Genetic variants in REC8, RNF212, and PRDM9 influence male recombination in cattle.

Animals; Cattle; Cell Cycle Proteins/genetics; Chromosome Mapping; Crossing Over, Genetic; Genetic Linkage; Genome; Histone-Lysine N-Methyltransferase/genetics; Homologous Recombination/genetics; Humans; Male; Miosis/genetics; Pedigree; Polymorphism, Single Nucleotide; Quantitative Trait Loci/genetics; Sequence Homology, Amino Acid; Sperm Count; Spermatozoa/cytology; Ubiquitin-Protein Ligases/genetics

Abstract :

[en] We use >250,000 cross-over events identified in >10,000 bovine sperm cells to perform an extensive characterization of meiotic recombination in male cattle. We map Quantitative Trait Loci (QTL) influencing genome-wide recombination rate, genome-wide hotspot usage, and locus-specific recombination rate. We fine-map three QTL and present strong evidence that genetic variants in REC8 and RNF212 influence genome-wide recombination rate, while genetic variants in PRDM9 influence genome-wide hotspot usage.

Disciplines :

Genetics & genetic processes

Author, co-author :

Sandor, Cynthia ; Université de Liège - ULiège > Département de productions animales > GIGA-R : Génomique animale

Li, Wanbo ; Université de Liège - ULiège > GIGA - Membres

Coppieters, Wouter ; Université de Liège - ULiège > Département de productions animales > GIGA-R : Génomique animale

Druet, Tom ; Université de Liège - ULiège > Département de productions animales > GIGA-R : Génomique animale

Charlier, Carole ; Université de Liège - ULiège > Département de productions animales > GIGA-R : Génomique animale

Georges, Michel ; Université de Liège - ULiège > Département de productions animales > GIGA-R : Génomique animale

Language :

English

Title :

Genetic variants in REC8, RNF212, and PRDM9 influence male recombination in cattle.

Publication date :

2012

Journal title :

PLoS Genetics

ISSN :

1553-7390

eISSN :

1553-7404

Publisher :

Public Library of Science, United States - California

Volume :

Issue :

Pages :

e1002854

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 15 January 2013

Statistics

Number of views

104 (11 by ULiège)

Number of downloads

141 (2 by ULiège)

More statistics

Scopus citations^®

109

Scopus citations^®
without self-citations

103

OpenCitations

117

OpenAlex citations

140

Bibliography

Roeder GS, (1997) Meiotic chromosomes: it takes two to tango. Gene Dev 11: 2600-2621.
Page SL, Hawley RS, (2003) Chromosome choreography: the meiotic ballet. Science 301: 785-791.
Coop G, Przeworski M, (2007) An evolutionary view of human recombination. Nat Rev Genet 8: 23-34.
Martinez-Perez E, Colaiácovo MP, (2009) Distribution of meiotic recombination events: talking to your neighbors. Curr Opin Genet Dev 19: 105-120.
Hassold T, Hunt P, (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2: 280-291.
Handel MA, Schimenti JC, (2010) Genetics of mammalian meiosis: regulation, dynamics and impact on fertility. Nat Rev Genet 11: 124-136.
Broman KW, Murray JC, Sheffield VC, White RL, Weber JL, (1998) Comprehensive human genetic maps: individual and sex-specific variation in recombination. Am. J. Hum. Genet. 63: 861-869.
Kong A, Gudbjartsson DF, Sainz J, Jonsdottir GM, Gudjonsson SA, et al. (2002) A high-resolution recombination map of the human genome. Nat Genet 31: 241-247.
Kong A, Barnard J, Gudbjartsson DF, Thorleifsson G, Jonsdottir G, et al. (2004) Recombination rate and reproductive success in humans. Nat Genet 36: 1203-1206.
Lenzi ML, Smith J, Snowden T, Kim M, Fishel R, et al. (2005) Extreme heterogeneity in the molecular events leading to the establishment of chiasmata during meiosis in human oocytes. Am J Hum Genet 76: 112-127.
Stefansson H, Helgason A, Thorleifsson G, Steinthorsdottir V, Masson G, et al. (2005) A common inversion under selection in Europeans. Nat Genet 37: 129-137.
Kong A, Thorleifsson G, Stefansson H, Masson G, Helgason A, et al. (2008) Sequence variants in the RNF212 gene associate with genome-wide recombination rate. Science 319: 1398-1401.
Chowdhury R, Bois PRJ, Feingold E, Sherman SL, Cheung VG, (2009) Genetic analysis of variation in human meiotic recombination. PLoS Genet 5: e1000648 doi:10.1371/journal.pgen.1000648.
Myers S, Bottolo L, Freeman C, McVean G, Donnelly P, (2005) A fine-scale map of recombination rates and hotspots across the human genome. Science 310: 321-324.
Paigen K, Petkov P, (2010) Mammalian recombination hot spots: properties, control and evolution. Nat Rev Genet 11: 221-233.
The 1,000 genomes project consortium (2010) A map of human genome variation from population-scale sequencing. Nature 467: 1061-1073.
Coop G, Wen X, Ober C, Pritchard JK, Przeworski M, (2008) High-resolution mapping of crossovers reveals extensive variation in fine-scale recombination patterns among humans. Science 319: 1395-1398.
Jeffreys AJ, Neumann R, (2009) The rise and fall of a human recombination hot spot. Nat Genet 41: 625-629.
Parvanov ED, Petkov PM, Paigen K, (2010) Prdm9 controls activation of mammalian recombination hotspots. Science 327: 835.
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.
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.
Berg IL, Neumann R, Lam KWG, Sarbajna S, Odenthal-Hesse L, et al. (2010) PRDM9 variation strongly influences recombination hot-spot activity and meiotic instability in humans. Nat Genet 42: 859-863.
Ptak SE, Hinds DA, Koehler K, Nickel B, Patil N, et al. (2005) Fine-scale recombination patterns differ between chimpanzees and humans. Nat Genet 37: 429-434.
Winckler W, Myers SR, Richter DJ, Onofrio RC, McDonald GJ, et al. (2005) Comparison of fine-scale recombination rates in humans and chimpanzees. Science 308: 107-111.
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.
Broman KW, Weber JL, (2000) Characterization of human crossover interference. Am J Hum Genet 66: 1911-1926.
Lian J, Yin Y, Oliver-Bonet M, Liehr T, Ko E, et al. (2008) Variation in crossover interference levels on individual chromosomes from human males. Hum Mol Genet 17: 2583-2594.
Meuwissen TH, Hayes BJ, Goddard ME, (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157: 1819-1829.
Bovine Genome Sequencing and Analysis Consortium (2009) The Genome Sequence of Taurine Cattle: A Window to Ruminant Biology and Evolution. Science 324: 522-528.
Ihara N, Takasuga A, Mizoshita K, Takeda H, Sugimoto M, et al. (2004) A comprehensive genetic map of the cattle genome based on 3802 microsatellites. Genome Res 14: 1987-1998.
Ross-Ibarra J, (2004) The evolution of recombination under domestication: a test of two hypotheses. Am Nat 163: 105-112.
Charlier C, Coppieters W, Rollin F, Desmecht D, Agerholm JS, et al. (2008) Highly effective SNP-based association mapping and management of recessive defects in livestock. Nat Genet 40: 449-454.
Matukumalli LK, Lawley CT, Schnabel RD, Taylor JF, Allan MF, et al. (2009) Development and characterization of a high density SNP genotyping assay for cattle. PLoS ONE 4: e5350 doi:10.1371/journal.pone.0005350.
Druet T, Georges M, (2010) A Hidden Markov Model combining linkage and linkage disequilibrium information for haplotype reconstruction and QTL fine mapping. Genetics 184: 789-798.
Fledel-Alon A, Wilson DJ, Broman K, Wen X, Ober C, et al. (2009) Broad-scale recombination patterns underlying proper disjunction in humans. PLoS Genet 5: e1000658 doi:10.1371/journal.pgen.1000658.
Sturt E, Smith CA, (1976) The relationship between chromatid interference and the mapping function. Cytogenet Cell Genet 17: 212-220.
Paigen K, Szatkiewicz JP, Sawyer K, Leahy N, Parvanov ED, Ng SHS, Graber JH, Broman KW, Petkow PM, (2008) The recombinational anatomy of a mouse chromosome. PLoS Genet 4: e1000119 doi:10.1371/journal.pgen.1000119.
McPeek MS, Speed TP, (1995) Modeling interference in genetic recombination. Genetics 139: 1031-1044.
Bannister LA, Reinholdt LG, Munroe RJ, Schimenti JC, (2004) Positional cloning and characterization of mouse mei8, a disrupted allelle of the meiotic cohesin Rec8. Genesis 40: 184-194.
Xu H, Beasley MD, Warren WD, Der Horst GTJ van, McKay MJ, (2005) Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis. Dev Cell 8: 949-961.
Ponting CP, (2011) What are the genomic drivers of the rapid evolution of PRDM9? Trends in Genetics 27: 165-171.
Axelsson E, Webster MT, Ratnakumar A, Consortium L, Ponting CP, Lindblad-Toh K, (2011) Death of PRDM9 coincides with stabilization of the recombination landscape in the dog genome. Genome Res Oct 17 [Epub ahead of print].
Munoz-Fuentes V, Di Rienzo A, Vila C, (2011) PRDM9, a major determinant of meiotic recombination hotspots, is not functional in dogs and their wild relatives, wolves and coyotes. PLoS ONE 6: e25498 doi:10.1371/journal.pone.0025498.
Liao D, (1999) Concerted evolution: molecular mechanism and biological implications. Am J Hum Genet 64: 24-30.
Housworth EA, Stahl FW, (2009) Is there variation in crossover interference levels among chromosomes from human males? Genetics 183: 403-405.
Housworth EA, Stahl FW, (2003) Crossover interference in humans. Am J Hum Genet 73: 188-197.
Kaback DB, Barber D, Mahon J, Lamb J, You J, (1999) Chromosome-size dependent control of meiotic reciprocal recombination in S. cerevisiae: the role of crossover interference. Genetics 152: 1475-1486.
Lynsch M, Walsh B, (1998) Genetics and Analysis of Quantitative Traits. In: Associates S, editors. (Sunderland).
Johnson DL, Thompson R, (1995) Restricted Maximum Likelihood Estimation of Variance Components for Univariate Animal Models Using Sparse Matrix Techniques and Average Information. J Dairy Sci 78: 449-456.
Churchill GA, Doerge RW, (1996) Permutation tests for multiple loci affecting a quantitative character. Genetics 142: 285-294.
Lander E, Kruglyak L, (1995) Genetic dissection of complex traits: guidelines for interpreting and reporting linkage results. Nat Genet 11: 241-247.