CYB-4/CDK-1 coordinates timing of meiotic entry, chromosome morphogenesis and oocyte maturation in C. elegans

Abstract

Meiotic chromosome segregation requires the earlier coordination of chromosome morphogenesis with cell-cycle progression. In C. elegans, the remodeling of chromosomes in preparation for the meiotic divisions and oocyte maturation is regulated by the master cell-cycle regulator cyclin-dependent kinase 1 (CDK-1). Here, we identify CYB-4 as a meiosis-specific B-type cyclin that is required for CDK-1-dependent functions in meiotic prophase. In a genetic suppressor analysis of a mutant defective in chromosome axis assembly, we isolated a null allele that revealed a function for CYB-4 in regulating chromosome structure at two key prophase transitions. Loss of CYB-4 first delays meiotic entry and the onset of chromosome axis formation, and at pachytene exit delays chromatin condensation, bivalent remodeling, and oocyte maturation. The defects in timely CO formation and bivalent packaging that accompany these delays are ultimately resolved before prophase exit, indicating that CYB-4 is required for the scheduling of events rather than if they occur. Together, our findings provide evidence that CDK-1 activity during meiotic prophase is defined by CYB-4 and support a model in which CYB-4/CDK-1 are essential for the sharp transitions at prophase entry and pachytene exit that coordinate chromosome morphogenesis with meiotic progression.