Crosstalk between cohesins and axis proteins determines meiotic chromosome architecture in Sordaria macrospora

Faithful chromosome segregation during meiosis requires the coordinated action of cohesin complexes and chromosome axis proteins. How these factors interact and communicate along chromosome axes, especially during meiotic prophase I, remains however, only partially understood. We therefore investigated the functional interplay between the cohesin components and regulators (Rad21, Rec8, Wapl, Sororin, Spo76/Pds5) and two meiosis-specific axis proteins Red1 and Hop1. Analysis of multiple combinations of their corresponding null mutants and of their genetic-epistasis interactions in the fungus Sordaria macrospora revealed a hierarchical regulatory network for their recruitment and releasing. This work uncovers an unexpected role of axis proteins Red1 and Hop1, that together with Sororin, provide stage-specific protection of Spo76/Pds5 against Wapl-mediated release. Furthermore, we identify that Spo76/Pds5 is the main target of Wapl and acts as a central guardian of kleisin stability against Slx8/STUbL-dependent proteasomal degradation. Together, our findings show that dynamic crosstalk between axis proteins and cohesins is crucial to preserve axis integrity and to ensure accurate meiotic progression.