Dataset Information

Crossover homeostasis in yeast meiosis.

ABSTRACT: Crossovers produced by homologous recombination promote accurate chromosome segregation in meiosis and are controlled such that at least one forms per chromosome pair and multiple crossovers are widely spaced. Recombination initiates with an excess number of double-strand breaks made by Spo11 protein. Thus, crossover control involves a decision by which some breaks give crossovers while others follow a predominantly noncrossover pathway(s). To understand this decision, we examined recombination when breaks are reduced in yeast spo11 hypomorphs. We find that crossover levels tend to be maintained at the expense of noncrossovers and that genomic loci differ in expression of this "crossover homeostasis." These findings define a previously unsuspected manifestation of crossover control, i.e., that the crossover/noncrossover ratio can change to maintain crossovers. Our results distinguish between existing models of crossover control and support the hypothesis that an obligate crossover is a genetically programmed event tied to crossover interference.

SUBMITTER: Martini E

PROVIDER: S-EPMC1949389 | biostudies-literature | 2006 Jul

REPOSITORIES: biostudies-literature

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Crossover homeostasis in yeast meiosis.

Martini Emmanuelle E Diaz Robert L RL Hunter Neil N Keeney Scott S

Cell 20060701 2

Crossovers produced by homologous recombination promote accurate chromosome segregation in meiosis and are controlled such that at least one forms per chromosome pair and multiple crossovers are widely spaced. Recombination initiates with an excess number of double-strand breaks made by Spo11 protein. Thus, crossover control involves a decision by which some breaks give crossovers while others follow a predominantly noncrossover pathway(s). To understand this decision, we examined recombination ...[more]

PMID: 16873061

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Project description:Accurate chromosome segregation during meiosis relies on the presence of crossover events distributed among all chromosomes. MutS? and MutL? 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 MutS?-MutL? crossovers, but whether the assembled SC structure per se is required for MutS?-MutL?-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 MutS? and MutL?-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 (MutS?)-independent. This separation-of-function version of Zip1 thus reveals that neither assembled SC nor MutS? 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 MutL? to preferentially promote resolution of MutS?-associated recombination intermediates.

Dataset Information

Crossover homeostasis in yeast meiosis.

Publications

Crossover homeostasis in yeast meiosis.

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