Separable Crossover-Promoting and Crossover-Constraining Aspects of Zip1 Activity during Budding Yeast Meiosis.
Separable Crossover-Promoting and Crossover-Constraining Aspects of Zip1 Activity during Budding Yeast Meiosis.
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DOI：
10.1371/journal.pgen.1005335
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发表时间：
2015-06
期刊：
影响因子：
4.5
通讯作者：
MacQueen AJ
中科院分区：
文献类型：
--
作者：
Voelkel-Meiman K;Johnston C;Thappeta Y;Subramanian VV;Hochwagen A;MacQueen AJ
Accurate chromosome segregation during meiosis relies on the presence of crossover events distributed among all chromosomes. MutSγ and MutLγ homologs (Msh4/5 and Mlh1/3) facilitate the formation of a prominent group of meiotic crossovers that mature within the context of an elaborate chromosomal structure called the synaptonemal complex (SC). SC proteins are required for intermediate steps in the formation of MutSγ-MutLγ crossovers, but whether the assembled SC structure per se is required for MutSγ-MutLγ-dependent crossover recombination events is unknown. Here we describe an interspecies complementation experiment that reveals that the mature SC is dispensable for the formation of Mlh3-dependent crossovers in budding yeast. Zip1 forms a major structural component of the budding yeast SC, and is also required for MutSγ and MutLγ-dependent crossover formation. Kluyveromyces lactis ZIP1 expressed in place of Saccharomyces cerevisiae ZIP1 in S. cerevisiae cells fails to support SC assembly (synapsis) but promotes wild-type crossover levels in those nuclei that progress to form spores. While stable, full-length SC does not assemble in S. cerevisiae cells expressing K. lactis ZIP1, aggregates of K. lactis Zip1 displayed by S. cerevisiae meiotic nuclei are decorated with SC-associated proteins, and K. lactis Zip1 promotes the SUMOylation of the SC central element protein Ecm11, suggesting that K. lactis Zip1 functionally interfaces with components of the S. cerevisiae synapsis machinery. Moreover, K. lactis Zip1-mediated crossovers rely on S. cerevisiae synapsis initiation proteins Zip3, Zip4, Spo16, as well as the Mlh3 protein, as do the crossovers mediated by S. cerevisiae Zip1. Surprisingly, however, K. lactis Zip1-mediated crossovers are largely Msh4/Msh5 (MutSγ)-independent. This separation-of-function version of Zip1 thus reveals that neither assembled SC nor MutSγ is required for Mlh3-dependent crossover formation per se in budding yeast. Our data suggest that features of S. cerevisiae Zip1 or of the assembled SC in S. cerevisiae normally constrain MutLγ to preferentially promote resolution of MutSγ-associated recombination intermediates. At the heart of reproductive cell formation is a nuclear division process (meiosis) whereby homologous chromosomes segregate from one another. Meiotic partner chromosomes establish exclusive associations via a patterned distribution of crossover recombination events. During the maturation of recombination intermediates into crossovers, homologous axes are aligned in the context of a striking proteinaceous structure, the synaptonemal complex (SC). While genetic data link the SC with crossovers, it is unclear whether the mature SC structure facilitates crossover formation. Here we describe an interspecies complementation experiment in which we replace the S. cerevisiae version of an SC structural protein with an ancestrally related version from K. lactis. Our experiment reveals that, while SC proteins are required, mature full-length SC is dispensable for the formation of SC-associated crossovers in budding yeast. We furthermore discovered that most, but not all, members of a conserved meiotic crossover pathway are required for the crossovers that form in this interspecies context. Our findings strengthen the notion that a primary function of many SC proteins is to facilitate crossover recombination, independent of a role in building the larger SC structure. Furthermore, these data suggest that during normal meiosis in S. cerevisiae the assembled SC may act to functionally couple key crossover recombination proteins to one another.
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