Natural variation in the zinc-finger-encoding exon of Prdm9 affects hybrid sterility phenotypes in mice

. 2024 Mar 06 ; 226 (3) : .

Jazyk angličtina Země Spojené státy americké Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid38217871

Grantová podpora
Max Planck Society
OD112/1-1 DFG CEP - Centrální evidence projektů
57334341 DAAD
22-299-28S Czech Science Foundation

PRDM9-mediated reproductive isolation was first described in the progeny of Mus musculus musculus (MUS) PWD/Ph and Mus musculus domesticus (DOM) C57BL/6J inbred strains. These male F1 hybrids fail to complete chromosome synapsis and arrest meiosis at prophase I, due to incompatibilities between the Prdm9 gene and hybrid sterility locus Hstx2. We identified 14 alleles of Prdm9 in exon 12, encoding the DNA-binding domain of the PRDM9 protein in outcrossed wild mouse populations from Europe, Asia, and the Middle East, 8 of which are novel. The same allele was found in all mice bearing introgressed t-haplotypes encompassing Prdm9. We asked whether 7 novel Prdm9 alleles in MUS populations and the t-haplotype allele in 1 MUS and 3 DOM populations induce Prdm9-mediated reproductive isolation. The results show that only combinations of the dom2 allele of DOM origin and the MUS msc1 allele ensure complete infertility of intersubspecific hybrids in outcrossed wild populations and inbred mouse strains examined so far. The results further indicate that MUS mice may share the erasure of PRDM9msc1 binding motifs in populations with different Prdm9 alleles, which implies that erased PRDM9 binding motifs may be uncoupled from their corresponding Prdm9 alleles at the population level. Our data corroborate the model of Prdm9-mediated hybrid sterility beyond inbred strains of mice and suggest that sterility alleles of Prdm9 may be rare.

Zobrazit více v PubMed

Altemose  N, Noor  N, Bitoun  E, Tumian  A, Imbeault  M, Chapman  JR, Aricescu  AR, Myers  SR. 2017a. A map of human PRDM9 binding provides evidence for novel behaviors of PRDM9 and other zinc-finger proteins in meiosis. Elife. 6:e28383. doi:10.7554/eLife.28383. PubMed DOI PMC

Altemose  N, Noor  N, Bitoun  E, Tumian  A, Imbeault  M, Chapman  JR, Aricescu  AR, Myers  SR. 2017b. Human PRDM9 can bind and activate promoters, and other zinc-finger proteins associate with reduced recombination in cis. bioRxiv. 10.1101/144295, preprint: not peer reviewed. DOI

Ambrosini  G, Groux  R, Bucher  P. 2018. PWMScan: a fast tool for scanning entire genomes with a position-specific weight matrix. Bioinformatics. 34(14):2483–2484. doi:10.1093/bioinformatics/bty127. PubMed DOI 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(4):1569–1579. doi:10.1093/genetics/151.4.1569. PubMed DOI PMC

Arora  UP, Dumont  BL. 2022. Meiotic drive in house mice: mechanisms, consequences, and insights for human biology. Chromosome Res. 30(2–3):165–186. doi:10.1007/s10577-022-09697-2. PubMed DOI PMC

Baker  CL, Kajita  S, Walker  M, Saxl  RL, Raghupathy  N, Choi  K, Petkov  PM, Paigen  K. 2015. PRDM9 drives evolutionary erosion of hotspots in Mus musculus through haplotype-specific initiation of meiotic recombination. PLoS Genet. 11(1):e1004916. doi:10.1371/journal.pgen.1004916. PubMed DOI PMC

Baker  CL, Walker  M, Kajita  S, Petkov  PM, Paigen  K. 2014. PRDM9 binding organizes hotspot nucleosomes and limits Holliday junction migration. Genome Res. 24(5):724–732. doi:10.1101/gr.170167.113. PubMed DOI PMC

Balcova  M, Faltusova  B, Gergelits  V, Bhattacharyya  T, Mihola  O, Trachtulec  Z, Knopf  C, Fotopulosova  V, Chvatalova  I, Gregorova  S, et al.  2016. Hybrid sterility locus on chromosome X controls meiotic recombination rate in mouse. PLoS Genet. 12(4):e1005906. doi:10.1371/journal.pgen.1005906. PubMed DOI PMC

Banker  SE, Bonhomme  F, Nachman  MW. 2022. Bidirectional introgression between Mus musculus domesticus and Mus spretus. Genome Biol Evol. 14(1):evab288. doi:10.1093/gbe/evab288. PubMed DOI PMC

Bateson  W. 1909. Heredity and variation in modern lights. In: Seward AC, editor. Darwin and Modern Science. Cambridge: Cambridge University Press. p. 85–101.

Baudat  F, Buard  J, Grey  C, Fledel-Alon  A, Ober  C, Przeworski  M, Coop  G, de Massy  B. 2010. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science. 327(5967):836–840. doi:10.1126/science.1183439. PubMed DOI PMC

Baudat  F, Imai  Y, de Massy  B. 2013. Meiotic recombination in mammals: localization and regulation. Nat Rev Genet. 14(11):794–806. doi:10.1038/nrg3573. PubMed DOI

Berg  IL, Neumann  R, Lam  KW, Sarbajna  S, Odenthal-Hesse  L, May  CA, Jeffreys  AJ. 2010. PRDM9 variation strongly influences recombination hotspot activity and meiotic instability in humans. Nat Genet. 42(10):859–863. doi:10.1038/ng.658. PubMed DOI PMC

Berg  IL, Neumann  R, Sarbajna  S, Odenthal-Hesse  L, Butler  NJ, Jeffreys  AJ. 2011. Variants of the protein PRDM9 differentially regulate a set of human meiotic recombination hotspots highly active in African populations. Proc Natl Acad Sci U S A. 108(30):12378–12383. doi:10.1073/pnas.1109531108. PubMed DOI PMC

Bhattacharyya  T, Gregorova  S, Mihola  O, Anger  M, Sebestova  J, Sebestova  J, Denny  P, Simecek  P, Forejt  J. 2013. Mechanistic basis of infertility of mouse intersubspecific hybrids. Proc Natl Acad Sci U S A. 110(6):E468–E477. doi:10.1073/pnas.1219126110. PubMed DOI PMC

Bhattacharyya  T, Reifova  R, Gregorova  S, Simecek  P, Gergelits  V, Mistrik  M, Martincova  I, Pialek  J, Forejt  J. 2014. X chromosome control of meiotic chromosome synapsis in mouse inter-subspecific hybrids. PLoS Genet. 10(2):e1004088. doi:10.1371/journal.pgen.1004088. PubMed DOI PMC

Billings  T, Parvanov  ED, Baker  CL, Walker  M, Paigen  K, Petkov  PM. 2013. DNA binding specificities of the long zinc-finger recombination protein PRDM9. Genome Biol. 14(4):R35. doi:10.1186/gb-2013-14-4-r35. PubMed DOI PMC

Boulton  A, Myers  RS, Redfield  RJ. 1997. The hotspot conversion paradox and the evolution of meiotic recombination. Proc Natl Acad Sci U S A. 94(15):8058–8063. doi:10.1073/pnas.94.15.8058. PubMed DOI PMC

Brick  K, Thibault-Sennett  S, Smagulova  F, Lam  KG, Pu  Y, Pratto  F, Camerini-Otero  RD, Petukhova  GV. 2018. Extensive sex differences at the initiation of genetic recombination. Nature. 561(7723):338–342. doi:10.1038/s41586-018-0492-5. PubMed DOI PMC

Buard  J, Rivals  E, Dunoyer de Segonzac  D, Garres  C, Caminade  P, de Massy  B, Boursot  P. 2014. Diversity of Prdm9 zinc finger array in wild mice unravels new facets of the evolutionary turnover of this coding minisatellite. PLoS One. 9(1):e85021. doi:10.1371/journal.pone.0085021. PubMed DOI PMC

Cole  F, Baudat  F, Grey  C, Keeney  S, de Massy  B, Jasin  M. 2014. Mouse tetrad analysis provides insights into recombination mechanisms and hotspot evolutionary dynamics. Nat Genet. 46(10):1072–1080. doi:10.1038/ng.3068. PubMed DOI PMC

Damm  E, Odenthal-Hesse  L. 2022. Orchestrating recombination initiation in mice and men. Curr Top Dev Biol. 151:27–42. doi:10.1016/bs.ctdb.2022.05.001. PubMed DOI

Damm  E, Ullrich  KK, Amos  WB, Odenthal-Hesse  L. 2022. Evolution of the recombination regulator PRDM9 in minke whales. BMC Genomics. 23(1):212. doi:10.1186/s12864-022-08305-1. PubMed DOI PMC

Davies  B, Hatton  E, Altemose  N, Hussin  JG, Pratto  F, Zhang  G, Hinch  AG, Moralli  D, Biggs  D, Diaz  R, et al.  2016. Re-engineering the zinc fingers of PRDM9 reverses hybrid sterility in mice. Nature. 530(7589):171–176. doi:10.1038/nature16931. PubMed DOI PMC

Dobzhansky  T. 1936. Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics. 21(2):113–135. doi:10.1093/genetics/21.2.113. PubMed DOI PMC

Dzur-Gejdosova  M, Simecek  P, Gregorova  S, Bhattacharyya  T, Forejt  J. 2012. Dissecting the genetic architecture of F1 hybrid sterility in house mice. Evolution. 66(11):3321–3335. doi:10.1111/j.1558-5646.2012.01684.x. PubMed DOI

Eram  MS, Bustos  SP, Lima-Fernandes  E, Siarheyeva  A, Senisterra  G, Hajian  T, Chau  I, Duan  S, Wu  H, Dombrovski  L, et al.  2014. Trimethylation of histone H3 lysine 36 by human methyltransferase PRDM9 protein. J Biol Chem. 289(17):12177–12188. doi:10.1074/jbc.M113.523183. PubMed DOI PMC

Fernandez-Capetillo  O, Mahadevaiah  SK, Celeste  A, Romanienko  PJ, Camerini-Otero  RD, Bonner  WM, Manova  K, Burgoyne  P, Nussenzweig  A. 2003. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell. 4(4):497–508. doi:10.1016/S1534-5807(03)00093-5. PubMed DOI

Flachs  P, Mihola  O, Simecek  P, Gregorova  S, Schimenti  JC, Matsui  Y, Baudat  F, de Massy  B, Piálek  J, Forejt  J, et al.  2012. Interallelic and intergenic incompatibilities of the Prdm9 (Hst1) gene in mouse hybrid sterility. PLoS Genet. 8(11):e1003044. doi:10.1371/journal.pgen.1003044. PubMed DOI PMC

Forejt  J. 2016. Genetics: asymmetric breaks in DNA cause sterility. Nature. 530(7589):167–168. doi:10.1038/nature16870. PubMed DOI

Forejt  J, Gregorova  S, Jansa  P. 1988. Three new t-haplotypes of Mus musculus reveal structural similarities to t-haplotypes of Mus domesticus. Genet Res. 51(2):111–119. doi:10.1017/S0016672300024125. PubMed DOI

Forejt  J, Ivanyi  P. 1974. Genetic studies on male sterility of hybrids between laboratory and wild mice (Mus musculus L.). Genet Res. 24(2):189–206. doi:10.1017/S0016672300015214. PubMed DOI

Forejt  J, Jansa  P. 2023. Meiotic recognition of evolutionarily diverged homologs: chromosomal hybrid sterility revisited. Mol Biol Evol. 40(4):msad083. doi:10.1093/molbev/msad083. PubMed DOI PMC

Forejt  J, Jansa  P, Parvanov  E. 2021. Hybrid sterility genes in mice (Mus musculus): a peculiar case of PRDM9 incompatibility. Trends Genet. 37(12):1095–1108. doi:10.1016/j.tig.2021.06.008. PubMed DOI

Fujiwara  K, Kawai  Y, Takada  T, Shiroishi  T, Saitou  N, Suzuki  H, Osada  N. 2022. Insights into Mus musculus population structure across Eurasia revealed by whole-genome analysis. Genome Biol Evol. 14(5):evac068. doi:10.1093/gbe/evac068. PubMed DOI PMC

Gregorova  S, Gergelits  V, Chvatalova  I, Bhattacharyya  T, Valiskova  B, Fotopulosova  V, Jansa  P, Wiatrowska  D, Forejt  J. 2018. Modulation of Prdm9-controlled meiotic chromosome asynapsis overrides hybrid sterility in mice. Elife. 7:e34282. doi:10.7554/eLife.34282. PubMed DOI PMC

Grey  C, Baudat  F, de Massy  B. 2018. PRDM9, a driver of the genetic map. PLoS Genet. 14(8):e1007479. doi:10.1371/journal.pgen.1007479. PubMed DOI PMC

Gupta  S, Stamatoyannopoulos  JA, Bailey  TL, Noble  WS. 2007. Quantifying similarity between motifs. Genome Biol. 8(2):R24. doi:10.1186/gb-2007-8-2-r24. PubMed DOI PMC

Hammer  MF, Silver  LM. 1993. Phylogenetic analysis of the alpha-globin pseudogene-4 (Hba-ps4) locus in the house mouse species complex reveals a stepwise evolution of t haplotypes. Mol Biol Evol. 10(5):971–1001. doi:10.1093/oxfordjournals.molbev.a040051. PubMed DOI

Hardouin  EA, Orth  A, Teschke  M, Darvish  J, Tautz  D, Bonhomme  F. 2015. Eurasian house mouse (Mus musculus L.) differentiation at microsatellite loci identifies the Iranian plateau as a phylogeographic hotspot. BMC Evol Biol. 15(1):26. doi:10.1186/s12862-015-0306-4. PubMed DOI PMC

Harr  B, Karakoc  E, Neme  R, Teschke  M, Pfeifle  C, Pezer  Ž, Babiker  H, Linnenbrink  M, Montero  I, Scavetta  R, et al.  2016. Genomic resources for wild populations of the house mouse, Mus musculus and its close relative Mus spretus. Sci Data. 3(1):160075. doi:10.1038/sdata.2016.75. PubMed DOI PMC

Hayashi  K, Yoshida  K, Matsui  Y. 2005. A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature. 438(7066):374–378. doi:10.1038/nature04112. PubMed DOI

Imai  Y, Baudat  F, Taillepierre  M, Stanzione  M, Toth  A, de Massy  B. 2017. The PRDM9 KRAB domain is required for meiosis and involved in protein interactions. Chromosoma. 126(6):681–695. doi:10.1007/s00412-017-0631-z. PubMed DOI PMC

Jeffreys  AJ, Cotton  VE, Neumann  R, Lam  KW. 2013. Recombination regulator PRDM9 influences the instability of its own coding sequence in humans. Proc Natl Acad Sci U S A. 110(2):600–605. doi:10.1073/pnas.1220813110. PubMed DOI PMC

Jeffreys  AJ, Neumann  R. 2002. Reciprocal crossover asymmetry and meiotic drive in a human recombination hot spot. Nat Genet. 31(3):267–271. doi:10.1038/ng910. PubMed DOI

Jeffreys  AJ, Neumann  R. 2005. Factors influencing recombination frequency and distribution in a human meiotic crossover hotspot. Hum Mol Genet. 14(15):2277–2287. doi:10.1093/hmg/ddi232. PubMed DOI

Jeffreys  AJ, Neumann  R, Wilson  V. 1990. Repeat unit sequence variation in minisatellites: a novel source of DNA polymorphism for studying variation and mutation by single molecule analysis. Cell. 60(3):473–485. doi:10.1016/0092-8674(90)90598-9. PubMed DOI

Kelemen  RK, Elkrewi  M, Lindholm  AK, Vicoso  B. 2022. Novel patterns of expression and recruitment of new genes on the t-haplotype, a mouse selfish chromosome. Proc Biol Sci. 289(1968):20211985. doi:10.1098/rspb.2021.1985. PubMed DOI PMC

Kelemen  RK, Vicoso  B. 2018. Complex history and differentiation patterns of the t-haplotype, a mouse meiotic driver. Genetics. 208(1):365–375. doi:10.1534/genetics.117.300513. PubMed DOI PMC

Kono  H, Tamura  M, Osada  N, Suzuki  H, Abe  K, Moriwaki  K, Ohta  K, Shiroishi  T. 2014. Prdm9 polymorphism unveils mouse evolutionary tracks. DNA Res. 21(3):315–326. doi:10.1093/dnares/dst059. PubMed DOI PMC

Latrille  T, Duret  L, Lartillot  N. 2017. The Red Queen model of recombination hotspot evolution: a theoretical investigation. Philos Trans R Soc Lond B Biol Sci. 372(1736):20160463. doi:10.1098/rstb.2016.0463. PubMed DOI PMC

Lawal  RA, Arora  UP, Dumont  BL. 2021. Selection shapes the landscape of functional variation in wild house mice. BMC Biol. 19(1):239. doi:10.1186/s12915-021-01165-3. PubMed DOI PMC

Lawson  C, Gieske  M, Murdoch  B, Ye  P, Li  Y, Hassold  T, Hunt  PA. 2011. Gene expression in the fetal mouse ovary is altered by exposure to low doses of bisphenol A. Biol Reprod. 84(1):79–86. doi:10.1095/biolreprod.110.084814. PubMed DOI PMC

Lustyk  D, Kinsky  S, Ullrich  KK, Yancoskie  M, Kasikova  L, Gergelits  V, Sedlacek  R, Chan  YF, Odenthal-Hesse  L, Forejt  J, et al.  2019. Genomic structure of Hstx2 modifier of Prdm9-dependent hybrid male sterility in mice. Genetics. 213(3):1047–1063. doi:10.1534/genetics.119.302554. PubMed DOI PMC

Lyon  MF. 2003. Transmission ratio distortion in mice. Annu Rev Genet. 37(1):393–408. doi:10.1146/annurev.genet.37.110801.143030. PubMed DOI

Mihola  O, Trachtulec  Z, Vlcek  C, Schimenti  JC, Forejt  J. 2009. A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science. 323(5912):373–375. doi:10.1126/science.1163601. PubMed DOI

Mukaj  A, Pialek  J, Fotopulosova  V, Morgan  AP, Odenthal-Hesse  L, Parvanov  ED, Forejt  J. 2020. Prdm9 inter-subspecific interactions in hybrid male sterility of house mouse. Mol Biol Evol. 37:3423–3438. doi:10.1093/molbev/msaa167. PubMed DOI PMC

Muller  HJ. 1942. Isolating mechanisms, evolution, and temperature. Biology Symposium. 6:71–125.

Myers  S, Bowden  R, Tumian  A, Bontrop  RE, Freeman  C, MacFie  TS, McVean  G, Donnelly  P. 2010. Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science. 327(5967):876–879. doi:10.1126/science.1182363. PubMed DOI PMC

Odenthal-Hesse  L, Berg  IL, Veselis  A, Jeffreys  AJ, May  CA. 2014. Transmission distortion affecting human noncrossover but not crossover recombination: a hidden source of meiotic drive. PLoS Genet. 10(2):e1004106. doi:10.1371/journal.pgen.1004106. PubMed DOI PMC

Olds-Clarke  P. 1997. Models for male infertility: the t haplotypes. Rev Reprod. 2(3):157–164. doi:10.1530/ror.0.0020157. PubMed DOI

Oliver  PL, Goodstadt  L, Bayes  JJ, Birtle  Z, Roach  KC, Phadnis  N, Beatson  SA, Lunter  G, Malik  HS, Ponting  CP. 2009. Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa. PLoS Genet. 5(12):e1000753. doi:10.1371/journal.pgen.1000753. PubMed DOI PMC

Paradis  E, Schliep  K. 2019. Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 35(3):526–528. doi:10.1093/bioinformatics/bty633. PubMed DOI

Parvanov  ED, Petkov  PM, Paigen  K. 2010. Prdm9 controls activation of mammalian recombination hotspots. Science. 327(5967):835. doi:10.1126/science.1181495. PubMed DOI PMC

Parvanov  ED, Tian  H, Billings  T, Saxl  RL, Spruce  C, Aithal  R, Krejci  L, Paigen  K, Petkov  PM. 2017. PRDM9 interactions with other proteins provide a link between recombination hotspots and the chromosomal axis in meiosis. Mol Biol Cell. 28(3):488–499. doi:10.1091/mbc.e16-09-0686. PubMed DOI PMC

Patel  A, Zhang  X, Blumenthal  RM, Cheng  X. 2017. Structural basis of human PR/SET domain 9 (PRDM9) allele C-specific recognition of its cognate DNA sequence. J Biol Chem. 292(39):15994–16002. doi:10.1074/jbc.M117.805754. PubMed DOI PMC

Persikov  AV, Osada  R, Singh  M. 2009. Predicting DNA recognition by Cys2His2 zinc finger proteins. Bioinformatics. 25(1):22–29. doi:10.1093/bioinformatics/btn580. PubMed DOI PMC

Persikov  AV, Singh  M. 2014. De novo prediction of DNA-binding specificities for Cys2His2 zinc finger proteins. Nucleic Acids Res. 42(1):97–108. doi:10.1093/nar/gkt890. PubMed DOI PMC

Phifer-Rixey  M, Harr  B, Hey  J. 2020. Further resolution of the house mouse (Mus musculus) phylogeny by integration over isolation-with-migration histories. BMC Evol Biol. 20(1):120. doi:10.1186/s12862-020-01666-9. PubMed DOI PMC

Pialek  J, Vyskocilova  M, Bimova  B, Havelkova  D, Pialkova  J, Dufkova  P, Bencova  V, Dureje  L, Albrecht  T, Hauffe  HC, et al.  2008. Development of unique house mouse resources suitable for evolutionary studies of speciation. J Hered. 99(1):34–44. doi:10.1093/jhered/esm083. PubMed DOI

Planchart  A, You  Y, Schimenti  JC. 2000. Physical mapping of male fertility and meiotic drive quantitative trait loci in the mouse t complex using chromosome deficiencies. Genetics. 155(2):803–812. doi:10.1093/genetics/155.2.803. PubMed DOI PMC

Powers  NR, Parvanov  ED, Baker  CL, Walker  M, Petkov  PM, Paigen  K. 2016. The meiotic recombination activator PRDM9 trimethylates both H3K36 and H3K4 at recombination hotspots in vivo. PLoS Genet. 12(6):e1006146. doi:10.1371/journal.pgen.1006146. PubMed DOI PMC

Quinlan  AR, Hall  IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 26(6):841–842. doi:10.1093/bioinformatics/btq033. PubMed DOI PMC

Santana-Garcia  W, Castro-Mondragon  JA, Padilla-Galvez  M, Nguyen  NTT, Elizondo-Salas  A, Ksouri  N, Gerbes  F, Thieffry  D, Vincens  P, Contreras-Moreira  B, et al.  2022. RSAT 2022: regulatory sequence analysis tools. Nucleic Acids Res. 50(W1):W670–W676. doi:10.1093/nar/gkac312. PubMed DOI PMC

Schimenti  JC, Reynolds  JL, Planchart  A. 2005. Mutations in Serac1 or Synj2 cause proximal t haplotype-mediated male mouse sterility but not transmission ratio distortion. Proc Natl Acad Sci U S A. 102(9):3342–3347. doi:10.1073/pnas.0407970102. PubMed DOI PMC

Silver  LM. 1985. Mouse t haplotypes. Annu Rev Genet. 19:179–208. doi:10.1146/annurev.ge.19.120185.001143. PubMed DOI

Smagulova  F, Brick  K, Pu  Y, Camerini-Otero  RD, Petukhova  GV. 2016. The evolutionary turnover of recombination hot spots contributes to speciation in mice. Genes Dev. 30(3):266–280. doi:10.1101/gad.270009.115. PubMed DOI PMC

Tamura  K, Nei  M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 10(3):512–526. doi:10.1093/oxfordjournals.molbev.a040023. PubMed DOI

Tiemann-Boege  I, Schwarz  T, Striedner  Y, Heissl  A. 2017. The consequences of sequence erosion in the evolution of recombination hotspots. Philos Trans R Soc Lond B Biol Sci. 372(1736):20160462. doi:10.1098/rstb.2016.0462. PubMed DOI PMC

Trachtulec  Z, Vlcek  C, Mihola  O, Gregorova  S, Fotopulosova  V, Forejt  J. 2008. Fine haplotype structure of a chromosome 17 region in the laboratory and wild mouse. Genetics. 178(3):1777–1784. doi:10.1534/genetics.107.082404. PubMed DOI PMC

Turner  LM, Harr  B. 2014. Genome-wide mapping in a house mouse hybrid zone reveals hybrid sterility loci and Dobzhansky–Muller interactions. Elife. 3:e02504. doi:10.7554/eLife.02504. PubMed DOI PMC

Turner  JM, Mahadevaiah  SK, Fernandez-Capetillo  O, Nussenzweig  A, Xu  X, Deng  C-X, Burgoyne  PS. 2005. Silencing of unsynapsed meiotic chromosomes in the mouse. Nat Genet. 37(1):41–47. doi:10.1038/ng1484. PubMed DOI

Turner  LM, Schwahn  DJ, Harr  B. 2012. Reduced male fertility is common but highly variable in form and severity in a natural house mouse hybrid zone. Evolution. 66(2):443–458. doi:10.1111/j.1558-5646.2011.01445.x. PubMed DOI

Ullrich  KK, Linnenbrink  M, Tautz  D. 2017. Introgression patterns between house mouse subspecies and species reveal genomic windows of frequent exchange. bioRxiv. 10.1101/168328, preprint: not peer reviewed. DOI

Valiskova  B, Gregorova  S, Lustyk  D, Simecek  P, Jansa  P, Forejt  J. 2022. Genic and chromosomal components of Prdm9-driven hybrid male sterility in mice (Mus musculus). Genetics. 222(1):iyac116. doi:10.1093/genetics/iyac116. PubMed DOI PMC

Vara  C, Capilla  L, Ferretti  L, Ledda  A, Sanchez-Guillen  RA, Gabriel  SI, Albert-Lizandra  G, Florit-Sabater  B, Bello-Rodríguez  J, Ventura  J. 2019. PRDM9 diversity at fine geographical scale reveals contrasting evolutionary patterns and functional constraints in natural populations of house mice. Mol Biol Evol. 36:1686–1700. doi:10.1093/molbev/msz091. PubMed DOI PMC

Walker  M, Billings  T, Baker  CL, Powers  N, Tian  H, Saxl  RL, Choi  K, Hibbs  MA, Carter  GW, Handel  MA, et al.  2015. Affinity-seq detects genome-wide PRDM9 binding sites and reveals the impact of prior chromatin modifications on mammalian recombination hotspot usage. Epigenetics Chromatin. 8(1):31. doi:10.1186/s13072-015-0024-6. PubMed DOI PMC

Wang  Y, Guo  T, Ke  H, Zhang  Q, Li  S, Luo  W, Qin  Y. 2021. Pathogenic variants of meiotic double strand break (DSB) formation genes PRDM9 and ANKRD31 in premature ovarian insufficiency. Genet Med. 23(12):2309–2315. doi:10.1038/s41436-021-01266-y. PubMed DOI PMC

Widmayer  SJ, Handel  MA, Aylor  DL. 2020. Age and genetic background modify hybrid male sterility in house mice. Genetics. 216(2):585–597. doi:10.1534/genetics.120.303474. PubMed DOI PMC

Wooldridge  LK, Dumont  BL. 2022. Rapid evolution of the fine-scale recombination landscape in wild house mouse (Mus musculus) populations. Mol Biol Evol. 40(1):msac267. doi:10.1093/molbev/msac267. PubMed DOI PMC

Wu  H, Mathioudakis  N, Diagouraga  B, Dong  A, Dombrovski  L, Baudat  F, Cusack  S, de Massy  B, Kadlec  J. 2013. Molecular basis for the regulation of the H3K4 methyltransferase activity of PRDM9. Cell Rep. 5(1):13–20. doi:10.1016/j.celrep.2013.08.035. PubMed DOI

Zelazowski  MJ, Cole  F. 2016. X marks the spot: PRDM9 rescues hybrid sterility by finding hidden treasure in the genome. Nat Struct Mol Biol. 23(4):267–269. doi:10.1038/nsmb.3201. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...