Monopolar orientation of kinetochores at meiosis is enforced by COHESINS and their regulators, CENP-C, and the deSUMOylase SPF2

The first division of meiosis is unique in its capacity to halve the ploidy of the future gametes. To this end, one key innovation compared to mitosis is the monopolar orientation of the pairs of sister kinetochores required for the proper separation of homologs at meiosis I. How monopolar orientation is imposed is unclear and seems to vary in eukaryotes. Here we performed a forward genetic screen in Arabidopsis thaliana, specifically designed to identify the molecular components imposing monopolar orientation, based on mutants ability to restore fertility in spo11 osd1 haploid plants. We show that monopolar orientation involves all four cohesin subunits (REC8, SCC3, SMC1, SMC3), the cohesion establishment factors CTF18 and DCC1, and the cohesin protectors SGO1/2 and PANS1, the inner kinetochore protein CENP-C, and the desumoylase SPF2. The mutants show bipolar orientation of achiasmatic chromosomes, but monopolar orientation is maintained in the presence of crossovers despite splitting of sister kinetochores at metaphase I and reduced levels of cohesin. Taken together, the findings demonstrate that cohesion establishment and protection, kinetochore function, and deSUMOylation, together with crossovers, enforce monopolar orientation in plants and support a cohesion-driven model of kinetochore orientation at meiosis I that is conserved across kingdoms.