Cohesin ring gates are specialized for meiotic cell division

Cohesin is a ring complex closed with structural maintenance of chromosome 1 (SMC-1), SMC-3, and a kleisin subunit, mediating sister chromatid cohesion in mitosis and meiosis. Kleisin N- and C-terminal domains interact with SMC-3 and SMC-1, forming two distinct cohesin gates. Whether these gates are specialized for mitosis and meiosis remains elusive. Here, we create Caenorhabditis elegans mutants that express chimeric proteins swapping N- and C-terminal domains between different kleisins to investigate how these gates are specialized for different cell division programs. Replacing the meiotic REC-8 N-terminus with that of a cell division-unrelated kleisin COH-1 or the mitotic kleisin sister chromatid cohesion protein 1 (SCC-1) disrupts inter-sister chromatid cohesion and causes severe meiotic defects. Swapping the REC-8 C-terminus with that of COH-1 or SCC-1 largely retains the meiotic functions of REC-8 but causes age-related chromosome abnormalities. A specialized C-terminus is also required for the functions of SCC-1. Furthermore, point mutations in the REC-8 C-terminus cause severe meiotic defects without impairing the SMC-1-kleisin interaction, suggesting an integrated SMC-1-kleisin gate. These findings suggest the requirements for specialized cohesin gates in different biological processes.