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

Author:

Legrand Sylvain1ORCID,Saifudeen Asma1ORCID,Bordelet Hélène2ORCID,Vernerey Julien1,Guille Arnaud1,Bignaud Amaury2,Thierry Agnès2,Acquaviva Laurent1,Gaudin Maxime1,Sanchez Aurore3,Johnson Dominic4,Friedrich Anne5ORCID,Schacherer Joseph5,Neale Matthew J.4ORCID,Borde Valérie3ORCID,Koszul Romain2ORCID,Llorente Bertrand1ORCID

Affiliation:

1. Centre de recherche en cancérologie de Marseille, CNRS UMR 7258, INSERM, Aix Marseille Université, Institut Paoli Calmettes, Marseille 13009, France

2. Institut Pasteur, CNRS UMR 3525, Université Paris Cité, Unité Régulation Spatiale des Génomes, Paris 75015, France

3. Institut Curie, Paris Sciences and Lettres University, Sorbonne Université, CNRS UMR 3244, Dynamics of Genetic Information, Paris 75005, France

4. Genome Damage and Stability Centre, School of Life Sciences, University of Sussex, Brighton BN1 9RH, United Kingdom

5. Université de Strasbourg, CNRS, Génétique moléculaire, génomique, microbiologie UMR 7156, Strasbourg 67000, France

Abstract

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.

Funder

EC | European Research Council

Wellcome Trust

Human Frontier Science Program

Agence Nationale de la Recherche

Fondation pour la Recherche Médicale

EC | ERC | HORIZON EUROPE European Research Council

Publisher

Proceedings of the National Academy of Sciences

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