In contrast to animals, the plant male germline is established after meiosis in distinctive haploid structures, termed pollen grains. The germline arises by a distinct asymmetric division of the meiotic products . The fates of the resulting vegetative and generative cells are distinct. In contrast to the larger vegetative cell, arrested in the G1 phase of the cell cycle, the smaller generative cell divides once to produce the two male gametes or sperm cells. Sperm cells are delivered to the female gametes by the pollen tube, which develops from the vegetative cell. In spite of recent efforts to understand pollen development , the molecular pathway controlling sperm-cell ontogenesis is unknown. Here, we present the isolation of DUO1, a novel R2R3 MYB gene of Arabidopsis, as the first gene shown to control male gamete formation in plants. DUO1 is specifically expressed in the male germline, and DUO1 protein accumulates in sperm-cell nuclei. Mutations in DUO1 produce a single larger diploid sperm cell unable to perform fertilization. DUO1 appears to be evolutionarily conserved in several plant species and defines a new subfamily of pollen-specific MYB genes.
Male germ line development in flowering plants is initiated with the formation of the generative cell that is the progenitor of the two sperm cells. While structural features of the generative cell are well documented, genetic programs required for generative cell cycle progression are unknown. We describe two novel Arabidopsis (Arabidopsis thaliana) mutants, duo pollen1 (duo1) and duo pollen2 (duo2), in which generative cell division is blocked, resulting in the formation of bicellular pollen grains at anthesis. duo1 and duo2 map to different chromosomes and act gametophytically in a male-specific manner. Both duo mutants progress normally through the first haploid division at pollen mitosis I (PMI) but fail at distinct stages of the generative cell cycle. Mutant generative cells in duo1 pollen fail to enter mitosis at G2-M transition, whereas mutant generative cells in duo2 enter PMII but arrest at prometaphase. In wild-type plants, generative and sperm nuclei enter S phase soon after inception, implying that male gametic cells follow a simple S to M cycle. Mutant generative nuclei in duo1 complete DNA synthesis but bypass PMII and enter an endocycle during pollen maturation. However, mutant generative nuclei in duo2 arrest in prometaphase of PMII with a 2C DNA content. Our results identify two essential gametophytic loci required for progression through different phases of the generative cell cycle, providing the first evidence to our knowledge for genetic regulators of male germ line development in flowering plants.Plant sexual reproduction depends on the timely construction of male and female gametes that are produced by the haploid gametophyte generation. In flowering plants, male gametogenesis is restricted to a simple cell lineage of two cell divisions following meiosis that results in the production of two nonmotile sperm cells. The first division of the microspore at pollen mitosis I (PMI) is asymmetric and gives rise to a large transcriptionally active vegetative cell and a diminutive generative cell with condensed chromatin and fewer organelles. After PMI, the two cells follow different developmental pathways that are characterized by the differential control of the cell cycle and gene expression. Whereas the vegetative cell exits the cell cycle in G1 and differentiates, the generative cell completes a further cell cycle to form the two sperm cells (for review, see Tanaka, 1997;Twell et al., 1998). Although the general pathway leading to sperm cell formation is clear, our knowledge of the genetic and molecular control of generative cell cycle progression and male germ line development is very limited.Gene expression within the male gametes has been explored in some plants. Male gamete specific histones have been identified in isolated generative cells of lily (Lilium longiflorum; Ueda and Tanaka, 1995), and some genes (ERCC1, LGC1, and FtsZ) that are expressed preferentially or specifically in the male gametes have been isolated (Xu et al., 1998(Xu et al., , 1999Mori and Tanaka, 2000). Recently, larg...
Male germline development in angiosperms produces the pair of sperm cells required for double fertilization. A key regulator of this process in Arabidopsis thaliana is the male germline-specific transcription factor DUO POLLEN1 (DUO1) that coordinates germ cell division and gamete specification. Here, we uncover the role of DUO3, a nuclear protein that has a distinct, but overlapping role with DUO1 in male germline development. DUO3 is a conserved protein in land plants and is related to GON-4, a cell lineage regulator of gonadogenesis in Caenorhabditis elegans. Mutant duo3-1 germ cells either fail to divide or show a delay in division, and we show that, unlike DUO1, DUO3 promotes entry into mitosis independent of the G2/M regulator CYCB1;1. We also show that DUO3 is required for the expression of a subset of germline genes under DUO1 control and that like DUO1, DUO3 is essential for sperm cell specification and fertilization. Furthermore, we demonstrate an essential sporophytic role for DUO3 in cell division and embryo patterning. Our findings demonstrate essential developmental roles for DUO3 in cell cycle progression and cell specification in both gametophytic and sporophytic tissues.
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