Absence of chromosome axis protein recruitment prevents meiotic recombination chromosome-wide in the budding yeast Lachancea kluyveri

• 成果类型: Article
• 署名作者: Legrand, Sylvain; Saifudeen, Asma; Vernerey, Julien; Guille, Arnaud; Bignaud, Amaury; Thierry, Agnes; Acquaviva, Laurent; Gaudin, Maxime; Sanchez, Aurore; Johnson, Dominic; Friedrich, Anne; Schacherer, Joseph; Neale, Matthew J.; Borde, Valerie; Koszul, Romain; Llorente, Bertrand
• 署名单位: Institut National de la Sante et de la Recherche Medicale (Inserm); UNICANCER; Institut Paoli-Calmette (IPC); Aix-Marseille Universite; Centre National de la Recherche Scientifique (CNRS); CNRS - National Institute for Biology (INSB); Pasteur Network; Universite Paris Cite; Institut Pasteur Paris; Centre National de la Recherche Scientifique (CNRS); CNRS - National Institute for Biology (INSB); Universite PSL; UNICANCER; Institut Curie; Centre National de la Recherche Scientifique (CNRS); Sorbonne Universite; CNRS - National Institute for Biology (INSB); University of Sussex; Centre National de la Recherche Scientifique (CNRS); CNRS - National Institute for Biology (INSB); Universites de Strasbourg Etablissements Associes; Universite de Strasbourg
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-9561
• DOI: 10.1073/pnas.2312820121
• 发表日期: 2024-03-19
• 关键词: double-strand breaks; sister-chromatid cohesion; molecular-biology; dna-replication; mismatch repair; initiation site; saccharomyces; meiosis; complex; EVOLUTION

摘要

Meiotic recombination shows broad variations across species and along chromosomes and is often suppressed at and around genomic regions determining sexual compatibility such as mating type loci in fungi. Here, we show that the absence of Spo11-DSBs and meiotic recombination on Lakl0C-left, the chromosome arm containing the sex locus of the Lachancea kluyveri budding yeast, results from the absence of recruitment of the two chromosome axis proteins Red1 and Hop1, essential for proper Spo11-DSBs formation. Furthermore, cytological observation of spread pachytene meiotic chromosomes reveals that Lakl0C-left does not undergo synapsis. However, we show that the behavior of Lakl0C-left is independent of its particularly early replication timing and is not accompanied by any peculiar chromosome structure as detectable by Hi - C in this yet poorly studied yeast. Finally, we observed an accumulation of heterozygous mutations on Lakl0C-left and a sexual dimorphism of the haploid meiotic offspring, supporting a direct effect of this absence of meiotic recombination on L. kluyveri genome evolution and fitness. Because suppression of meiotic recombination on sex chromosomes is widely observed across eukaryotes, the mechanism for recombination suppression described here may apply to other species, with the potential to impact sex chromosome evolution. Significance Meiosis is the specialized cell division generating gametes. In most organisms including the extensively studied yeast Saccharomyces cerevisiae , parental homologous chromosomes recombine during meiosis prophase which ensures proper chromosome segregation and shuffles parental genetic information. While recombination is generally suppressed at sex loci, such suppression sometimes extends over entire chromosome arms by unknown mechanisms. Using the poorly studied yeast Lachancea kluyveri , a S. cerevisiae relative, we show that recombination suppression can be mediated over the entire chromosome arm containing the sex locus by the absence of recruitment of proteins essential for recombination initiation. This novel mechanism for recombination suppression affects L. kluyveri genome evolution and fitness, and may apply to other species, with the potential to impact sex chromosome evolution.