Abstract
Mitosis and meiosis both rely on cohesin, which embraces the sister chromatids and plays a crucial role for the faithful distribution of chromosomes to daughter cells. Prior to the cleavage by Separase at anaphase onset, cohesin is largely removed from chromosomes by the non-proteolytic action of WINGS APART-LIKE (WAPL), a mechanism referred to as the prophase pathway. To prevent the premature loss of sister chromatid cohesion, WAPL is inhibited in early mitosis by Sororin. However, Sororin homologs have only been found to function as WAPL inhibitors during mitosis in vertebrates and Drosophila. Here we show that SWITCH 1/DYAD defines a WAPL antagonist that acts in meiosis of Arabidopsis. Crucially, SWI1 becomes dispensable for sister chromatid cohesion in the absence of WAPL. Despite the lack of any sequence similarities, we found that SWI1 is regulated and functions in a similar manner as Sororin hence likely representing a case of convergent molecular evolution across the eukaryotic kingdom.
Highlights
Mitosis and meiosis both rely on cohesin, which embraces the sister chromatids and plays a crucial role for the faithful distribution of chromosomes to daughter cells
The cohesin complex is highly conserved in the eukaryotic kingdom with homologs present from animals to plants comprising four core subunits: SMC1 and SMC3, two ATPases that belong to the family of structural maintenance of chromosomes (SMC) proteins, the heat-repeat domain protein SCC3/SA and one α-kleisin component RAD21/SCC1, which is replaced in meiosis by REC8/SYN1
We observed that the majority of cohesin (~90%) in the wildtype, but not in the previously described wapl[1] wapl[2] double mutant[11], is already largely released from chromatin prior to anaphase I indicating that the impact of the WAPLdependent prophase pathway on cohesin removal is very strong in male meiosis of Arabidopsis (Fig. 1a–c; Supplementary Movies 1 and 2)
Summary
Mitosis and meiosis both rely on cohesin, which embraces the sister chromatids and plays a crucial role for the faithful distribution of chromosomes to daughter cells. To prevent the premature loss of sister chromatid cohesion, WAPL is inhibited in early mitosis by Sororin. The cohesin complex is crucial for genome stability, DNA repair, chromatin structure organization, and gene expression[1,2,3,4]. Sister chromatid cohesion is established in the subsequent S-phase and regulated by several cohesin accessory proteins, including the PRECOCIOUS DISSOCIATION OF SISTER 5 (PDS5) and WINGS APART-LIKE (WAPL)[5,6,7]. Cohesin is largely protected by the ShugoshinPP2A complex[15,16] This centromeric cohesin is released by a Separase-dependent proteolytic cleavage of the kleisin subunit RAD21/REC8, thereby allowing the separation of sister chromatids at anaphase onset (anaphase II in meiosis). An ortholog of Sororin, named Dalmatian, was found in Drosophila, which exert both Sororin’s cohesin stabilizing and Shugoshin’s cohesin protecting functions in mitosis[20]
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