Histone H3 modifications are widely reprogrammed during male meiosis I in rice dependently on MEL1 Argonaute protein

Abstract

Roles of epigenetic mechanisms including small RNA-mediated silencing in plant meiosis are largely remained unclear, despite of their importance in plant reproduction. This study unveiled that rice chromosomes were reprogrammed during premeiosis-to-meiosis transition in pollen mohter cells (PMCs). This large-scale meiotic chromosome reprogramming (LMR) continued throughout meiosis I, in which H3 lysine-9 dimethylation (H3K9me2) was increased, and H3K9 acetylation and H3 serine-10 phosphorylation were decreased broadly, as accompanying immunostaining pattern shift of RNA polymerase II. LMR occurred dependently on a rice Argonaute protein, MEIOSIS ARRESTED AT LEPTOTENE1 (MEL1), which is specifically expressed in germ cells prior to meiosis, because LMR was depleted severely in mel1 mutant anthers. Pivotal meiotic events, such as pre-synaptic centromere association, DNA double-strand break initiation, and synapsis of homologous chromosomes, were also disrupted in the mutant. Interestingly, opposed to the LMR loss in most chromosomal regions, aberrant meiotic protein loading and hyper H3K9me2 accumulation emerged on the nucleolar organizing region in the mel1 PMCs. These results suggest that MEL1 plays important roles in epigenetic LMR to promote faithful homologous recombination and synapsis in rice meiosis.