Cargando…

Lessons from the meiotic recombination landscape of the ZMM deficient budding yeast Lachancea waltii

Meiotic recombination is a driving force for genome evolution, deeply characterized in a few model species, notably in the budding yeast Saccharomyces cerevisiae. Interestingly, Zip2, Zip3, Zip4, Spo16, Msh4, and Msh5, members of the so-called ZMM pathway that implements the interfering meiotic cros...

Descripción completa

Detalles Bibliográficos
Autores principales: Dutreux, Fabien, Dutta, Abhishek, Peltier, Emilien, Bibi-Triki, Sabrina, Friedrich, Anne, Llorente, Bertrand, Schacherer, Joseph
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9851511/
https://www.ncbi.nlm.nih.gov/pubmed/36608114
http://dx.doi.org/10.1371/journal.pgen.1010592
_version_ 1784872413133012992
author Dutreux, Fabien
Dutta, Abhishek
Peltier, Emilien
Bibi-Triki, Sabrina
Friedrich, Anne
Llorente, Bertrand
Schacherer, Joseph
author_facet Dutreux, Fabien
Dutta, Abhishek
Peltier, Emilien
Bibi-Triki, Sabrina
Friedrich, Anne
Llorente, Bertrand
Schacherer, Joseph
author_sort Dutreux, Fabien
collection PubMed
description Meiotic recombination is a driving force for genome evolution, deeply characterized in a few model species, notably in the budding yeast Saccharomyces cerevisiae. Interestingly, Zip2, Zip3, Zip4, Spo16, Msh4, and Msh5, members of the so-called ZMM pathway that implements the interfering meiotic crossover pathway in S. cerevisiae, have been lost in Lachancea yeast species after the divergence of Lachancea kluyveri from the rest of the clade. In this context, after investigating meiosis in L. kluyveri, we determined the meiotic recombination landscape of Lachancea waltii. Attempts to generate diploid strains with fully hybrid genomes invariably resulted in strains with frequent whole-chromosome aneuploidy and multiple extended regions of loss of heterozygosity (LOH), which mechanistic origin is so far unclear. Despite the lack of multiple ZMM pro-crossover factors in L. waltii, numbers of crossovers and noncrossovers per meiosis were higher than in L. kluyveri but lower than in S. cerevisiae, for comparable genome sizes. Similar to L. kluyveri but opposite to S. cerevisiae, L. waltii exhibits an elevated frequency of zero-crossover bivalents. Lengths of gene conversion tracts for both crossovers and non-crossovers in L. waltii were comparable to those observed in S. cerevisiae and shorter than in L. kluyveri despite the lack of Mlh2, a factor limiting conversion tract size in S. cerevisiae. L. waltii recombination hotspots were not shared with either S. cerevisiae or L. kluyveri, showing that meiotic recombination hotspots can evolve at a rather limited evolutionary scale within budding yeasts. Finally, L. waltii crossover interference was reduced relative to S. cerevisiae, with interference being detected only in the 25 kb distance range. Detection of positive inference only at short distance scales in the absence of multiple ZMM factors required for interference-sensitive crossovers in other systems likely reflects interference between early recombination precursors such as DSBs.
format Online
Article
Text
id pubmed-9851511
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-98515112023-01-20 Lessons from the meiotic recombination landscape of the ZMM deficient budding yeast Lachancea waltii Dutreux, Fabien Dutta, Abhishek Peltier, Emilien Bibi-Triki, Sabrina Friedrich, Anne Llorente, Bertrand Schacherer, Joseph PLoS Genet Research Article Meiotic recombination is a driving force for genome evolution, deeply characterized in a few model species, notably in the budding yeast Saccharomyces cerevisiae. Interestingly, Zip2, Zip3, Zip4, Spo16, Msh4, and Msh5, members of the so-called ZMM pathway that implements the interfering meiotic crossover pathway in S. cerevisiae, have been lost in Lachancea yeast species after the divergence of Lachancea kluyveri from the rest of the clade. In this context, after investigating meiosis in L. kluyveri, we determined the meiotic recombination landscape of Lachancea waltii. Attempts to generate diploid strains with fully hybrid genomes invariably resulted in strains with frequent whole-chromosome aneuploidy and multiple extended regions of loss of heterozygosity (LOH), which mechanistic origin is so far unclear. Despite the lack of multiple ZMM pro-crossover factors in L. waltii, numbers of crossovers and noncrossovers per meiosis were higher than in L. kluyveri but lower than in S. cerevisiae, for comparable genome sizes. Similar to L. kluyveri but opposite to S. cerevisiae, L. waltii exhibits an elevated frequency of zero-crossover bivalents. Lengths of gene conversion tracts for both crossovers and non-crossovers in L. waltii were comparable to those observed in S. cerevisiae and shorter than in L. kluyveri despite the lack of Mlh2, a factor limiting conversion tract size in S. cerevisiae. L. waltii recombination hotspots were not shared with either S. cerevisiae or L. kluyveri, showing that meiotic recombination hotspots can evolve at a rather limited evolutionary scale within budding yeasts. Finally, L. waltii crossover interference was reduced relative to S. cerevisiae, with interference being detected only in the 25 kb distance range. Detection of positive inference only at short distance scales in the absence of multiple ZMM factors required for interference-sensitive crossovers in other systems likely reflects interference between early recombination precursors such as DSBs. Public Library of Science 2023-01-06 /pmc/articles/PMC9851511/ /pubmed/36608114 http://dx.doi.org/10.1371/journal.pgen.1010592 Text en © 2023 Dutreux et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Dutreux, Fabien
Dutta, Abhishek
Peltier, Emilien
Bibi-Triki, Sabrina
Friedrich, Anne
Llorente, Bertrand
Schacherer, Joseph
Lessons from the meiotic recombination landscape of the ZMM deficient budding yeast Lachancea waltii
title Lessons from the meiotic recombination landscape of the ZMM deficient budding yeast Lachancea waltii
title_full Lessons from the meiotic recombination landscape of the ZMM deficient budding yeast Lachancea waltii
title_fullStr Lessons from the meiotic recombination landscape of the ZMM deficient budding yeast Lachancea waltii
title_full_unstemmed Lessons from the meiotic recombination landscape of the ZMM deficient budding yeast Lachancea waltii
title_short Lessons from the meiotic recombination landscape of the ZMM deficient budding yeast Lachancea waltii
title_sort lessons from the meiotic recombination landscape of the zmm deficient budding yeast lachancea waltii
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9851511/
https://www.ncbi.nlm.nih.gov/pubmed/36608114
http://dx.doi.org/10.1371/journal.pgen.1010592
work_keys_str_mv AT dutreuxfabien lessonsfromthemeioticrecombinationlandscapeofthezmmdeficientbuddingyeastlachanceawaltii
AT duttaabhishek lessonsfromthemeioticrecombinationlandscapeofthezmmdeficientbuddingyeastlachanceawaltii
AT peltieremilien lessonsfromthemeioticrecombinationlandscapeofthezmmdeficientbuddingyeastlachanceawaltii
AT bibitrikisabrina lessonsfromthemeioticrecombinationlandscapeofthezmmdeficientbuddingyeastlachanceawaltii
AT friedrichanne lessonsfromthemeioticrecombinationlandscapeofthezmmdeficientbuddingyeastlachanceawaltii
AT llorentebertrand lessonsfromthemeioticrecombinationlandscapeofthezmmdeficientbuddingyeastlachanceawaltii
AT schachererjoseph lessonsfromthemeioticrecombinationlandscapeofthezmmdeficientbuddingyeastlachanceawaltii