Suppression of meiotic double-strand break formation in somatic cells by DREAM factors TCX5/6 maintains genome stability

Abstract

Meiotic recombination in reproductive cells is initiated by DNA double-strand breaks (DSBs) and requires the expression of meiosis-specific genes, yet how the transcription of those genes is regulated in either meiotic or somatic cells remains unclear. Here, using a representative meiosis-specific DMC1 gene promoter as a bait, we identified two DREAM factors TCX5 and TCX6 required for direct repression of DMC1 in somatic cells. Transcriptomic analyses show broad ectopic up-regulation of meiotic genes in tcx5/6 leaves . Consistently, tcx5/6 somatic cells form DSBs and exhibit hypersensitivity to DNA damage compared to wild type. Further genetic analyses reveal that SPO11-1 is dispensable for ectopic meiotic gene activation but essential for the DNA damage response in tcx5/6 somatic cells. Last, we demonstrated that TCX5/6 repress meiotic gene expression through H3K4me3 modification. This finding uncovers an unexpected mechanism for suppressing meiotic recombination in somatic cells, thus preventing genetic diversity and genome instability in organisms.