Hybrid Sterility Locus on Chromosome X Controls Meiotic Recombination Rate in Mouse
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
27104744
PubMed Central
PMC4841592
DOI
10.1371/journal.pgen.1005906
PII: PGENETICS-D-15-02438
Knihovny.cz E-zdroje
- MeSH
- chromozom X * MeSH
- genetická vazba MeSH
- histonlysin-N-methyltransferasa genetika MeSH
- hybridizace genetická * MeSH
- meióza genetika MeSH
- mužská infertilita genetika MeSH
- myši MeSH
- poškození DNA MeSH
- rekombinace genetická * MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- myši MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- histonlysin-N-methyltransferasa MeSH
- prdm9 protein, mouse MeSH Prohlížeč
Meiotic recombination safeguards proper segregation of homologous chromosomes into gametes, affects genetic variation within species, and contributes to meiotic chromosome recognition, pairing and synapsis. The Prdm9 gene has a dual role, it controls meiotic recombination by determining the genomic position of crossover hotspots and, in infertile hybrids of house mouse subspecies Mus m. musculus (Mmm) and Mus m. domesticus (Mmd), it further functions as the major hybrid sterility gene. In the latter role Prdm9 interacts with the hybrid sterility X 2 (Hstx2) genomic locus on Chromosome X (Chr X) by a still unknown mechanism. Here we investigated the meiotic recombination rate at the genome-wide level and its possible relation to hybrid sterility. Using immunofluorescence microscopy we quantified the foci of MLH1 DNA mismatch repair protein, the cytological counterparts of reciprocal crossovers, in a panel of inter-subspecific chromosome substitution strains. Two autosomes, Chr 7 and Chr 11, significantly modified the meiotic recombination rate, yet the strongest modifier, designated meiotic recombination 1, Meir1, emerged in the 4.7 Mb Hstx2 genomic locus on Chr X. The male-limited transgressive effect of Meir1 on recombination rate parallels the male-limited transgressive role of Hstx2 in hybrid male sterility. Thus, both genetic factors, the Prdm9 gene and the Hstx2/Meir1 genomic locus, indicate a link between meiotic recombination and hybrid sterility. A strong female-specific modifier of meiotic recombination rate with the effect opposite to Meir1 was localized on Chr X, distally to Meir1. Mapping Meir1 to a narrow candidate interval on Chr X is an important first step towards positional cloning of the respective gene(s) responsible for variation in the global recombination rate between closely related mouse subspecies.
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Baker CL, Walker M, Kajita S, Petkov PM, Paigen K (2014) PRDM9 binding organizes hotspot nucleosomes and limits Holliday junction migration. Genome Res 24: 724–732. 10.1101/gr.170167.113 PubMed DOI PMC
Moens PB, Kolas NK, Tarsounas M, Marcon E, Cohen PE, et al. (2002) The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination. J Cell Sci 115: 1611–1622. PubMed
Baier B, Hunt P, Broman KW, Hassold T (2014) Variation in genome-wide levels of meiotic recombination is established at the onset of prophase in mammalian males. PLoS Genet 10: e1004125 10.1371/journal.pgen.1004125 PubMed DOI PMC
Bellani MA, Boateng KA, McLeod D, Camerini-Otero RD (2010) The expression profile of the major mouse SPO11 isoforms indicates that SPO11beta introduces double strand breaks and suggests that SPO11alpha has an additional role in prophase in both spermatocytes and oocytes. Mol Cell Biol 30: 4391–4403. 10.1128/MCB.00002-10 PubMed DOI PMC
Boateng KA, Bellani MA, Gregoretti IV, Pratto F, Camerini-Otero RD (2013) Homologous pairing preceding SPO11-mediated double-strand breaks in mice. Dev Cell 24: 196–205. 10.1016/j.devcel.2012.12.002 PubMed DOI PMC
Baudat F, de Massy B (2007) Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis. Chromosome Res 15: 565–577. PubMed
Lichten M, de Massy B (2011) The impressionistic landscape of meiotic recombination. Cell 147: 267–270. 10.1016/j.cell.2011.09.038 PubMed DOI PMC
Myers S, Bowden R, Tumian A, Bontrop RE, Freeman C, et al. (2010) Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327: 876–879. 10.1126/science.1182363 PubMed DOI PMC
Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, et al. (2010) PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327: 836–840. 10.1126/science.1183439 PubMed DOI PMC
Parvanov ED, Petkov PM, Paigen K (2010) Prdm9 controls activation of mammalian recombination hotspots. Science 327: 835 10.1126/science.1181495 PubMed DOI PMC
Baudat F, Imai Y, de Massy B (2013) Meiotic recombination in mammals: localization and regulation. Nat Rev Genet 14: 794–806. 10.1038/nrg3573 PubMed DOI
Brick K, Smagulova F, Khil P, Camerini-Otero RD, Petukhova GV (2012) Genetic recombination is directed away from functional genomic elements in mice. Nature 485: 642–645. 10.1038/nature11089 PubMed DOI PMC
Hayashi K, Yoshida K, Matsui Y (2005) A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 438: 374–378. PubMed
Cole F, Kauppi L, Lange J, Roig I, Wang R, et al. (2012) Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat Cell Biol 14: 424–430. 10.1038/ncb2451 PubMed DOI PMC
Holloway JK, Booth J, Edelmann W, McGowan CH, Cohen PE (2008) MUS81 generates a subset of MLH1-MLH3-independent crossovers in mammalian meiosis. PLoS Genet 4: e1000186 10.1371/journal.pgen.1000186 PubMed DOI PMC
Petkov PM, Broman KW, Szatkiewicz JP, Paigen K (2007) Crossover interference underlies sex differences in recombination rates. Trends Genet 23: 539–542. PubMed
Kyslikova L, Forejt J (1972) Chiasma frequency in three inbred strains of mice. Folia Biol (Praha) 18: 216–221. PubMed
Forejt J (1972) Chiasmata and crossing-over in the male mouse (Mus musculus). Suppression of recombination and chiasma frequencies in the ninth linkage group. Folia Biol (Praha) 18: 161–170. PubMed
Dumont BL, White MA, Steffy B, Wiltshire T, Payseur BA (2011) Extensive recombination rate variation in the house mouse species complex inferred from genetic linkage maps. Genome Res 21: 114–125. 10.1101/gr.111252.110 PubMed DOI PMC
Chowdhury R, Bois PR, Feingold E, Sherman SL, Cheung VG (2009) Genetic analysis of variation in human meiotic recombination. PLoS Genet 5: e1000648 10.1371/journal.pgen.1000648 PubMed DOI PMC
Ma L, O'Connell JR, VanRaden PM, Shen B, Padhi A, et al. (2015) Cattle Sex-Specific Recombination and Genetic Control from a Large Pedigree Analysis. PLoS Genet 11: e1005387 10.1371/journal.pgen.1005387 PubMed DOI PMC
Koehler KE, Cherry JP, Lynn A, Hunt PA, Hassold TJ (2002) Genetic control of mammalian meiotic recombination. I. Variation in exchange frequencies among males from inbred mouse strains. Genetics 162: 297–306. PubMed PMC
Dumont BL, Payseur BA (2008) Evolution of the genomic rate of recombination in mammals. Evolution 62: 276–294. PubMed
Dumont BL, Payseur BA (2011) Genetic analysis of genome-scale recombination rate evolution in house mice. PLoS Genet 7: e1002116 10.1371/journal.pgen.1002116 PubMed DOI PMC
Dumont BL, Payseur BA (2011) Evolution of the genomic recombination rate in murid rodents. Genetics 187: 643–657. 10.1534/genetics.110.123851 PubMed DOI PMC
Murdoch B, Owen N, Shirley S, Crumb S, Broman KW, et al. (2010) Multiple loci contribute to genome-wide recombination levels in male mice. Mamm Genome 21: 550–555. 10.1007/s00335-010-9303-5 PubMed DOI PMC
Mihola O, Trachtulec Z, Vlcek C, Schimenti JC, Forejt J (2009) A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science 323: 373–375. 10.1126/science.1163601 PubMed DOI
Bhattacharyya T, Reifova R, Gregorova S, Simecek P, Gergelits V, et al. (2014) X chromosome control of meiotic chromosome synapsis in mouse inter-subspecific hybrids. PLoS Genet 10: e1004088 10.1371/journal.pgen.1004088 PubMed DOI PMC
Bhattacharyya T, Gregorova S, Mihola O, Anger M, Sebestova J, et al. (2013) Mechanistic basis of infertility of mouse intersubspecific hybrids. Proc Natl Acad Sci U S A 110: E468–477. 10.1073/pnas.1219126110 PubMed DOI PMC
Flachs P, Bhattacharyya T, Mihola O, Pialek J, Forejt J, et al. (2014) Prdm9 incompatibility controls oligospermia and delayed fertility but no selfish transmission in mouse intersubspecific hybrids. PLoS One 9: e95806 10.1371/journal.pone.0095806 PubMed DOI PMC
Yang H, Wang JR, Didion JP, Buus RJ, Bell TA, et al. (2011) Subspecific origin and haplotype diversity in the laboratory mouse. Nat Genet 43: 648–655. 10.1038/ng.847 PubMed DOI PMC
Gregorova S, Divina P, Storchova R, Trachtulec Z, Fotopulosova V, et al. (2008) Mouse consomic strains: exploiting genetic divergence between Mus m. musculus and Mus m. domesticus subspecies. Genome Res 18: 509–515. 10.1101/gr.7160508 PubMed DOI PMC
Nadeau J, Singer J, Matin A, Lander E (2000) Analysing complex genetic traits with chromosome substitution strains. Nat Genet 24: 221–225. PubMed
Nadeau JH, Forejt J, Takada T, Shiroishi T (2012) Chromosome substitution strains: gene discovery, functional analysis, and systems studies. Mamm Genome 23: 693–705. 10.1007/s00335-012-9426-y PubMed DOI PMC
Kong A, Thorleifsson G, Frigge ML, Masson G, Gudbjartsson DF, et al. (2014) Common and low-frequency variants associated with genome-wide recombination rate. Nat Genet 46: 11–16. 10.1038/ng.2833 PubMed DOI
Flachs P, Mihola O, Simecek P, Gregorova S, Schimenti JC, et al. (2012) Interallelic and intergenic incompatibilities of the Prdm9 (Hst1) gene in mouse hybrid sterility. PLoS Genet 8: e1003044 10.1371/journal.pgen.1003044 PubMed DOI PMC
Liu EY, Morgan AP, Chesler EJ, Wang W, Churchill GA, et al. (2014) High-resolution sex-specific linkage maps of the mouse reveal polarized distribution of crossovers in male germline. Genetics 197: 91–106. 10.1534/genetics.114.161653 PubMed DOI PMC
Forejt J (1996) Hybrid sterility in the mouse. Trends Genet 12: 412–417. PubMed
Dzur-Gejdosova M, Simecek P, Gregorova S, Bhattacharyya T, Forejt J (2012) Dissecting the genetic architecture of f(1) hybrid sterility in house mice. Evolution 66: 3321–3335. 10.1111/j.1558-5646.2012.01684.x PubMed DOI
Good JM, Giger T, Dean MD, Nachman MW (2010) Widespread over-expression of the X chromosome in sterile F hybrid mice. PLoS Genet 6. PubMed PMC
White MA, Stubbings M, Dumont BL, Payseur BA (2012) Genetics and Evolution of Hybrid Male Sterility in House Mice. Genetics. PubMed PMC
Oka A, Mita A, Sakurai-Yamatani N, Yamamoto H, Takagi N, et al. (2004) Hybrid breakdown caused by substitution of the X chromosome between two mouse subspecies. Genetics 166: 913–924. PubMed PMC
Oka A, Shiroishi T (2014) Regulatory divergence of X-linked genes and hybrid male sterility in mice. Genes Genet Syst 89: 99–108. PubMed
Storchova R, Gregorova S, Buckiova D, Kyselova V, Divina P, et al. (2004) Genetic analysis of X-linked hybrid sterility in the house mouse. Mamm Genome 15: 515–524. PubMed
Forejt J, Pialek J, Trachtulec Z (2012) Hybrid male sterility genes in the mouse subspecific crosses In: Macholan M, Baird SJE, Muclinger P, Pialek J, editors. Evolution of the House Mouse. Cambridge: Cambridge University Press.
Pratto F, Brick K, Khil P, Smagulova F, Petukhova GV, et al. (2014) DNA recombination. Recombination initiation maps of individual human genomes. Science 346: 1256442 10.1126/science.1256442 PubMed DOI PMC
Paigen K, Petkov P (2010) Mammalian recombination hot spots: properties, control and evolution. Nat Rev Genet 11: 221–233. 10.1038/nrg2712 PubMed DOI PMC
Singer JB, Hill AE, Burrage LC, Olszens KR, Song J, et al. (2004) Genetic dissection of complex traits with chromosome substitution strains of mice. Science 304: 445–448. PubMed
Reynolds A, Qiao H, Yang Y, Chen JK, Jackson N, et al. (2013) RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nat Genet 45: 269–278. 10.1038/ng.2541 PubMed DOI PMC
Sun F, Fujiwara Y, Reinholdt LG, Hu J, Saxl RL, et al. (2015) Nuclear localization of PRDM9 and its role in meiotic chromatin modifications and homologous synapsis. Chromosoma. PubMed PMC
Margolin G, Khil PP, Kim J, Bellani MA, Camerini-Otero RD (2014) Integrated transcriptome analysis of mouse spermatogenesis. BMC Genomics 15: 39 10.1186/1471-2164-15-39 PubMed DOI PMC
Churchill GA, Airey DC, Allayee H, Angel JM, Attie AD, et al. (2004) The Collaborative Cross, a community resource for the genetic analysis of complex traits. Nat Genet 36: 1133–1137. PubMed
Collaborative Cross C (2012) The genome architecture of the Collaborative Cross mouse genetic reference population. Genetics 190: 389–401. 10.1534/genetics.111.132639 PubMed DOI PMC
Yang F, Silber S, Leu NA, Oates RD, Marszalek JD, et al. (2015) TEX11 is mutated in infertile men with azoospermia and regulates genome-wide recombination rates in mouse. EMBO Mol Med. PubMed PMC
Wang J, Fan HC, Behr B, Quake SR (2012) Genome-wide single-cell analysis of recombination activity and de novo mutation rates in human sperm. Cell 150: 402–412. 10.1016/j.cell.2012.06.030 PubMed DOI PMC
Cox A, Ackert-Bicknell CL, Dumont BL, Ding Y, Bell JT, et al. (2009) A new standard genetic map for the laboratory mouse. Genetics 182: 1335–1344. 10.1534/genetics.109.105486 PubMed DOI PMC
Hunter N, Chambers S, Louis E, Borts R (1996) The mismatch repair system contributes to meiotic sterility in an interspecific yeast hybrid. EMBO J 15: 1726–1733. PubMed PMC
Greig D, Travisano M, Louis EJ, Borts RH (2003) A role for the mismatch repair system during incipient speciation in Saccharomyces. J Evol Biol 16: 429–437. PubMed
Liti G, Barton DB, Louis EJ (2006) Sequence diversity, reproductive isolation and species concepts in Saccharomyces. Genetics 174: 839–850. PubMed PMC
Anderson LK, Reeves A, Webb LM, Ashley T (1999) Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics 151: 1569–1579. PubMed PMC
R_Development_Core_Team (2008) R: A language and environment for statistical computing [http://www.R-project.org]. Vienna: R Foundation for Statistical Computing.
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50: 346–363. 10.1002/bimj.200810425 PubMed DOI
Koller M (2015) Robustlmm: Robust Linear Mixed Effects Models. R package version 1.7–5. https://githubcom/kollerma/robustlmm.
Bates D, Machler M, Bolker B, Walker S (2015) lme4: Linear mixed-effects models using Eigen and S4_. R package version 1.1–8. <URL: http://CRANR-projectorg/package=lme4%3E.
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models using lme4. Journal of Statistical Software, ArXiv e-print; in press, URL: http://arxivorg/abs/14065823
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