KNUCKLES promotes meiotic cell-cycle progression by directly repressing the expression of KRP1 and KRP3 to ensure male fertility

Meiosis is an essential process for sexual reproduction in most eukaryotes. Unlike mitosis, the specific cell cycle regulation for meiotic progression control is elusive. As the terminator for floral meristem activity and carpel development, loss function of the transcriptional repressor KNUCKLES (KNU) leads to male sterility in Arabidopsis, but the detailed regulatory mechanism remains unknown. Here, we find that during anther development, KNU specifically localizes in meiocytes and mutating KNU disrupts the meiotic progression with relatively more cells in meiotic prophase I, thus undergoing apoptosis. Transcriptome analysis shows that the numerous genes related to meiosis were down-regulated in knu-2 meiocytes. Further, we demonstrate that KNU can directly repress two cell cycle inhibitors of INTERACTOR/INHIBITOR OF CDK 1/KIP-RELATED PROTEIN 1 (ICK1/KRP1) and KRP3. Knockout of either KRP1 or KRP3 in knu-2 background largely rescues the knu-2 defects in male meiosis and fertility, suggesting that KNU modulates male meiotic progression and fertility via likely repressing KRP1 and KRP3 in cell cycle dependent manner. Taken together, our findings uncover that KNU is a “stabilizer” of cell-cycle progression for male meiotic progression and could be potentially applied as a candidate gene for genetic improvement for crops.