[en] Meiotic recombination is an essential biological process that ensures proper chromosome segregation and creates genetic diversity. Individual variation in global recombination rates has been shown to be heritable in several species, and variants significantly associated with this trait have been identified. Recombination on the sex chromosome has often been ignored in these studies although this trait may be particularly interesting as it may correspond to a biological process distinct from that on autosomes. For instance, recombination in males is restricted to the pseudo-autosomal region (PAR). We herein used a large cattle pedigree with more than 100,000 genotyped animals to improve the genetic map of the X chromosome and to study the genetic architecture of individual variation in recombination rate on the sex chromosome (XRR). The length of the genetic map was 46.4 and 121.2 cM in males and females, respectively, but the recombination rate in the PAR was six times higher in males. The heritability of CO counts on the X chromosome was comparable to that of autosomes in males (0.011) but larger than that of autosomes in females (0.024). XRR was highly correlated (0.76) with global recombination rate (GRR) in females, suggesting that both traits might be governed by shared variants. In agreement, a set of eleven previously identified variants associated with GRR had correlated effects on female XRR (0.86). In males, XRR and GRR appeared to be distinct traits, although more accurate CO counts on the PAR would be valuable to confirm these results.
Disciplines :
Animal production & animal husbandry Genetics & genetic processes
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Bibliography
Abecasis GR, Cherny SS, Cookson WO, Cardon LR (2002) Merlin-rapid analysis of dense genetic maps using sparse gene flow trees. Nat Genet 30:97–101
Acquaviva L, Boekhout M, Karasu ME, Brick K, Pratto F, Li T et al. (2020) Ensuring meiotic DNA break formation in the mouse pseudoautosomal region. Nature 582:426–431
Albers PK, McVean G (2020) Dating genomic variants and shared ancestry in population-scale sequencing data. PLoS Biol 18:e3000586
Amaral ME, Kata SR, Womack JE (2002) A radiation hybrid map of bovine X chromosome (BTAX). Mamm Genome 13:268–271
Arishima T, Sasaki S, Isobe T, Ikebata Y, Shimbara S, Ikeda S et al. (2017) Maternal variant in the upstream of FOXP3 gene on the X chromosome is associated with recurrent infertility in Japanese Black cattle. BMC Genet 18:103
Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, Przeworski M et al. (2010) PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327:836–840
Bilton TP, Schofield MR, Black MA, Chagné D, Wilcox PL, Dodds KG (2018) Accounting for errors in low coverage high-throughput sequencing data when constructing genetic maps using biparental outcrossed populations. Genetics 209:65–76
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
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
Broman KW, Rowe LB, Churchill GA, Paigen K (2002) Crossover interference in the mouse. Genetics 160:1123–1131
Browning SR, Browning BL (2007) Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet 81:1084–1097
Campbell CL, Furlotte NA, Eriksson N, Hinds D, Auton A (2015) Escape from crossover interference increases with maternal age. Nat Commun 6:6260
Chowdhury R, Bois PR, Feingold E, Sherman SL, Cheung VG (2009) Genetic analysis of variation in human meiotic recombination. PLoS Genet 5:e1000648
Coop G, Przeworski M (2007) An evolutionary view of human recombination. Nat Rev Genet 8:23–34
Demars J, Fabre S, Sarry J, Rossetti R, Gilbert H, Persani L et al. (2013) Genome-wide association studies identify two novel BMP15 mutations responsible for an atypical hyperprolificacy phenotype in sheep. PLoS Genet 9:e1003482
Druet T, Farnir FP (2011) Modeling of identity-by-descent processes along a chromosome between haplotypes and their genotyped ancestors. Genetics 188:409–419
Druet T, Gautier M (2017) A model-based approach to characterize individual inbreeding at both global and local genomic scales. Mol Ecol 26:5820–5841
Druet T, Georges M (2010) A hidden markov model combining linkage and linkage disequilibrium information for haplotype reconstruction and quantitative trait locus fine mapping. Genetics 184:789–798
Druet T, Georges M (2015) LINKPHASE3: an improved pedigree-based phasing algorithm robust to genotyping and map errors. Bioinformatics 31:1677–1679
Fernandez AI, Munoz M, Alves E, Folch JM, Noguera JL, Enciso MP et al. (2014) Recombination of the porcine X chromosome: a high density linkage map. BMC Genet 15:148
Fledel-Alon A, Leffler EM, Guan Y, Stephens M, Coop G, Przeworski M (2011) Variation in human recombination rates and its genetic determinants. PLoS One 6:e20321
Frohlich J, Kubickova S, Musilova P, Cernohorska H, Muskova H, Vodicka R et al. (2017) Karyotype relationships among selected deer species and cattle revealed by bovine FISH probes. PLoS One 12:e0187559
Groenen MA, Archibald AL, Uenishi H, Tuggle CK, Takeuchi Y, Rothschild MF et al. (2012) Analyses of pig genomes provide insight into porcine demography and evolution. Nature 491:393–398
Grossman SR, Shlyakhter I, Karlsson EK, Byrne EH, Morales S, Frieden G et al. (2010) A composite of multiple signals distinguishes causal variants in regions of positive selection. Science 327:883–886
Hinch AG, Altemose N, Noor N, Donnelly P, Myers SR (2014) Recombination in the human Pseudoautosomal region PAR1. PLoS Genet 10:e1004503
Housworth EA, Stahl FW (2003) Crossover interference in humans. Am J Hum Genet 73:188–197
Jansen J, Lagerweij GW (1987) Adjustment of non-return rates of AI technicians and dairy bulls. Livest Prod Sci 16:363–372
Johnson T, Keehan M, Harland C, Lopdell T, Spelman RJ, Davis SR et al. (2019) Short communication: identification of the pseudoautosomal region in the Hereford bovine reference genome assembly ARS-UCD1.2. J Dairy Sci 102:3254–3258
Johnston SE, Berenos C, Slate J, Pemberton JM (2016) Conserved genetic architecture underlying individual recombination rate variation in a wild population of Soay sheep (Ovis aries). Genetics 203:583–598
Johnston SE, Huisman J, Ellis PA, Pemberton JM (2017) A high-density linkage map reveals sexual dimorphism in recombination landscapes in red deer (Cervus elaphus). G3: Genes, Genomes, Genet 7:2859–2870
Kadri NK, Harland C, Faux P, Cambisano N, Karim L, Coppieters W et al. (2016) Coding and noncoding variants in HFM1, MLH3, MSH4, MSH5, RNF212, and RNF212B affect recombination rate in cattle. Genome Res 26:1323–1332
Karoui S, Carabano MJ, Diaz C, Legarra A (2012) Joint genomic evaluation of French dairy cattle breeds using multiple-trait models. Genet Sel Evol 44:39
Kauppi L, Barchi M, Baudat F, Romanienko PJ, Keeney S, Jasin M (2011) Distinct properties of the XY pseudoautosomal region crucial for male meiosis. Science 331:916–920
Khramtsova EA, Davis LK, Stranger BE (2019) The role of sex in the genomics of human complex traits. Nat Rev Genet 20:173–190
Kong A, Thorleifsson G, Frigge ML, Masson G, Gudbjartsson DF, Villemoes R et al. (2014) Common and low-frequency variants associated with genome-wide recombination rate. Nat Genet 46:11–16
Kong A, Thorleifsson G, Gudbjartsson DF, Masson G, Sigurdsson A, Jonasdottir A et al. (2010) Fine-scale recombination rate differences between sexes, populations and individuals. Nature 467:1099–1103
Kong A, Thorleifsson G, Stefansson H, Masson G, Helgason A, Gudbjartsson DF et al. (2008) Sequence variants in the RNF212 gene associate with genome-wide recombination rate. Science 319:1398–1401
Lander ES, Green P (1987) Construction of multilocus genetic linkage maps in humans. Proc Natl Acad Sci USA 84:2363–2367
Leutenegger AL, Prum B, Genin E, Verny C, Lemainque A, Clerget-Darpoux F et al. (2003) Estimation of the inbreeding coefficient through use of genomic data. Am J Hum Genet 73:516–523
Liu EY, Morgan AP, Chesler EJ, Wang W, Churchill GA, Pardo-Manuel de Villena F (2014) High-resolution sex-specific linkage maps of the mouse reveal polarized distribution of crossovers in male germline. Genetics 197:91–106
Ma J, Amos CI (2012) Investigation of inversion polymorphisms in the human genome using principal components analysis. PLoS One 7:e40224
Ma L, O’Connell JR, VanRaden PM, Shen B, Padhi A, Sun C et al. (2015) Cattle sex-specific recombination and genetic control from a large pedigree analysis. PLoS Genet 11:e1005387
Mackay TF, Stone EA, Ayroles JF (2009) The genetics of quantitative traits: challenges and prospects. Nat Rev Genet 10:565–577
Maier R, Moser G, Chen GB, Ripke S, Coryell W, Potash JB et al. (2015) Joint analysis of psychiatric disorders increases accuracy of risk prediction for schizophrenia, bipolar disorder, and major depressive disorder. Am J Hum Genet 96:283–294
Megens HJ, Crooijmans RP, Bastiaansen JW, Kerstens HH, Coster A, Jalving R et al. (2009) Comparison of linkage disequilibrium and haplotype diversity on macro- and microchromosomes in chicken. BMC Genet 10:86
Meyer K, Houle D (2013) Sampling based approximation of confidence intervals for functions of genetic covariance matrices. Proc Assoc Adv Anim Breed Genet 20:523–526
Misztal I, Tsuruta S, Strabel T, Auvray B, Druet T, DL, (2002) BLUPF90 and related programs (BGF90) In: Proceedings of the 7th World Congress on Genetics Applied to Livestock Production, vol 28. p 21–22
Murgiano L, Shirokova V, Welle MM, Jagannathan V, Plattet P, Oevermann A et al. (2016) Hairless streaks in cattle implicate TSR2 in early hair follicle formation. PLoS Genet 11:e1005427
Pacheco HA, Rezende FM, Peñagaricano F (2020) Gene mapping and genomic prediction of bull fertility using sex chromosome markers. J Dairy Sci 103:3304–3311
Peterson AL, Miller ND, Payseur BA (2019) Conservation of the genome-wide recombination rate in white-footed mice. Heredity 123:442–457
Petit M, Astruc JM, Sarry J, Drouilhet L, Fabre S, Moreno CR et al. (2017) Variation in recombination rate and its genetic determinism in sheep populations. Genetics 207:767–784
Rastas P, Paulin L, Hanski I, Lehtonen R, Auvinen P (2013) Lep-MAP: fast and accurate linkage map construction for large SNP datasets. Bioinformatics 29:3128–3134
Rodionov AV (1996) Micro vs. macro: structural-functional organization of avian micro- and macrochromosomes. Genetika 32:597–608
Rosen BD, Bickhart DM, Schnabel RD, Koren S, Elsik CG, Tseng E et al (2020) De novo assembly of the cattle reference genome with single-molecule sequencing. Gigascience 9. 10.1093/gigascience/giaa021
Rouyer F, Simmler MC, Vergnaud G, Johnsson C, Levilliers J, Petit C et al. (1986) The pseudoautosomal region of the human sex chromosomes. Cold Spring Harb Symp Quant Biol 51(Pt 1):221–228
Sandor C, Li W, Coppieters W, Druet T, Charlier C, Georges M (2012) Genetic variants in REC8, RNF212, and PRDM9 influence male recombination in cattle. PLoS Genet 8:e1002854
Scheet P, Stephens M (2006) A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet 78:629–644
Schmitt K, Lazzeroni LC, Foote S, Vollrath D, Fisher EM, Goradia TM et al. (1994) Multipoint linkage map of the human pseudoautosomal region, based on single-sperm typing: do double crossovers occur during male meiosis? Am J Hum Genet 55:423–430
Soriano P, Keitges EA, Schorderet DF, Harbers K, Gartler SM, Jaenisch R (1987) High rate of recombination and double crossovers in the mouse pseudoautosomal region during male meiosis. Proc Natl Acad Sci USA 84:7218–7220
Stapley J, Feulner PGD, Johnston SE, Santure AW, Smadja CM (2017) Variation in recombination frequency and distribution across eukaryotes: patterns and processes. Philos Trans R Soc Lond B Biol Sci 372:20160455
Stranden I, Garrick DJ (2009) Technical note: derivation of equivalent computing algorithms for genomic predictions and reliabilities of animal merit. J Dairy Sci 92:2971–2975
Van Laere AS, Coppieters W, Georges M (2008) Characterization of the bovine pseudoautosomal boundary: documenting the evolutionary history of mammalian sex chromosomes. Genome Res 18:1884–1895
Venn O, Turner I, Mathieson I, de Groot N, Bontrop R, McVean G (2014) Nonhuman genetics. Strong male bias drives germline mutation in chimpanzees. Science 344:1272–1275
Wang H, Misztal I, Aguilar I, Legarra A, Muir WM (2012) Genome-wide association mapping including phenotypes from relatives without genotypes. Genet Res 94:73–83
Wang RJ, Dumont BL, Jing P, Payseur BA (2019) A first genetic portrait of synaptonemal complex variation. PLOS Genet 15:1008337
Wang Z, Shen B, Jiang J, Li J, Ma L (2016) Effect of sex, age and genetics on crossover interference in cattle. Sci Rep 6:37698
Wise AL, Gyi L, Manolio TA (2013) eXclusion: toward integrating the X chromosome in genome-wide association analyses. Am J Hum Genet 92:643–647
Zhang Z, Guillaume F, Sartelet A, Charlier C, Georges M, Farnir F et al. (2012) Ancestral haplotype-based association mapping with generalized linear mixed models accounting for stratification. Bioinformatics 28:2467–2473
Zheng C, Boer MP, van Eeuwijk FA (2019) Construction of genetic linkage maps in multiparental populations. Genetics 212:1031–1044
Similar publications
Sorry the service is unavailable at the moment. Please try again later.
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.
