FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
PloS one2013; 8(4); e61746; doi: 10.1371/journal.pone.0061746

Characterization of Prdm9 in equids and sterility in mules.

Abstract: Prdm9 (Meisetz) is the first speciation gene discovered in vertebrates conferring reproductive isolation. This locus encodes a meiosis-specific histone H3 methyltransferase that specifies meiotic recombination hotspots during gametogenesis. Allelic differences in Prdm9, characterized for a variable number of zinc finger (ZF) domains, have been associated with hybrid sterility in male house mice via spermatogenic failure at the pachytene stage. The mule, a classic example of hybrid sterility in mammals also exhibits a similar spermatogenesis breakdown, making Prdm9 an interesting candidate to evaluate in equine hybrids. In this study, we characterized the Prdm9 gene in all species of equids by analyzing sequence variation of the ZF domains and estimating positive selection. We also evaluated the role of Prdm9 in hybrid sterility by assessing allelic differences of ZF domains in equine hybrids. We found remarkable variation in the sequence and number of ZF domains among equid species, ranging from five domains in the Tibetan kiang and Asiatic wild ass, to 14 in the Grevy's zebra. Positive selection was detected in all species at amino acid sites known to be associated with DNA-binding specificity of ZF domains in mice and humans. Equine hybrids, in particular a quartet pedigree composed of a fertile mule showed a mosaic of sequences and number of ZF domains suggesting that Prdm9 variation does not seem by itself to contribute to equine hybrid sterility.
Get Full Text
Publication Date: 2013-04-22 PubMed ID: 23613924PubMed Central: PMC3632555DOI: 10.1371/journal.pone.0061746Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • U.S. Gov't
  • Non-P.H.S.

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research investigated the role of the Prdm9 gene, known to be associated with sterility in hybrid species, in equids – specifically, mules which frequently experience sterility. They undertook gene sequencing in various equid species, assessing variations and evolutionary adaptions of the gene. The study did not find a direct link between variations in the Prdm9 gene and sterility in equine hybrids.

Understanding the Prdm9 Gene

  • The Prdm9 gene, or Meisetz, is significant because it is the first identified gene associated with speciation, or the formation of new and distinct species, in vertebrates. This means that it can contribute to reproductive isolation, where different species are unable to interbreed successfully.
  • Prdm9 is a meiosis-specific histone H3 methyltransferase, indicating its role during gametogenesis, the process by which an organism’s germ cells (eggs or sperm) are produced through a type of cell division called meiosis.
  • This gene is especially known for controlling the places where recombination occurs during meiosis, which involves the shuffling of genetic materials. These sites are often called recombination hotspots.
  • Previous studies in house mice have associated variations in the Prdm9 gene, especially in the number of zinc finger (ZF) domains, with hybrid sterility. Hybrid mice suffer from spermatogenesis breakdown during the pachytene stage, a phase of meiosis in which the process cannot proceed resulting in sterility.

Prdm9 in Equids and Mule Sterility

  • Given its known impacts in other species, researchers considered Prdm9 a candidate for similar studies in equids, a family of animals that includes horses, donkeys, and zebras. Mules, offspring of a male donkey and a female horse, are often sterile, providing a further reason to consider this gene.
  • The researchers characterized the Prdm9 gene in all species of equids. They did this by sequencing the gene and particularly evaluating the variations in the ZF domains of the gene. They also estimated the rate of positive selection, reflecting the speed of evolutionary adaptations of this gene.
  • The findings highlighted a notable variation in the sequence and number of ZF domains among equid species. For instance, the Tibetan kiang and Asiatic wild ass each have five domains, while the Grevy’s zebra has 14.
  • A vital observation was that all studied species showed positive selection at amino acid sites related to the DNA-binding specificity of the ZF domains, a characteristic found in mice and humans as well.

Prdm9 and Equine Hybrid Sterility

  • The role of Prdm9 in hybrid sterility was further evaluated by studying the differences in ZF domains in equine hybrids, specifically including a fertile mule.
  • Mules displayed a varied number and sequences of ZF domains. However, these differences were not directly associated with sterility in these equine hybrids. In simpler terms, variations in the Prdm9 gene appear not to be directly responsible for mule sterility, contrary to what has been observed in other species such as mice.

Cite This Article

APA
Steiner CC, Ryder OA. (2013). Characterization of Prdm9 in equids and sterility in mules. PLoS One, 8(4), e61746. https://doi.org/10.1371/journal.pone.0061746

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 8
Issue: 4
Pages: e61746
PII: e61746

Researcher Affiliations

Steiner, Cynthia C
  • Genetics Division, San Diego Zoo Institute for Conservation Research, San Diego Zoo Global, Escondido, California, USA. csteiner@sandiegozoo.org
Ryder, Oliver A

    MeSH Terms

    • Alleles
    • Amino Acid Sequence
    • Animals
    • Equidae / genetics
    • Evolution, Molecular
    • Female
    • Genetic Variation
    • Histone-Lysine N-Methyltransferase / chemistry
    • Histone-Lysine N-Methyltransferase / genetics
    • Histone-Lysine N-Methyltransferase / metabolism
    • Hybridization, Genetic
    • Infertility / enzymology
    • Infertility / genetics
    • Male
    • Molecular Sequence Data
    • Protein Structure, Tertiary
    • Selection, Genetic

    Conflict of Interest Statement

    The authors have declared that no competing interests exist.

    References

    This article includes 48 references
    1. Laurie CC. The weaker sex is heterogametic: 75 years of Haldane's rule.. Genetics 1997 Nov;147(3):937-51.
      pmc: PMC1208269pubmed: 9383043doi: 10.1093/genetics/147.3.937google scholar: lookup
    2. Muller H. Isolating mechanisms, evolution, and temperature. 1942.
    3. Coyne J, Orr H. Speciation. 2004.
    4. Presgraves DC. The molecular evolutionary basis of species formation.. Nat Rev Genet 2010 Mar;11(3):175-80.
      pubmed: 20051985doi: 10.1038/nrg2718google scholar: lookup
    5. Johnson NA. Hybrid incompatibility genes: remnants of a genomic battlefield?. Trends Genet 2010 Jul;26(7):317-25.
      pubmed: 20621759doi: 10.1016/j.tig.2010.04.005google scholar: lookup
    6. Perez DE, Wu CI. Further characterization of the Odysseus locus of hybrid sterility in Drosophila: one gene is not enough.. Genetics 1995 May;140(1):201-6.
      pmc: PMC1206547pubmed: 7635285doi: 10.1093/genetics/140.1.201google scholar: lookup
    7. Masly JP, Jones CD, Noor MA, Locke J, Orr HA. Gene transposition as a cause of hybrid sterility in Drosophila.. Science 2006 Sep 8;313(5792):1448-50.
      pubmed: 16960009doi: 10.1126/science.1128721google scholar: lookup
    8. Phadnis N, Orr HA. A single gene causes both male sterility and segregation distortion in Drosophila hybrids.. Science 2009 Jan 16;323(5912):376-9.
      pmc: PMC2628965pubmed: 19074311doi: 10.1126/science.1163934google scholar: lookup
    9. Mihola O, Trachtulec Z, Vlcek C, Schimenti JC, Forejt J. A mouse speciation gene encodes a meiotic histone H3 methyltransferase.. Science 2009 Jan 16;323(5912):373-5.
      pubmed: 19074312doi: 10.1126/science.1163601google scholar: lookup
    10. Hayashi K, Yoshida K, Matsui Y. A histone H3 methyltransferase controls epigenetic events required for meiotic prophase.. Nature 2005 Nov 17;438(7066):374-8.
      pubmed: 16292313doi: 10.1038/nature04112google scholar: lookup
    11. Grey C, Barthès P, Chauveau-Le Friec G, Langa F, Baudat F, de Massy B. Mouse PRDM9 DNA-binding specificity determines sites of histone H3 lysine 4 trimethylation for initiation of meiotic recombination.. PLoS Biol 2011 Oct;9(10):e1001176.
      pmc: PMC3196474pubmed: 22028627doi: 10.1371/journal.pbio.1001176google scholar: lookup
    12. Ponting CP. What are the genomic drivers of the rapid evolution of PRDM9?. Trends Genet 2011 May;27(5):165-71.
      pubmed: 21388701doi: 10.1016/j.tig.2011.02.001google scholar: lookup
    13. Hayashi K, Matsui Y. Meisetz, a novel histone tri-methyltransferase, regulates meiosis-specific epigenesis.. Cell Cycle 2006 Mar;5(6):615-20.
      pubmed: 16582607doi: 10.4161/cc.5.6.2572google scholar: lookup
    14. Thomas JH, Emerson RO, Shendure J. Extraordinary molecular evolution in the PRDM9 fertility gene.. PLoS One 2009 Dec 30;4(12):e8505.
      pmc: PMC2794550pubmed: 20041164doi: 10.1371/journal.pone.0008505google scholar: lookup
    15. Oliver PL, Goodstadt L, Bayes JJ, Birtle Z, Roach KC, Phadnis N, Beatson SA, Lunter G, Malik HS, Ponting CP. Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa.. PLoS Genet 2009 Dec;5(12):e1000753.
      pmc: PMC2779102pubmed: 19997497doi: 10.1371/journal.pgen.1000753google scholar: lookup
    16. Muñoz-Fuentes V, Di Rienzo A, Vilà C. Prdm9, a major determinant of meiotic recombination hotspots, is not functional in dogs and their wild relatives, wolves and coyotes.. PLoS One 2011;6(11):e25498.
      pmc: PMC3213085pubmed: 22102853doi: 10.1371/journal.pone.0025498google scholar: lookup
    17. Myers S, Bowden R, Tumian A, Bontrop RE, Freeman C, MacFie TS, McVean G, Donnelly P. Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination.. Science 2010 Feb 12;327(5967):876-9.
      pmc: PMC3828505pubmed: 20044541doi: 10.1126/science.1182363google scholar: lookup
    18. Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, Przeworski M, Coop G, de Massy B. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice.. Science 2010 Feb 12;327(5967):836-40.
      pmc: PMC4295902pubmed: 20044539doi: 10.1126/science.1183439google scholar: lookup
    19. Parvanov ED, Petkov PM, Paigen K. Prdm9 controls activation of mammalian recombination hotspots.. Science 2010 Feb 12;327(5967):835.
      pmc: PMC2821451pubmed: 20044538doi: 10.1126/science.1181495google scholar: lookup
    20. Berg IL, Neumann R, Sarbajna S, Odenthal-Hesse L, Butler NJ, Jeffreys AJ. 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 2011 Jul 26;108(30):12378-83.
      pmc: PMC3145720pubmed: 21750151doi: 10.1073/pnas.1109531108google scholar: lookup
    21. Ségurel L, Leffler EM, Przeworski M. The case of the fickle fingers: how the PRDM9 zinc finger protein specifies meiotic recombination hotspots in humans.. PLoS Biol 2011 Dec;9(12):e1001211.
      pmc: PMC3232208pubmed: 22162947doi: 10.1371/journal.pbio.1001211google scholar: lookup
    22. Miyamoto T, Koh E, Sakugawa N, Sato H, Hayashi H, Namiki M, Sengoku K. Two single nucleotide polymorphisms in PRDM9 (MEISETZ) gene may be a genetic risk factor for Japanese patients with azoospermia by meiotic arrest.. J Assist Reprod Genet 2008 Nov-Dec;25(11-12):553-7.
      pmc: PMC2593767pubmed: 18941885doi: 10.1007/s10815-008-9270-xgoogle scholar: lookup
    23. Chandley AC, Jones RC, Dott HM, Allen WR, Short RV. Meiosis in interspecific equine hybrids. I. The male mule (Equus asinus X E. caballus) and hinny (E. caballus X E. asinus).. Cytogenet Cell Genet 1974;13(4):330-41.
      pubmed: 4430187doi: 10.1159/000130284google scholar: lookup
    24. Horie T, Nishikawa Y. Studies on the reproduction ability of mules II. On functions of testes. Bulletin of the National Institute of Agricultural Science Series G 1959 8: 143–149.
    25. Lindsay E, Opdyke N, Johnson N. Pliocene dispersal of the horse Equus and late Cenozoic mammalian dispersal events. Nature 1980 287: 135–138.
    26. Hulbert RJ. The ancestry of the horse. 1996.
    27. Allen WR, Short RV. Interspecific and extraspecific pregnancies in equids: anything goes.. J Hered 1997 Sep-Oct;88(5):384-92.
      pubmed: 9378914doi: 10.1093/oxfordjournals.jhered.a023123google scholar: lookup
    28. Cordingley JE, Sundaresan S, Fischhoff I, Shapiro B, Ruskey J. Is the endangered Grevy’s zebra threatened by hybridization?. Animal Conservation 2009 12: 505–513.
    29. BENIRSCHKE K, LOW RJ, SULLIVAN MM, CARTER RM. CHROMOSOME STUDY OF AN ALLEGED FERTILE MARE MULE.. J Hered 1964 Jan-Feb;55:31-8.
      pubmed: 14134074doi: 10.1093/oxfordjournals.jhered.a107283google scholar: lookup
    30. Short RV, Chandley AC, Jones RC, Allen WR. Meiosis in interspecific equine hybrids. II. The przewalski horse/domestic horse hybrid.. Cytogenet Cell Genet 1974;13(5):465-78.
      pubmed: 4462982doi: 10.1159/000130300google scholar: lookup
    31. Ryder OA, Chemnick LG, Bowling AT, Benirschke K. Male mule foal qualifies as the offspring of a female mule and jack donkey.. J Hered 1985 Sep-Oct;76(5):379-81.
      pubmed: 4056372
    32. Rong R, Chandley AC, Song J, McBeath S, Tan PP, Bai Q, Speed RM. A fertile mule and hinny in China.. Cytogenet Cell Genet 1988;47(3):134-9.
      pubmed: 3378453doi: 10.1159/000132531google scholar: lookup
    33. Henry M, Gastal EL, Pinheiro LEL, Guimarmes SEF. Mating pattern and chromosome analysis of a mule and her offspring. Biology of Reproduction Monograph Series 1995 1: 273–279.
    34. Drummond A, Kearse M, Heled J, Moir R, Thierer T. Geneious v1.2.1. 2006.
    35. Steiner CC, Mitelberg A, Tursi R, Ryder OA. Molecular phylogeny of extant equids and effects of ancestral polymorphism in resolving species-level phylogenies.. Mol Phylogenet Evol 2012 Nov;65(2):573-81.
      pubmed: 22846684doi: 10.1016/j.ympev.2012.07.010google scholar: lookup
    36. Maddison D, Maddison W. MacClade 4.08. 2005.
    37. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.. Nucleic Acids Res 1994 Nov 11;22(22):4673-80.
      pmc: PMC308517pubmed: 7984417doi: 10.1093/nar/22.22.4673google scholar: lookup
    38. Swofford D. PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods) 4.0 Beta. 2002.
    39. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.. Syst Biol 2010 May;59(3):307-21.
      pubmed: 20525638doi: 10.1093/sysbio/syq010google scholar: lookup
    40. Felsenstein J. CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP.. Evolution 1985 Jul;39(4):783-791.
      pubmed: 28561359doi: 10.1111/j.1558-5646.1985.tb00420.xgoogle scholar: lookup
    41. Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood.. Comput Appl Biosci 1997 Oct;13(5):555-6.
      pubmed: 9367129doi: 10.1093/bioinformatics/13.5.555google scholar: lookup
    42. Fog CK, Galli GG, Lund AH. PRDM proteins: important players in differentiation and disease.. Bioessays 2012 Jan;34(1):50-60.
      pubmed: 22028065doi: 10.1002/bies.201100107google scholar: lookup
    43. Fumasoni I, Meani N, Rambaldi D, Scafetta G, Alcalay M, Ciccarelli FD. Family expansion and gene rearrangements contributed to the functional specialization of PRDM genes in vertebrates.. BMC Evol Biol 2007 Oct 4;7:187.
      pmc: PMC2082429pubmed: 17916234doi: 10.1186/1471-2148-7-187google scholar: lookup
    44. Alkan C, Sajjadian S, Eichler EE. Limitations of next-generation genome sequence assembly.. Nat Methods 2011 Jan;8(1):61-5.
      pmc: PMC3115693pubmed: 21102452doi: 10.1038/nmeth.1527google scholar: lookup
    45. Smith GP. Evolution of repeated DNA sequences by unequal crossover.. Science 1976 Feb 13;191(4227):528-35.
      pubmed: 1251186doi: 10.1126/science.1251186google scholar: lookup
    46. Choo Y, Klug A. Selection of DNA binding sites for zinc fingers using rationally randomized DNA reveals coded interactions.. Proc Natl Acad Sci U S A 1994 Nov 8;91(23):11168-72.
      pmc: PMC45188pubmed: 7972028doi: 10.1073/pnas.91.23.11168google scholar: lookup
    47. Flachs P, Mihola O, Simeček P, Gregorová S, Schimenti JC, Matsui Y, Baudat F, de Massy B, Piálek J, Forejt J, Trachtulec Z. Interallelic and intergenic incompatibilities of the Prdm9 (Hst1) gene in mouse hybrid sterility.. PLoS Genet 2012;8(11):e1003044.
      pmc: PMC3486856pubmed: 23133405doi: 10.1371/journal.pgen.1003044google scholar: lookup
    48. Dzur-Gejdosova M, Simecek P, Gregorova S, Bhattacharyya T, Forejt J. Dissecting the genetic architecture of F1 hybrid sterility in house mice.. Evolution 2012 Nov;66(11):3321-35.
      pubmed: 23106700doi: 10.1111/j.1558-5646.2012.01684.xgoogle scholar: lookup

    Citations

    This article has been cited 21 times.
    1. Cui Y, Liu P, Yu S, He J, Afedo SY, Zou S, Zhang Q, Liu J, Song L, Xu Y, Wang T, Li H. Expression Analysis of Molecular Chaperones Hsp70 and Hsp90 on Development and Metabolism of Different Organs and Testis in Cattle (Cattle-yak and Yak). Metabolites 2022 Nov 15;12(11).
      doi: 10.3390/metabo12111114pubmed: 36422254google scholar: lookup
    2. Damm E, Ullrich KK, Amos WB, Odenthal-Hesse L. Evolution of the recombination regulator PRDM9 in minke whales. BMC Genomics 2022 Mar 16;23(1):212.
      doi: 10.1186/s12864-022-08305-1pubmed: 35296233google scholar: lookup
    3. Hanot P, Herrel A, Guintard C, Cornette R. Unravelling the hybrid vigor in domestic equids: the effect of hybridization on bone shape variation and covariation. BMC Evol Biol 2019 Oct 15;19(1):188.
      doi: 10.1186/s12862-019-1520-2pubmed: 31615394google scholar: lookup
    4. Beeson SK, Mickelson JR, McCue ME. Exploration of fine-scale recombination rate variation in the domestic horse. Genome Res 2019 Oct;29(10):1744-1752.
      doi: 10.1101/gr.243311.118pubmed: 31434677google scholar: lookup
    5. Grey C, Baudat F, de Massy B. PRDM9, a driver of the genetic map. PLoS Genet 2018 Aug;14(8):e1007479.
      doi: 10.1371/journal.pgen.1007479pubmed: 30161134google scholar: lookup
    6. Janečka JE, Davis BW, Ghosh S, Paria N, Das PJ, Orlando L, Schubert M, Nielsen MK, Stout TAE, Brashear W, Li G, Johnson CD, Metz RP, Zadjali AMA, Love CC, Varner DD, Bellott DW, Murphy WJ, Chowdhary BP, Raudsepp T. Horse Y chromosome assembly displays unique evolutionary features and putative stallion fertility genes. Nat Commun 2018 Jul 27;9(1):2945.
      doi: 10.1038/s41467-018-05290-6pubmed: 30054462google scholar: lookup
    7. Paigen K, Petkov PM. PRDM9 and Its Role in Genetic Recombination. Trends Genet 2018 Apr;34(4):291-300.
      doi: 10.1016/j.tig.2017.12.017pubmed: 29366606google scholar: lookup
    8. Heintzman PD, Zazula GD, MacPhee R, Scott E, Cahill JA, McHorse BK, Kapp JD, Stiller M, Wooller MJ, Orlando L, Southon J, Froese DG, Shapiro B. A new genus of horse from Pleistocene North America. Elife 2017 Nov 28;6.
      doi: 10.7554/eLife.29944pubmed: 29182148google scholar: lookup
    9. Tiemann-Boege I, Schwarz T, Striedner Y, Heissl A. The consequences of sequence erosion in the evolution of recombination hotspots. Philos Trans R Soc Lond B Biol Sci 2017 Dec 19;372(1736).
      doi: 10.1098/rstb.2016.0462pubmed: 29109225google scholar: lookup
    10. Cucchi T, Mohaseb A, Peigné S, Debue K, Orlando L, Mashkour M. Detecting taxonomic and phylogenetic signals in equid cheek teeth: towards new palaeontological and archaeological proxies. R Soc Open Sci 2017 Apr;4(4):160997.
      doi: 10.1098/rsos.160997pubmed: 28484618google scholar: lookup
    11. Padhi A, Shen B, Jiang J, Zhou Y, Liu GE, Ma L. Ruminant-specific multiple duplication events of PRDM9 before speciation. BMC Evol Biol 2017 Mar 14;17(1):79.
      doi: 10.1186/s12862-017-0892-4pubmed: 28292260google scholar: lookup
    12. Capilla L, Sánchez-Guillén RA, Farré M, Paytuví-Gallart A, Malinverni R, Ventura J, Larkin DM, Ruiz-Herrera A. Mammalian Comparative Genomics Reveals Genetic and Epigenetic Features Associated with Genome Reshuffling in Rodentia. Genome Biol Evol 2016 Dec 1;8(12):3703-3717.
      doi: 10.1093/gbe/evw276pubmed: 28175287google scholar: lookup
    13. Ahlawat S, De S, Sharma P, Sharma R, Arora R, Kataria RS, Datta TK, Singh RK. Evolutionary dynamics of meiotic recombination hotspots regulator PRDM9 in bovids. Mol Genet Genomics 2017 Feb;292(1):117-131.
      doi: 10.1007/s00438-016-1260-6pubmed: 27744561google scholar: lookup
    14. Powers NR, Parvanov ED, Baker CL, Walker M, Petkov PM, Paigen K. The Meiotic Recombination Activator PRDM9 Trimethylates Both H3K36 and H3K4 at Recombination Hotspots In Vivo. PLoS Genet 2016 Jun;12(6):e1006146.
      doi: 10.1371/journal.pgen.1006146pubmed: 27362481google scholar: lookup
    15. Ahlawat S, Sharma P, Sharma R, Arora R, De S. Zinc Finger Domain of the PRDM9 Gene on Chromosome 1 Exhibits High Diversity in Ruminants but Its Paralog PRDM7 Contains Multiple Disruptive Mutations. PLoS One 2016;11(5):e0156159.
      doi: 10.1371/journal.pone.0156159pubmed: 27203728google scholar: lookup
    16. Baker CL, Petkova P, Walker M, Flachs P, Mihola O, Trachtulec Z, Petkov PM, Paigen K. Multimer Formation Explains Allelic Suppression of PRDM9 Recombination Hotspots. PLoS Genet 2015 Sep;11(9):e1005512.
      doi: 10.1371/journal.pgen.1005512pubmed: 26368021google scholar: lookup
    17. Walker M, Billings T, Baker CL, Powers N, Tian H, Saxl RL, Choi K, Hibbs MA, Carter GW, Handel MA, Paigen K, Petkov PM. Affinity-seq detects genome-wide PRDM9 binding sites and reveals the impact of prior chromatin modifications on mammalian recombination hotspot usage. Epigenetics Chromatin 2015;8:31.
      doi: 10.1186/s13072-015-0024-6pubmed: 26351520google scholar: lookup
    18. Baker CL, Kajita S, Walker M, Saxl RL, Raghupathy N, Choi K, Petkov PM, Paigen K. PRDM9 drives evolutionary erosion of hotspots in Mus musculus through haplotype-specific initiation of meiotic recombination. PLoS Genet 2015 Jan;11(1):e1004916.
      doi: 10.1371/journal.pgen.1004916pubmed: 25568937google scholar: lookup
    19. Jónsson H, Schubert M, Seguin-Orlando A, Ginolhac A, Petersen L, Fumagalli M, Albrechtsen A, Petersen B, Korneliussen TS, Vilstrup JT, Lear T, Myka JL, Lundquist J, Miller DC, Alfarhan AH, Alquraishi SA, Al-Rasheid KA, Stagegaard J, Strauss G, Bertelsen MF, Sicheritz-Ponten T, Antczak DF, Bailey E, Nielsen R, Willerslev E, Orlando L. Speciation with gene flow in equids despite extensive chromosomal plasticity. Proc Natl Acad Sci U S A 2014 Dec 30;111(52):18655-60.
      doi: 10.1073/pnas.1412627111pubmed: 25453089google scholar: lookup
    20. Buard J, Rivals E, Dunoyer de Segonzac D, Garres C, Caminade P, de Massy B, Boursot P. Diversity of Prdm9 zinc finger array in wild mice unravels new facets of the evolutionary turnover of this coding minisatellite. PLoS One 2014;9(1):e85021.
      doi: 10.1371/journal.pone.0085021pubmed: 24454780google scholar: lookup
    21. Baudat F, Imai Y, de Massy B. Meiotic recombination in mammals: localization and regulation. Nat Rev Genet 2013 Nov;14(11):794-806.
      doi: 10.1038/nrg3573pubmed: 24136506google scholar: lookup
    Subscribe to our newsletter
    Join 99,824 horse owners like you who receive our email updates on horse health and nutrition.