Abstract
Meiosis produces haploid cells essential for sexual reproduction. In yeast, entry into meiosis activates transcription factors which trigger a transcriptional cascade that results in sequential co-expression of early, middle and late meiotic genes. However, these factors are not conserved, and the factors and regulatory mechanisms that ensure proper meiotic gene expression in multicellular eukaryotes are poorly understood. Here, we report that DUET/MMD1, a PHD finger protein essential for Arabidopsis male meiosis, functions as a transcriptional regulator in plant meiosis. We find that DUET-PHD binds H3K4me2 in vitro, and show that this interaction is critical for function during meiosis. We also show that DUET is required for proper microtubule organization during meiosis II, independently of its function in meiosis I. Remarkably, DUET protein shows stage-specific expression, confined to diplotene. We identify two genes TDM1 and JAS with critical functions in cell cycle transitions and spindle organization in male meiosis, as DUET targets, with TDM1 being a direct target. Thus, DUET is required to regulate microtubule organization and cell cycle transitions during male meiosis, and functions as a direct transcription activator of the meiotic gene TDM1. Expression profiling showed reduced expression of a subset comprising about 12% of a known set of meiosis preferred genes in the duet mutant. Our results reveal the action of DUET as a transcriptional regulator during male meiosis in plants, and suggest that transcription of meiotic genes is under stagewise control in plants as in yeast.
Highlights
Reproductive development in sexual organisms culminates in the production of highly specialized haploid cells, the gametes, which fuse to produce the zygote
We further show by chromatin immunoprecipitation experiments (ChIP) that DUET binds THREE DIVISION MUTANT 1 (TDM1) promoter, indicating that TDM1 is a direct target of DUET
Our results reveal that DUET functions as a transcriptional regulator during male meiosis in Arabidopsis, and that binding of its Plant Homeo Domain (PHD) finger to H3K4me2 is critical for function
Summary
Reproductive development in sexual organisms culminates in the production of highly specialized haploid cells, the gametes, which fuse to produce the zygote. An essential event in the production of gametes is meiosis, which is directly responsible for producing haploid cells. Coordination of meiotic events is essential for successful production of haploid daughter cells. Temporal control of meiotic gene expression plays a critical part in coordinating meiotic events with meiotic progression. Entry into meiosis in yeast triggers a transcriptional cascade resulting in sequential expression of meiotic genes. In S. cerevisiae, entry into meiosis activates Ime, a transcription factor that is responsible for expression of early genes that are required for premeiotic S-phase, synapsis and recombination. Among ImeI targets, Ndt is a transcription factor that activates middle genes, which are required for progression through meiotic divisions and spore formation, followed by late genes which control spore development [1]. The key transcription factors Ste and Mei are not homologues of their S. cerevisiae counterparts ImeI and Ndt respectively, indicating poor conservation of these factors even though the transcriptional cascades they control are conserved [2]
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