m⁶<scp>A</scp> demethylase <scp>O</scp>s<scp>ALKBH</scp>5 is required for double‐strand break formation and repair by affecting m<scp>RNA</scp> stability in rice meiosis

Abstract

Summary N 6 ‐methyladenosine (m 6 A) RNA modification is the most prevalent messenger RNA (mRNA) modification in eukaryotes and plays critical roles in the regulation of gene expression. m 6 A is a reversible RNA modification that is deposited by methyltransferases (writers) and removed by demethylases (erasers). The function of m 6 A erasers in plants is highly diversified and their roles in cereal crops, especially in reproductive development essential for crop yield, are largely unknown. Here, we demonstrate that rice OsALKBH5 acts as an m 6 A demethylase required for the normal progression of male meiosis. OsALKBH5 is a nucleo‐cytoplasmic protein, highly enriched in rice anthers during meiosis, that associates with P‐bodies and exon junction complexes, suggesting that it is involved in regulating mRNA processing and abundance. Mutations of OsALKBH5 cause reduced double‐strand break (DSB) formation, severe defects in DSB repair, and delayed meiotic progression, leading to complete male sterility. Transcriptome analysis and m 6 A profiling indicate that OsALKBH5‐mediated m 6 A demethylation stabilizes the mRNA level of multiple meiotic genes directly or indirectly, including several genes that regulate DSB formation and repair. Our study reveals the indispensable role of m 6 A metabolism in post‐transcriptional regulation of meiotic progression in rice.