Genome-wide single nucleotide polymorphism (SNP) identification and characterization in a non-model organism, the African buffalo (Syncerus caffer), using next generation sequencing
smitz, nathalie; Van Hooft, pim; Heller, Rasmuset al.
[en] This study aimed to develop a set of SNP markers with high resolution and accuracy within the African
buffalo. Such a set can be used, among others, to depict subtle population genetic structure for a better
understanding of buffalo population dynamics. In total, 18.5 million DNA sequences of 76 bp were generated
by next generation sequencing on an Illumina Genome Analyzer II from a reduced representation
library using DNA from a panel of 13 African buffalo representative of the four subspecies. We identified
2534 SNPs with high confidence within the panel by aligning the short sequences to the cattle genome
(Bos taurus). The average sequencing depth of the complete aligned set of reads was estimated at 5x, and
at 13x when only considering the final set of putative SNPs that passed the filtering criterion. Our set of
SNPs was validated by PCR amplification and Sanger sequencing of 15 SNPs. Of these 15 SNPs, 14 amplified
successfully and 13 were shown to be polymorphic (success rate: 87%). The fidelity of the identified
set of SNPs and potential future applications are finally discussed.
Disciplines :
Zoology
Author, co-author :
smitz, nathalie
Van Hooft, pim
Heller, Rasmus
Cornelis, Daniel
Chardonnet, Philippe
Kraus, Robert
Greyling, Ben
Crooijmans, Richard
Groenen, Martien
Michaux, Johan ; Université de Liège > Département des sciences de la vie > Génétique et physiologie des microalgues
Language :
English
Title :
Genome-wide single nucleotide polymorphism (SNP) identification and characterization in a non-model organism, the African buffalo (Syncerus caffer), using next generation sequencing
Abdurashitov, M.A., Tomilov, V.N., Chernukhin, V.A., Gonchar, D.A., Degtyarev, S. Kh., Mammalian chromosomal DNA digestion with restriction endonucleases in silico. Ovchinnikov Bull. Biotechnol. Phys. Chem. Biol. 2 (2006), 29–38.
Abdurashitov, M.A., Tomilov, V.N., Chernukhin, V.A., Gonchar, D.A., Degtyarev, S. Kh., Comparative analysis of human chromosomal DNA digestion with restriction endonucleases in vitro and in silico. Med. Genet. 6 (2007), 29–36.
Aitken, N., Smith, S., Schwarz, C., Morin, P.A., Single nucleotide polymorphism (SNP) discovery in mammals: a targeted-gene approach. Mol. Ecol. 13 (2004), 1423–1431, 10.1111/j.1365-294X.2004.02159.x.
Andreassen, R., Lunner, S., Høyheim, B., Targeted SNP discovery in Atlantic salmon (Salmo salar) genes using a 3′UTR-primed SNP detection approach. BMC Genomics, 11, 2010, 706, 10.1186/1471-2164-11-706.
Brookes, A.J., The essence of SNPs. Gene 234 (1999), 177–186.
Cooper, D.N., Mort, M., Stenson, P.D., Ball, E.V., Chuzhanova, N.A., Methylation-mediated deamination of 5-methylcytosine appears to give rise to mutations causing human inherited disease in CpNpG trinucleotides, as well as in CpG dinucleotides. Hum. Genomics 4 (2010), 406–410.
Cramer, E.R.A., Stenzler, L., Talaba, A.L., Makarewich, C.A., Vehrencamp, S.L., Lovette, I.J., Isolation and characterization of SNP variation at 90 anonymous loci in the banded wren (Thryothorus pleurostictus). Conserv. Genet. 9 (2008), 1657–1660, 10.1007/s10592-008-9511-7.
Cross, P., Lloyd-Smith, J., Bowers, J., Hay, C., Hofmeyr, M., Getz, W., Integrating association data and disease dynamics: an illustration using African buffalo in Kruger National Park. Ann. Zool. Fennici 41 (2004), 879–892.
Cross, P.C., Lloyd-Smith, J.O., Getz, W.M., Disentangling association patterns in fission-fusion societies using African buffalo as an example. Anim. Behav. 69 (2005), 499–506, 10.1016/j.anbehav.2004.08.006.
DePristo, M.A., Banks, E., Poplin, R., Garimella, K., Maguire, V., Hartl, J.R., Philippakis, C., Angel, A.A., del, G., Rivas, M.A., Hanna, M., McKenna, A., Fennell, T.J., Kernytsky, A.M., Sivachenko, A.Y., Cibulskis, K., Gabriel, S.B., Altshuler, D., Daly, M.J., A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43 (2011), 491–498, 10.1038/ng.806.
Dohm, J.C., Lottaz, C., Borodina, T., Himmelbauer, H., Substantial biases in ultra-short read data sets from high-throughput DNA sequencing. Nucleic Acids Res., 36, 2008, e105, 10.1093/nar/gkn425.
Du Toit, R., Trypanosomiasis in Zululand and the control of tsetse flies by chemical means. Onderstepoort J. Vet. Res. 26 (1954), 317–387.
East, R., African Antelope Database 1999. 1999, Gland: IUCN, Switzerland and Cambridge.
Ewing, B., Green, P., Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8 (1998), 186–194.
Frankham, R., Ballou, J.D., Briscoe, D.A., Introduction to Conservation Genetics. 2002, Cambridge University Press, Cambridge.
Garine-Wichatitsky, M., de Caron, A., Gomo, C., Foggin, C., Dutlow, K., Pfukenyi, D., Lane, E., Bel, S., Le Hofmeyr, M., Hlokwe, T., Michel, A., Bovine tuberculosis in buffaloes, Southern Africa. Emerg. Infect. Dis. 16 (2010), 884–885, 10.1890/02-5266.
Hall, T.A., BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41 (1999), 95–98.
Hassanin, A., Ropiquet, A., Molecular phylogeny of the tribe Bovini (Bovidae, Bovinae) and the taxonomic status of the Kouprey, Bos sauveli Urbain 1937. Mol. Phylogenet. Evol. 33 (2004), 896–907, 10.1016/j.ympev.2004.08.009.
Hedges, S.B., Dudley, J., Kumar, S., TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22 (2006), 2971–2972, 10.1093/bioinformatics/btl505.
Huang, Y., Li, Y., Burt, D.W., Chen, H., Zhang, Y., et al. The duck genome and transcriptome provide insight into an avian influenza virus reservoir species. Nat. Genet. 45 (2013), 776–784, 10.1038/ng.2657.
Jolles, A.E., Cooper, D.V., Levin, S.A., Hidden effects of chronic tuberculosis in African buffalo. Ecology 86 (2005), 2358–2364, 10.1890/05-0038.
Jonker, R.M., Zhang, Q., Van Hooft, P., Loonen, M.J.J.E., Van der Jeugd, H.P., Crooijmans, R.P.M.A., Groenen, M.A.M., Prins, H.H.T., Kraus, R.H.S., The development of a genome wide SNP set for the Barnacle goose Branta leucopsis. PLoS One, 7, 2012, e38412, 10.1371/journal.pone.0038412.
Kappmeier, K., Nevill, E.M., Bagnall, R.J., Review of tsetse flies and trypanosomosis in South Africa. Onderstepoort J. Vet. Res. 65 (1998), 195–203.
Kerstens, H.H.D., Crooijmans, R.P.M., Veenendaal, A., Dibbits, B.W., Chin-A-Woeng, T.F.C., den Dunnen, J.T., Groenen, M.A.M., Large scale single nucleotide polymorphism discovery in unsequenced genomes using second generation high throughput sequencing technology: applied to turkey. BMC Genomics, 10, 2009, 479, 10.1186/1471-2164-10-479.
Kraus, R.H.S., Kerstens, H.H.D., Van Hooft, P., Crooijmans, R.P.M.A., Van Der Poel, J.J., Elmberg, J., Vignal, A., Huang, Y., Li, N., Prins, H.H.T., Groenen, M.A.M., Genome wide SNP discovery, analysis and evaluation in mallard (Anas platyrhynchos). BMC Genomics, 12, 2011, 150, 10.1186/1471-2164-12-150.
Kraus, R.H.S., Kerstens, H.H.D., van Hooft, P., Megens, H.-J., Elmberg, J., Tsvey, A., Sartakov, D., Soloviev, S.A., Crooijmans, R.P.M.A., Groenen, M.A.M., Ydenberg, R.C., Prins, H.H.T., Widespread horizontal genomic exchange does not erode species barriers among sympatric ducks. BMC Evol. Biol., 12, 2012, 45, 10.1186/1471-2148-12-45.
Kraus, R.H.S., Vonholdt, B., Cocchiararo, B., Harms, V., Bayerl, H., Uhn, R.K., Orster, D.W.F., Roos, C., A single-nucleotide polymorphism-based approach for rapid and cost-effective genetic wolf monitoring in Europe based on noninvasively collected samples. Mol. Ecol. Resour., 2014, 10.1111/1755-0998.12307.
Kumar, S., Hedges, S.B., TimeTree2: species divergence times on the iPhone. Bioinformatics 27 (2011), 2023–2024, 10.1093/bioinformatics/btr315.
Le Roex, N., Noyes, H., Brass, A., Bradley, D.G., Kemp, S.J., Kay, S., van Helden, P.D., Hoal, E.G., Novel SNP discovery in African buffalo syncerus caffer, using high-throughput sequencing. PLoS One, 7, 2012, e48792, 10.1371/journal.pone.0048792.
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., The sequence alignment/map (SAM) format and SAM tools. Bioinformatics 25 (2009), 2078–2079.
Li, S., Wan, H., Ji, H., Zhou, K., Yang, G., SNP discovery based on CATS and genotyping in the finless porpoise (Neophocaena phocaenoides). Conserv. Genet. 10 (2009), 2013–2019.
Liu, N., Chen, L., Wang, S., Oh, C., Zhao, H., Comparison of single-nucleotide polymorphisms and microsatellites in inference of population structure. BMC Genet., 6(Suppl. 1), 2005, S26, 10.1186/1471-2156-6-s1-s26.
Luikart, G., England, P.R., Tallmon, D., Jordan, S., Taberlet, P., The power and promise of population genomics: from genotyping to genome typing. Nat. Rev. Genet. 4 (2003), 981–994, 10.1038/nrg1226.
Matukumalli, L.K., Lawley, C.T., Schnabel, R.D., Taylor, J.F., Allan, M.F., Heaton, M.P., O'Connell, J., Moore, S.S., Smith, T.P.L., Sonstegard, T.S., Van Tassell, C.P., Development and characterization of a high density SNP genotyping assay for cattle. PLoS One, 4, 2009, e5350, 10.1371/journal.pone.0005350.
Michel, A.L., Bengis, R.G., Keet, D.F., Hofmeyr, M., DE Klerk, L.M., Cross, P.C., Jolles, A.E., Cooper, D., Whyte, I.J., Buss, P., Godfroid, J., Wildlife tuberculosis in South African conservation areas: implications and challenges. Vet. Microbiol. 112 (2006), 91–100, 10.1016/j.vetmic.2005.11.035.
Michelizzi, V.N., Wu, X., Dodson, M.V., Michal, J.J., Zambrano-varon, J., Mclean, D.J., Jiang, Z., A global view of 54, 001 single nucleotide polymorphisms (SNPs) on the illumina BovineSNP50 BeadChip and their transferability to water buffalo. Int. J. Biol. Sci. 7 (2011), 18–27.
Miller, J.M., Poissant, J., Kijas, J.W., Coltman, D.W., A genome-wide set of SNPs detects population substructure and long range linkage disequilibrium in wild sheep. Mol. Ecol. Resour. 11 (2010), 314–322, 10.1111/j.1755-0998.2010.02918.x.
Morin, P., Luikart, G., Wayne, R.K., SNPs in ecology, evolution and conservation. Trends Ecol. Evol. 19 (2004), 208–216, 10.1016/j.tree.2004.01.009.
Morin, P., Mccarthy, M., Highly accurate SNP genotyping from historical and low-quality samples. Mol. Ecol. Notes 7 (2007), 937–946, 10.1111/j.1471-8286.2007.01804.x.
Morin, P.A., Aitken, N.C., Rubio-Cisneros, N., Dizon, A.E., Mesnick, S., Characterization of 18 SNP markers for sperm whale (Physeter macrocephalus). Mol. Ecol. Notes 7 (2007), 626–630, 10.1111/j.1471-8286.2006.01654.x.
Morin, P., Martien, K.K., Taylor, B.L., Assessing statistical power of SNPs for population structure and conservation studies. Mol. Ecol. Resour. 9 (2009), 66–73, 10.1111/j.1755-0998.2008.02392.x.
Olsen, M.T., Volny, V.H., Bérubé, M., Dietz, R., Lydersen, C., Kovacs, K.M., Dodd, R.S., Palsbøll, P.J., A simple route to single-nucleotide polymorphisms in a nonmodel species: identification and characterization of SNPs in the Artic ringed seal (Pusa hispida hispida). Mol. Ecol. Resour. 11:Suppl. 1 (2011), 9–19, 10.1111/j.1755-0998.2010.02941.x.
Pitra, C., Hansen, A.J., Lieckfeldt, D., Arctander, P., An exceptional case of historical outbreeding in African sable antelope populations. Mol. Ecol. 11 (2002), 1197–1208.
Ramos, A.M., Crooijmans, R.P.M., Affara, N., Amaral, A.J., Archibald, A.L., Beever, J.E., Bendixen, C., Churcher, C., Clark, R., Dehais, P., Hansen, M.S., Hedegaard, J., Hu, Z.-L., Kerstens, H.H., Law, A.S., Megens, H.-J., Milan, D., Nonneman, D.J., Rohrer, G., Rothschild, M.F., Smith, T.P.L., Schnabel, R.D., Van Tassell, C.P., Taylor, J.F., Wiedmann, R.T., Schook, L.B., Groenen, M.M., Design of a high density SNP genotyping assay in the pig using SNPs identified and characterized by next generation sequencing technology. PLoS One, 4, 2009, e6524, 10.1371/journal.pone.0006524.
Robinson, T.J., Ropiquet, A., Examination of hemiplasy, homoplasy and phylogenetic discordance in chromosomal evolution of the Bovidae. Syst. Biol. 60 (2011), 439–450, 10.1093/sysbio/syr045.
Rodwell, T.C., Whyte, I.J., Boyce, W.M., Evaluation of population effects of bovine tuberculosis in free-ranging african Buffalo (Syncerus caffer). J. Mammal. 82 (2001), 231–238, 10.1644/1545-1542(2001)082<0231:EOPEOB>2.0.CO;2.
Rozen, S., Skaletsky, H., Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132 (2000), 365–386.
Ryman, N., Palm, S., André, C., Carvalho, G.R., Dahlgren, T.G., Jorde, P.E., Laikre, L., Larsson, L.C., Palmé, A., Ruzzante, D.E., Power for detecting genetic divergence: differences between statistical methods and marker loci. Mol. Ecol. 15 (2006), 2031–2045, 10.1111/j.1365-294X.2006.02839.x.
Sanger, F., Nicklen, S., Coulson, A.R., DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. U. S. A. 74 (1977), 5463–5467.
Santure, A.W., Stapley, J., Ball, A.D., Birkhead, T.R., Burke, T., Slate, J., On the use of large marker panels to estimate inbreeding and relatedness: empirical and simulation studies of a pedigreed zebra finch population typed at 771 SNPs. Mol. Ecol. 19 (2010), 1439–1451, 10.1111/j.1365-294X.2010.04554.x.
Scarano, E., Iaccarino, M., Grippo, P., Parisi, E., The heterogeneity of thymine methyl group origin in DNA pyrimidine isostichs of developing sea urchin embryos. Proc. Natl. Acad. Sci. U. S. A. 57 (1967), 1394–1400.
Schlötterer, C., The evolution of molecular markers—just a matter of fashion?. Nat. Rev. Genet. 5 (2004), 63–69.
Seeb, J.E., Carvalho, G., Hauser, L., Naish, K., Roberts, S., Seeb, L.W., Single-nucleotide polymorphism (SNP) discovery and applications of SNP genotyping in non model organisms. Mol. Ecol. Resour. 11:Suppl. 1 (2011), 1–8, 10.1111/j.1755-0998.2010.02979.x.
Smitz, N., Berthouly, C., Cornélis, D., Heller, R., Van Hooft, P., Chardonnet, P., Caron, A., Prins, H., van Vuuren, B.J., De Iongh, H., Michaux, J., Pan-African genetic structure in the African buffalo (Syncerus caffer): investigating intraspecific divergence. PLoS One, 8, 2013, e56235, 10.1371/journal.pone.0056235.
Smitz, N., Cornélis, D., Chardonnet, P., Caron, A., De Garine-wichatitsky, M., Jori, F., Mouton, A., Latinne, A., Pigneur, L., Melletti, M., Kanapeckas, K.L., Michaux, J., Genetic structure of fragmented southern populations of African Cape buffalo (Syncerus caffer caffer). BMC Evol. Biol., 2014, 1–19, 10.1186/s12862-014-0203-2.
Stromberg, M.P., 2010. Enabling high-throughput sequencing data analysis with MOSAIK, PhD, Boston College. http://hdl.handle.net/2345/1332.
Van Tassell, C.P., Smith, T.P.L., Matukumalli, L.K., Taylor, J.F., Schnabel, R.D., Lawley, C.T., Haudenschild, C.D., Moore, S.S., Warren, W.C., Sonstegard, T.S., SNP discovery and allele frequency estimation by deep sequencing of reduced representation libraries. Nat. Methods 5 (2008), 247–252, 10.1038/NMETH.1185.
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., Higgins, D.G., The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997), 4876–4882.
Van Bers, N.E.M., van Oers, K., Kerstens, H.H.D., Dibbits, B.W., Crooijmans, R.P.M., Visser, M.E., Groenen, M.A., Genome-wide SNP detection in the great tit Parus major using high throughput sequencing. Mol. Ecol. 19:Suppl. 1 (2010), 89–99, 10.1111/j.1365-294X.2009.04486.x.
Van Hooft, W.F., Hanotte, O., Wenink, P.W., Groen, A.F., Sugimoto, Y., Prins, H.H.T., Teale, A., Applicability of bovine microsatellite markers for population genetic studies on African buffalo (Syncerus caffer). Anim. Genet. 30 (1999), 214–220.
Van Hooft, W.F., Groen, A.F., Prins, H.H.T., Phylogeography of the African buffalo based on mitochondrial and Y-chromosomal loci: pleistocene origin and population expansion of the Cape buffalo subspecies. Mol. Ecol. 11 (2002), 267–279.
Vignal, A., Milan, D., SanCristobal, M., Eggen, A., A review on SNP and other types of molecular markers and their use in animal genetics. Genet. Sel. Evol. 34 (2002), 275–305, 10.1051/gse.
Young, A.G., Clarke, G.M., Genetics, Demography and Viability of Fragmented Populations. 2000, Cambridge University Press, Cambridge.