Cited by 415Genomics and Chromatin DynamicsChromosomal and Genetic VariationsDNA Repair Mechanisms

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Genetic recombination is directed away from functional genomic elements in mice

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Brick, Kevin, Smagulova, Fatima, Khil, Pavel, Camerini-Otero, R. Daniel, Petukhova, Galina V.·2012·Nature

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Abstract

Genetic recombination occurs during meiosis, the key developmental programme of gametogenesis. Recombination in mammals has been recently linked to the activity of a histone H3 methyltransferase, PR domain containing 9 (PRDM9), the product of the only known speciation-associated gene in mammals. PRDM9 is thought to determine the preferred recombination sites--recombination hotspots--through sequence-specific binding of its highly polymorphic multi-Zn-finger domain. Nevertheless, Prdm9 knockout mice are proficient at initiating recombination. Here we map and analyse the genome-wide distribution of recombination initiation sites in Prdm9 knockout mice and in two mouse strains with different Prdm9 alleles and their F(1) hybrid. We show that PRDM9 determines the positions of practically all hotspots in the mouse genome, with the exception of the pseudo-autosomal region (PAR)--the only area of the genome that undergoes recombination in 100% of cells. Surprisingly, hotspots are still observed in Prdm9 knockout mice, and as in wild type, these hotspots are found at H3 lysine 4 (H3K4) trimethylation marks. However, in the absence of PRDM9, most recombination is initiated at promoters and at other sites of PRDM9-independent H3K4 trimethylation. Such sites are rarely targeted in wild-type mice, indicating an unexpected role of the PRDM9 protein in sequestering the recombination machinery away from gene-promoter regions and other functional genomic elements.

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Reviewer #2 (Public Review): ARID1A governs the silencing of sex-linked transcription during male meiosis in the mouse
(2023) · eLife · doi:10.7554/elife.88024.2.sa1
Reviewer #1 (Public Review): ARID1A governs the silencing of sex-linked transcription during male meiosis in the mouse
(2023) · eLife · doi:10.7554/elife.88024.2.sa2
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Additional file 2 of The histone modification reader ZCWPW1 promotes double-strand break repair by regulating cross-talk of histone modifications and chromatin accessibility at meiotic hotspots
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Additional file 3 of The histone modification reader ZCWPW1 promotes double-strand break repair by regulating cross-talk of histone modifications and chromatin accessibility at meiotic hotspots
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Additional file 1 of The GC-content at the 5′ ends of human protein-coding genes is undergoing mutational decay
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Additional file 1 of Rat PRDM9 shapes recombination landscapes, duration of meiosis, gametogenesis, and age of fertility
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Additional file 3 of The GC-content at the 5′ ends of human protein-coding genes is undergoing mutational decay
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Additional file 1 of Analysis of archaic human haplotypes suggests that 5hmC acts as an epigenetic guide for NCO recombination
Lee, B., Cyrill, S. L., Lee, W., Melchiotti, R., Andiappan, A. K., Poidinger, M., & Rötzschke, O. (2022) · Figshare · doi:10.6084/m9.figshare.20438282
Additional file 1 of The histone modification reader ZCWPW1 promotes double-strand break repair by regulating cross-talk of histone modifications and chromatin accessibility at meiotic hotspots
Yuan, S., Huang, T., Bao, Z., Wang, S., Wu, X., Liu, J., Liu, H., & Chen, Z.-J. (2022) · Figshare · doi:10.6084/m9.figshare.21009546
Additional file 1 of Genetic variation in recombination rate in the pig
Johnsson, M., Whalen, A., Ros-Freixedes, R., Gorjanc, G., Chen, C.-Y., Herring, W. O., de Koning, D.-J., & Hickey, J. M. (2021) · Figshare · doi:10.6084/m9.figshare.14850641
Additional file 4 of The histone modification reader ZCWPW1 promotes double-strand break repair by regulating cross-talk of histone modifications and chromatin accessibility at meiotic hotspots
Yuan, S., Huang, T., Bao, Z., Wang, S., Wu, X., Liu, J., Liu, H., & Chen, Z.-J. (2022) · Figshare · doi:10.6084/m9.figshare.21009555
Additional file 1 of Genetic differentiation and intrinsic genomic features explain variation in recombination hotspots among cocoa tree populations
Schwarzkopf, E. J., Motamayor, J. C., & Cornejo, O. E. (2020) · Figshare · doi:10.6084/m9.figshare.12218657
Additional file 2 of The GC-content at the 5′ ends of human protein-coding genes is undergoing mutational decay
Qiu, Y., Kang, Y. M., Korfmann, C., Pouyet, F., Eckford, A. W., & Palazzo, A. F. (2024) · Figshare · doi:10.6084/m9.figshare.26629997
Rapid evolution of fine-scale recombination during domestication: a perspective from population genomicsPreprint
Liu, Z.-X., Li, M., Ge, X.-H., Wang, K., Si, S., Ge, C.-R., Chen, J., Hu, L.-R., Peng, M., Yin, T.-T., et al. (2026) · eLife · doi:10.7554/elife.109490.1
Rapid evolution of fine-scale recombination during domestication: a perspective from population genomicsPreprint
Liu, Z.-X., Li, M., Ge, X.-H., Wang, K., Si, S., Ge, C.-R., Chen, J., Hu, L.-R., Peng, M., Yin, T.-T., et al. (2026) · eLife · doi:10.7554/elife.109490
A genome-wide atlas of meiotic recombination intermediates reveals distinct modes of DNA repair that direct crossovers away from transcriptionally marked genesPreprint
Henfrey, C., Print, E. H. T., Zhang, G., Hinch, R., Maudlin, I., Moralli, D., Davies, B. L., Donnelly, P., & Hinch, A. G. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.26.714455
Critical roles of MCM8 in meiotic recombination during mouse spermatogenesisPreprint
Surarapu, L. K., Tilton, K., Stritto, M. R. D., Acharya, A., Menendez, A. M., Lu, M., Shaheen, N., Liang, S., Iyer, M., Ćejka, P., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.28.714908
Study of the role of neddylation in the regulation of meiotic recombination
Tagliaro-Jahns, M. (2014) · theses.fr (ABES) · doi:10.70675/3d413e8bz3772z4ba9z8582z8698e585ff46
Rôle de l'activité méthyltransférase de la protéine PRDM9 dans la recombinaison méiotique chez la souris
Diagouraga, B. (2015) · theses.fr (ABES) · doi:10.70675/6992b6c8z7c66z4afbz8a88z34168d0ab438
Meiotic recombination evolution : Prdm9 gene variation and evolution in mice
de Segonzac, D. D. (2016) · theses.fr (ABES) · doi:10.70675/4f23518fz0509z4fa5z96f0zb94275a9db50
Diversité et déterminisme génétique de la recombinaison méiotique chez Saccharomyces cerevisiae
Raffoux, X. (2018) · theses.fr (ABES) · doi:10.70675/4cfc4e3czf3b1z4fa8zaab7z7cc42e359b79
Biochemical properties and regulation of the TopoVI-like complex responsible for the initiation of meiotic recombination
Nore, A. (2018) · theses.fr (ABES) · doi:10.70675/349d15a9za386z43e3za9d4z8b660947d348
Étude de la recombinaison méiotique chez la levure Lachancea kluyveri
Legrand, S. (2020) · theses.fr (ABES) · doi:10.70675/d3548e39z4e8az44a9zafbdz82828e704276
La suppression de Topaz1 perturbe la méiose et l'expression des ARN non-codant longs testiculaires au cours de la spermatogenèse murine.
Chadourne, M. (2021) · theses.fr (ABES) · doi:10.70675/f837cdf2zff4fz48d4zbad1zde5177634ec1
Apport de la recombinaison dans l’optimisation des plans de croisements de blé tendre
Alice, D. D. D. (2021) · doi:10.70675/d642f2a6z68bbz408ez95afz797f18a5d482
Interplay between meiotic crossing-overs and chromosome architecture : role of the meiosis specific complex Zip2-Zip4-Spo16
Pyatnitskaya, A. (2021) · theses.fr (ABES) · doi:10.70675/88aa41c7z2926z475bzad55z97961883fb55

Authors: Brick, K., Smagulova, F., Khil, P., Camerini-Otero, R. D., & Petukhova, G. V.
Affiliations: National Institute of Diabetes and Digestive and Kidney Diseases (US)
Uniformed Services University of the Health Sciences (US)
National Institutes of Health (US)
Corresponding author: Petukhova, Galina V.
ORCID: Brick, Kevin
Smagulova, Fatima
Khil, Pavel
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2012-05
Volume: 485
Issue: 7400
Pages: 642-645
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature11089
PMC: PMC3367396
OpenAlex: W2024459631
Cited by: 414
References: 30
Citations by year: 2026: 19 · 2025: 15 · 2024: 31 · 2023: 31 · 2022: 30 · 2021: 27 · 2020: 28 · 2019: 31 · 2018: 36 · 2017: 33 · 2016: 36 · 2015: 31 · 2014: 32 · 2013: 24 · 2012: 10
FWCI: 12.48
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
HAL (submittedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: National Institutes of Health
National Institute of General Medical Sciences (R01GM084104)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Keywords: PRDM9, meiotic recombination, recombination hotspots, H3K4 trimethylation, promoter targeting, meiosis
MeSH terms: Alleles, Amino Acid Sequence, Animals, Base Sequence, Histones, Meiosis, Methylation, Molecular Sequence Data, Promoter Regions, Genetic, Histone-Lysine N-Methyltransferase, Recombination, Genetic, Genome, Mice, Knockout, Mice, DNA Breaks, Double-Stranded

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Genetic recombination is directed away from functional genomic elements in mice

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