporogenous cell) Abbreviations: DCL1, DICER-LIKE1; DUO1, DUO POLLEN1; GCS1, GENERATIVE CELL-SPECIFIC PROTEIN 1; HAP2, HAPLESS2; MGH3, MALE GAMETE-SPECIFIC HISTONE H3 ; MGU, male germ unit; piRNA, Piwi-interacting RNA; PLCζ , phospholipase Cζ ; PMC, pollen mother cell; PM, pollen mitosis; PPC, primary parietal cell; PSC, primary sporogenous cell; SC, sperm cell; SSP, SHORT SUSPENSOR; TE, transposable element; VN, vegetative nucleus. 1 To whom correspondence should be addressed (email jbecker@igc.gulbenkian.pt). PPC differentiates into the tapetum, a sterile nourishing tissue that is essential for the early stages of pollen development. Consecutive divisions of the PSC generate a central mass of microsporocytes, the PMCs (pollen mother cells). PMCs remain interconnected by cytoplasmic bridges, the cytomictic channels. These channels result from the continuity of the inner side of the cytoplasmic membrane (symplast) of neighbouring cells and are believed to be necessary for the subsequent synchronization of PMC development. Such synchronization will regulate meiosis, a process that will ultimately result in the formation of four microspores (for a review, se