Evolutionary dynamics of meiotic recombination hotspots regulator PRDM9 in bovids
- 462 Downloads
Hybrid sterility or reproductive isolation in mammals has been attributed to allelic incompatibilities in a DNA-binding protein PRDM9. Not only is PRDM9 exceptional in being the only known ‘speciation gene’ in vertebrates, but it is also considered to be the fastest evolving gene in the genome. The terminal zinc finger (ZF) domain of PRDM9 specifies genome-wide meiotic recombination hotspot locations in mammals. Intriguingly, PRDM9 ZF domain is highly variable between as well as within species, possibly activating different recombination hotspots. The present study characterized the full-length coding sequence of PRDM9 in cattle and buffalo and explored the diversity of the ZF array in 514 samples from different bovids (cattle, yak, mithun, and buffalo). Substantial numerical and sequence variability were observed in the ZFs, with the number of repeats ranging from 6 to 9 in different bovines. Sequence analysis revealed the presence of 37 different ZFs in cattle, 3 in mithun, 4 in yak, and 13 in buffaloes producing 41 unique PRDM9 alleles in these species. The posterior mean of dN/dS or omega values calculated using Codeml tool of PAMLX identified sites −5, −1, +2, +3, +4, +5, and +6 in the ZF domain to be evolving positively in the studied species. Concerted evolution which typifies the evolution of this gene was consistently evident in all bovines. Our results demonstrate the extraordinary diversity of PRDM9 ZF array across bovines, reinforcing similar observations in other metazoans. The high variability is suggestive of unique repertoire of meiotic recombination hotspots in each species.
KeywordsMeiosis Recombination Speciation Positive selection Concerted evolution
This study was supported by the Indian Council of Agricultural Research, New Delhi, India.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no competing interests.
This article does not contain any studies with animals performed by any of the authors.
- Auton A, Fledel-Alon A, Pfeifer S, Venn O, Ségurel L, Street T, Leffler EM, Bowden R, Aneas I, Broxholme J, Humburg P, Iqbal Z, Lunter G, Maller J, Hernandez RD, Melton C, Venkat A, Nobrega MA, Bontrop R, Myers S, Donnelly P, Przeworski M, McVean G (2012) A fine-scale chimpanzee genetic map from population sequencing. Science 336:193–198CrossRefPubMedPubMedCentralGoogle Scholar
- Dobzhansky T (1951) Genetics and the origin of species. Columbia University, New YorkGoogle Scholar
- Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In: Nucleic acids symposium series 41:95–98Google Scholar
- Hinch AG, Tandon A, Patterson N, Song Y, Rohland N, Palmer CD, Chen GK, Wang K, Buxbaum SG, Akylbekova EL, Aldrich MC, Ambrosone CB, Amos C, Bandera EV, Berndt SI, Bernstein L, Blot WJ, Bock CH, Boerwinkle E, Cai Q, Caporaso N, Casey G, Cupples LA, Deming SL, Diver WR, Divers J, Fornage M, Gillanders EM, Glessner J, Harris CC, Hu JJ, Ingles SA, Isaacs W, John EM, Kao WH, Keating B, Kittles RA, Kolonel LN, Larkin E, Le Marchand L, McNeill LH, Millikan RC, Murphy A, Musani S, Neslund-Dudas C, Nyante S, Papanicolaou GJ, Press MF, Psaty BM, Reiner AP, Rich SS, Rodriguez-Gil JL, Rotter JI, Rybicki BA, Schwartz AG, Signorello LB, Spitz M, Strom SS, Thun MJ, Tucker MA, Wang Z, Wiencke JK, Witte JS, Wrensch M, Wu X, Yamamura Y, Zanetti KA, Zheng W, Ziegler RG, Zhu X, Redline S, Hirschhorn JN, Henderson BE, Taylor HA Jr, Price AL, Hakonarson H, Chanock SJ, Haiman CA, Wilson JG, Reich D, Myers SR (2011) The landscape of recombination in African Americans. Nature 476:170–175CrossRefPubMedPubMedCentralGoogle Scholar
- Hussin J, Sinnett D, Casals F, Idaghdour Y, Bruat V, Saillour V, Healy J, Grenier JC, de Malliard T, Busche S, Spinella JF, Larivière M, Gibson G, Andersson A, Holmfeldt L, Ma J, Wei L, Zhang J, Andelfinger G, Downing JR, Mullighan CG, Awadalla P (2013) Rare allelic forms of PRDM9 associated with childhood leukemogenesis. Genome Res 23:419–430CrossRefPubMedPubMedCentralGoogle Scholar
- Kong A, Thorleifsson G, Gudbjartsson DF, Masson G, Sigurdsson A, Jonasdottir A, Walters GB, Jonasdottir A, Gylfason A, Kristinsson KT, Gudjonsson SA, Frigge ML, Helgason A, Thorteinsdottir U, Stefansson K (2010) Fine-scale recombination rate differences between sexes, populations and individuals. Nature 467:1099–1103CrossRefPubMedGoogle Scholar
- Mandal DK, Tyagi S (2004) Pre-copulatory behaviour of Sahiwal bulls during semen collection and effects of age and season on their sexual performance. Indian J Dairy Sci 57:334–338Google Scholar
- Muller H (1942) Isolating mechanisms, evolution, and temperature. In: T D (ed.) Biological Symposia. Jaques Cattell Press, Lancaster, p 71–125Google Scholar
- Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbour Laboratory, New YorkGoogle Scholar
- Singh A (2005) Crossbreeding of cattle for increasing milk production in India: a review. Indian J Anim Sci 75:383–390Google Scholar