title: The synaptonemal complex is assembled by a polySUMOylation-driven feedback mechanism in yeast.
abstract: During meiotic prophase I, proteinaceous structures called synaptonemal complexes (SCs) connect homologous chromosomes along their lengths via polymeric arrays of transverse filaments (TFs). Thus, control of TF polymerization is central to SC formation. Using budding yeast, we show that efficiency of TF polymerization closely correlates with the extent of SUMO conjugation to Ecm11, a component of SCs. HyperSUMOylation of Ecm11 leads to highly aggregative TFs, causing frequent assembly of extrachromosomal structures. In contrast, hypoSUMOylation leads to discontinuous, fragmented SCs, indicative of defective TF polymerization. We further show that the N terminus of the yeast TF, Zip1, serves as an activator for Ecm11 SUMOylation. Coexpression of the Zip1 N terminus and Gmc2, a binding partner of Ecm11, is sufficient to induce robust polySUMOylation of Ecm11 in nonmeiotic cells. Because TF assembly is mediated through N-terminal head-to-head associations, our results suggest that mutual activation between TF assembly and Ecm11 polySUMOylation acts as a positive feedback loop that underpins SC assembly.
authors.affiliation: Genome Damage and Stability Centre, Life Sciences, University of Sussex, Brighton BN19RQ, England, UK.
authors.forename: Wing-Kit
authors.initials: WK
authors.lastname: Leung
authors.affiliation: Genome Damage and Stability Centre, Life Sciences, University of Sussex, Brighton BN19RQ, England, UK.
authors.forename: Neil
authors.initials: N
authors.lastname: Humphryes
authors.affiliation: Genome Damage and Stability Centre, Life Sciences, University of Sussex, Brighton BN19RQ, England, UK.
authors.forename: Negar
authors.initials: N
authors.lastname: Afshar
authors.affiliation: Genome Damage and Stability Centre, Life Sciences, University of Sussex, Brighton BN19RQ, England, UK.
authors.forename: Bilge
authors.initials: B
authors.lastname: Argunhan
authors.affiliation: Genome Damage and Stability Centre, Life Sciences, University of Sussex, Brighton BN19RQ, England, UK.
authors.forename: Yaroslav
authors.initials: Y
authors.lastname: Terentyev
authors.affiliation: National Institute for Basic Biology, National Institutes of Natural Sciences, Myodaiji, Okazaki, Aichi 444-8585, Japan.
authors.forename: Tomomi
authors.initials: T
authors.lastname: Tsubouchi
authors.affiliation: Genome Damage and Stability Centre, Life Sciences, University of Sussex, Brighton BN19RQ, England, UK.
authors.forename: Hideo
authors.initials: H
authors.lastname: Tsubouchi
mesh_terms: D018797:Cell Cycle Proteins / Q000378:metabolism; D010450:Endopeptidases / Q000378:metabolism; D025461:Feedback, Physiological; D005656:Fungal Proteins / Q000378:metabolism*; D009687:Nuclear Proteins / Q000378:metabolism; D054730:Protein Interaction Domains and Motifs; D055503:Protein Multimerization; D004718:Saccharomycetales / Q000378:metabolism*; D058207:Sumoylation; D013573:Synaptonemal Complex / Q000378:metabolism*
chemical_list: D018797:Cell Cycle Proteins; D005656:Fungal Proteins; D009687:Nuclear Proteins; D010450:Endopeptidases