Cohesin and its regulation promote monopolar kinetochore orientation at meiosis I in Arabidopsis

Authors:

Dipesh-Kumar Singh, Alexander Mahlandt, Stephanie Durand, Sylvie Jolivet, Birgit Walkemeier, Christelle Taochy, Victor Solier, Maria Derkacheva, Imran Siddiqi, Laurence Cromer, Raphael Mercier

Keywords:

meiosis; kinetochore; centromere; monopolar co-orientation; cohesion; deSUMOylase; CENP-C; Shugoshin; Arabidopsis

Abstract:

The first division of meiosis is unique in its capacity to halve the ploidy of future gametes. To this end, one key innovation compared with 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, and SMC3), the cohesion establishment factors CTF18 and DCC1, the cohesin protectors SGO1/2 and PATRONUS (PANS1), the inner kinetochore protein CENP-C, and the deSUMOylase SUMO PROTEASE RELATED TO FERTILITY 2 (SPF2). The mutants show bipolar orientation of achiasmatic chromosomes; however, monopolar orientation is maintained in the presence of crossovers, despite most of them displaying the splitting of sister kinetochores and reduced levels of cohesin at metaphase I. Taken together, the findings demonstrate that cohesion establishment and maintenance, kinetochore function, and deSUMOylation, together with crossovers, promote monopolar orientation in plants and support a cohesion-driven model of kinetochore orientation at meiosis I that is conserved across kingdoms.

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