Telomere bouquet formation, a highly conserved meiotic event, plays an important role in homologous pairing and therefore progression of meiosis; however, the underlying molecular mechanism remains largely unknown. Here, we identified ZYGOTENE1 (ZYGO1), a novel F-box protein in rice (Oryza sativa), and verified its essential role in bouquet formation during early meiosis. In zygo1 mutants, zygotene chromosome aggregation and telomere clustering failed to occur. The suppressed telomere clustering in homologous pairing aberration in rice meiosis1 (pair1) zygo1 and rice completion of meiotic recombination (Oscom1) zygo1 double mutants, together with the altered localization of OsSAD1 (a SUN protein associated with the nuclear envelope) in zygo1, showed that ZYGO1 has a significant function in bouquet formation. In addition, the interaction between ZYGO1 and rice SKP1-like protein 1 suggested that ZYGO1 might modulate bouquet formation as a component of the SKP1-Cullin1-F-box complex. Although double-strand break formation and early recombination element installation occurred normally, zygo1 mutants showed defects in full-length pairing and synaptonemal complex assembly. Furthermore, crossover (CO) formation was disturbed, and foci of Human enhancer of invasion 10 were restricted to the partially synapsed chromosome regions, indicating that CO reduction might be caused by the failure of full-length chromosome alignment in zygo1 Therefore, we propose that ZYGO1 mediates bouquet formation to efficiently promote homolog pairing, synapsis, and CO formation in rice meiosis.
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