PRDM9 drives the location and rapid evolution of recombination hotspots in salmonid fish

• Published in: PLOS Biology
• Main Authors: Raynaud, Marie, Sanna, Paola, Joseph, Julien, Clément, Julie, Imai, Yukiko, Lareyre, Jean-Jacques, Laurent, Audrey, Galtier, Nicolas, Baudat, Frédéric, Duret, Laurent, Gagnaire, Pierre-Alexandre, de Massy, Bernard
• Other Authors: Institut des Sciences de l'Evolution de Montpellier (UMR ISEM), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École Pratique des Hautes Études (EPHE), Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Institut de recherche pour le développement IRD : UR226-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), Institut de génétique humaine (IGH), Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Interactions Hôtes-Pathogènes-Environnements (IHPE), Université de Perpignan Via Domitia (UPVD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), National Institute of Genetics Shizuoka, Japan (NIG), Laboratoire de Physiologie et Génomique des Poissons = Fish Physiology and Genomics Institute (LPGP), Structure Fédérative de Recherche en Biologie et Santé de Rennes (Biosit : Biologie - Santé - Innovation Technologique)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), This project was funded by CNRS (Centre national de la recherche scientifique; https://www.cnrs.fr) and by ANR (Agence nationale de la recherche; https://anr.fr) (HotRec ANR-19-CE12-0019), ANR-19-CE12-0019,HotRec,Origine des points chauds méïotiques PRDM9-dépendants: où, comment et pourquoi recombiner?(2019)
• Format: Article in Journal/Newspaper
• Language: English
• Published: CCSD 2025
• Subjects: [SDV]Life Sciences [q-bio]; Salmo salar
• Online Access: https://hal.inrae.fr/hal-04934911; https://doi.org/10.1371/journal.pbio.3002950

International audience In many eukaryotes, meiotic recombination occurs preferentially at discrete sites, called recombination hotspots. In various lineages, recombination hotspots are located in regions with promoter-like features and are evolutionarily stable. Conversely, in some mammals, hotspots are driven by PRDM9 that targets recombination away from promoters. Paradoxically, PRDM9 induces the self-destruction of its targets and this triggers an ultra-fast evolution of mammalian hotspots. PRDM9 is ancestral to all animals, suggesting a critical importance for the meiotic program, but has been lost in many lineages with surprisingly little effect on meiosis success. However, it is unclear whether the function of PRDM9 described in mammals is shared by other species. To investigate this, we analyzed the recombination landscape of several salmonids, the genome of which harbors one full-length PRDM9 and several truncated paralogs. We identified recombination initiation sites in Oncorhynchus mykiss by mapping meiotic DNA double-strand breaks (DSBs). We found that DSBs clustered at hotspots positioned away from promoters, enriched for the H3K4me3 and H3K36me3 and the location of which depended on the genotype of full-length Prdm9 . We observed a high level of polymorphism in the zinc finger domain of full-length Prdm9 , indicating diversification driven by positive selection. Moreover, population-scaled recombination maps in O . mykiss , Oncorhynchus kisutch and Salmo salar revealed a rapid turnover of recombination hotspots caused by PRDM9 target motif erosion. Our results imply that PRDM9 function is conserved across vertebrates and that the peculiar evolutionary runaway caused by PRDM9 has been active for several hundred million years.