Abstract
Single nucleotide polymorphisms (SNPs) and insertions-deletions (InDels) are valuable molecular markers for genomics and genetics studies and molecular breeding. The advent of next-generation sequencing techniques has enabled researchers to approach high-throughput and cost-effective SNP and InDel discovery on a genomic scale. In this report, 36 common bean genotypes grown in Canada were used to construct reduced representation libraries for next-generation sequencing. Using 76 million sequence reads generated by the Illumina HiSeq 2000 Sequencing System, we identified a total of 43,698 putative SNPs and 1,267 putative InDels. Of the SNPs, 43,504 were bi-allelic and 194 were tri-allelic, and the InDels comprised 574 insertions and 693 deletions. The putative bi-allelic SNPs were distributed across all 11 chromosomes with the highest number of SNPs observed in chromosome 2 (4,788), and the lowest in chromosome 10 (2,941). With the aid of the recent release of the first chromosome-scale version of Phaseolus vulgaris, 24,907 bi-allelic SNPs, 79 tri-allelic SNPs, 315 insertions, and 377 deletions were located in 8,758, 77, 273, and 364 genes, respectively. Among these 24,907 bi-allelic SNPs, 7,168 nonsynonymous bi-allelic SNPs were identified within 36 common bean genotypes that were located in 4,303 genes. A total of 113 putative SNPs were randomly chosen for validation using high-resolution melt analysis. Of the 113 candidate SNPs, 105 (92.9 %) contained the predicted SNPs.
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References
Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Plant Biol 8:135–141
Altshuler D, Pollara VJ, Cowles CR, Van Etten WJ, Baldwin J, Linton L, Lander ES (2000) An SNP map of the human genome generated by reduced representation shotgun sequencing. Nature 407:513–516
Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815
Arai-Kichise Y, Shiwa Y, Nagasaki H, Ebana K, Yoshikawa H, Yano M, Wakasa K (2011) Discovery of genome-wide DNA polymorphisms in a landrace cultivar of Japonica rice by whole-genome sequencing. Plant Cell Physiol 52:274–282
Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3:e3376
Bennett MD, Leitch IJ (1995) Nuclear DNA amounts in angiosperms. Ann Bot 76:113–176
Bennetzen JL, Ma J, Devos KM (2005) Mechanisms of recent genome size variation in flowering plants. Ann Bot 95:127–132
Bitocchi E, Nanni L, Bellucci E, Rossi M, Giardini A, Zeuli PS, Logozzo G, Stougaard J, McClean P, Attene G, Papa R (2012) Mesoamerican origin of the common bean (Phaseolus vulgaris L.) is revealed by sequence data. Proc Natl Acad Sci USA 109:E788–E796
Blair MW, Cortés AJ, Penmetsa RV, Farmer A, Carrasquilla-Garcia N, Cook DR (2013) A high-throughput SNP marker system for parental polymorphism screening, and diversity analysis in common bean (Phaseolus vulgaris L.). Theor Appl Genet 126:535–548
Choi IY, Hyten DL, Matukumalli LK, Song Q, Chaky JM, Quigley CV, Chase K, Lark KG, Reiter RS, Yoon MS, Hwang EY, Yi SI, Young ND, Shoemaker RC, Van Tassell CP, Specht JE, Cregan PB (2007) A soybean transcript map: gene distribution, haplotype and single-nucleotide polymorphism analysis. Genetics 176:685–696
Clark RM, Schweikert G, Toomajian C, Ossowski S, Zeller G, Shinn P, Warthmann N, Hu TT, Fu G, Hinds DA, Chen H, Frazer KA, Huson DH, Schölkopf B, Nordborg M, Rätsch G, Ecker JR, Weigel D (2007) Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317:338–342
Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12:499–510
Depristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, Del Angel G, Rivas MA, Hanna M, McKenna A, Fennell TJ, Kernytsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuler D, Daly MJ (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43:491–501
Deschamps S, Campbell MA (2010) Utilization of next-generation sequencing platforms in plant genomics and genetic variant discovery. Mol Breed 25:553–570
Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127:1309–1321
Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379
Fonsêca A, Ferreira J, Dos Santos TRB, Mosiolek M, Bellucci E, Kami J, Gepts P, Geffroy V, Schweizer D, Dos Santos KGB, Pedrosa-Harand A (2010) Cytogenetic map of common bean (Phaseolus vulgaris L.). Chromosome Res 18:487–502
Freyre R, Skroch PW, Geffroy V, Adam-Blondon AF, Shirmohamadali A, Johnson WC, Llaca V, Nodari RO, Pereira PA, Tsai SM, Tohme J, Dron M, Nienhuis J, Vallejos CE, Gepts P (1998) Towards an integrated linkage map of common bean. 4. Development of a core linkage map and alignment of RFLP maps. Theor Appl Genet 97:847–856
Fu YB, Peterson GW (2012) Developing genomic resources in two Linum species via 454 pyrosequencing and genomic reduction. Mol Ecol Resour 12:492–500
Gaitan-Solis E, Choi IY, Quigley C, Cregan P, Tohme J (2008) Single nucleotide polymorphisms in common bean: their discovery and genotyping using a multiplex detection system. Plant Genome 1:125–134
Galeano CH, Fernández AC, Gómez M, Blair MW (2009) Single strand conformation polymorphism based SNP and Indel markers for genetic mapping and synteny analysis of common bean (Phaseolus vulgaris L.). BMC Genomics 10:629
Galeano CH, Cortés AJ, Fernández AC, Soler T, Franco-Herrera N, Makunde G, Vanderleyden J, Blair MW (2012) Gene-based single nucleotide polymorphism markers for genetic and association mapping in common bean. BMC Genet 13:48
Gaur R, Azam S, Jeena G, Khan AW, Choudhary S, Jain M, Yadav G, Tyagi AK, Chattopadhyay D, Bhatia S (2012) High-throughput SNP discovery and genotyping for constructing a saturated linkage map of chickpea (Cicer arietinum L.). DNA Res 19:357–373
Gepts P (1998) Origin and evolution of common bean: past events and recent trends. HortScience 33:1124–1130
Gepts P, Debouck D (1991) Origin, domestication, and evolution of the common bean (Phaseolus vulgaris L.). In: van Schoonhaven A, Voysest O (eds) Common beans: research for crop improvement. C.A.B. International, Oxon, pp 7–53
Gepts P, Aragão FL, Barros E, Blair M, Brondani R, Broughton W, Galasso I, Hernández G, Kami J, Lariguet P, McClean P, Melotto M, Miklas P, Pauls P, Pedrosa-Harand A, Porch T, Sánchez F, Sparvoli F, Yu K (2008) Genomics of Phaseolus beans, a major source of dietary protein and micronutrients in the tropics. In: Moore P, Ming R (eds) Genomics of Tropical Crop Plants. Springer, New York, pp 113–143
Hayashi K, Yoshida H, Ashikawa I (2006) Development of PCR-based allele-specific and InDel marker sets for nine rice blast resistance genes. Theor Appl Genet 113:251–260
Herrmann MG, Durtschi JD, Bromley LK, Wittwer CT, Voelkerding KV (2006) Amplicon DNA melting analysis for mutation scanning and genotyping: cross-platform comparison of instruments and dyes. Clin Chem 52:494–503
Hillier LW, Marth GT, Quinlan AR, Dooling D, Fewell G, Barnett D, Fox P, Glasscock JI, Hickenbotham M, Huang W, Magrini VJ, Richt RJ, Sander SN, Stewart DA, Stromberg M, Tsung EF, Wylie T, Schedl T, Wilson RK, Mardis ER (2008) Whole-genome sequencing and variant discovery in C. elegans. Nat Methods 5:183–188
Hufford MB, Xu X, Van Heerwaarden J, Pyhäjärvi T, Chia JM, Cartwright RA, Elshire RJ, Glaubitz JC, Guill KE, Kaeppler SM, Lai J, Morrell PL, Shannon LM, Song C, Springer NM, Swanson-Wagner RA, Tiffin P, Wang J, Zhang G, Doebley J, McMullen MD, Ware D, Buckler ES, Yang S, Ross-Ibarra J (2012) Comparative population genomics of maize domestication and improvement. Nat Genet 44:808–811
Hyten DL, Song Q, Zhu Y, Choi IY, Nelson RL, Costa JM, Specht JE, Shoemaker RC, Cregan PB (2006) Impact of genetic bottlenecks on soybean genome diversity. Proc Natl Acad Sci USA 103:16666–16671
Hyten DL, Cannon SB, Song Q, Weeks N, Fickus EW, Shoemaker RC, Specht JE, Farmer AD, May GD, Cregan PB (2010a) High-throughput SNP discovery through deep resequencing of a reduced representation library to anchor and orient scaffolds in the soybean whole genome sequence. BMC Genomics 11:38
Hyten DL, Song Q, Fickus EW, Quigley CV, Lim JS, Choi IY, Hwang EY, Pastor-Corrales M, Cregan PB (2010b) High-throughput SNP discovery and assay development in common bean. BMC Genomics 11:475
Keller I, Bensasson D, Nichols RA (2007) Transition-transversion bias is not universal: a counter example from grasshopper pseudogenes. PLoS Genet 3:0185–0191
Kumar S, Banks TW, Cloutier S (2012) SNP discovery through next-generation sequencing and its applications. Int J Plant Genomics. Article ID 831460. doi:10.1155/2012/831460
Kwak M, Gepts P (2009) Structure of genetic diversity in the two major gene pools of common bean (Phaseolus vulgaris L., Fabaceae). Theor Appl Genet 118:979–992
Lai J, Li R, Xu X, Jin W, Xu M, Zhao H, Xiang Z, Song W, Ying K, Zhang M, Jiao Y, Ni P, Zhang J, Li D, Guo X, Ye K, Jian M, Wang B, Zheng H, Liang H, Zhang X, Wang S, Chen S, Li J, Fu Y, Springer NM, Yang H, Wang J, Dai J, Schnable PS, Wang J (2010) Genome-wide patterns of genetic variation among elite maize inbred lines. Nat Genet 42:1027–1030
Lai K, Duran C, Berkman PJ, Lorenc MT, Stiller J, Manoli S, Hayden MJ, Forrest KL, Fleury D, Baumann U, Zander M, Mason AS, Batley J, Edwards D (2012) Single nucleotide polymorphism discovery from wheat next-generation sequence data. Plant Biotechnol J 10:743–749
Lam HM, Xu X, Liu X, Chen W, Yang G, Wong FL, Li MW, He W, Qin N, Wang B, Li J, Jian M, Wang J, Shao G, Sun SSM, Zhang G (2010) Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet 42:1053–1059
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760
Mamidi S, Rossi M, Annam D, Moghaddam S, Lee R, Papa R, McClean P (2011) Investigation of the domestication of common bean (Phaseolus vulgaris) using multilocus sequence data. Funct Plant Biol 38:953–967
Mammadov J, Aggarwal R, Buyyarapu R, Kumpatla S (2012) SNP markers and their impact on plant breeding. Int J Plant Genomics. Article ID 728398. doi:10.1155/2012/728398
Maughan PJ, Yourstone SM, Byers RL, Smith SM, Udall JA (2010) Single-nucleotide polymorphism genotyping in mapping populations via genomic reduction and next-generation sequencing: proof of concept. Plant Genome 3:166–178
McClean PE, Lee RK, Otto C, Gepts P, Bassett MJ (2002) Molecular and phenotypic mapping of genes controlling seed coat pattern and color in common bean (Phaseolus vulgaris L.). J Hered 93:148–152
McClean P, Kami J, Gepts P (2004) Genomics and genetic diversity in common bean. In: Wilson RF, Stalker HT, Brummer EC (eds) Legume crop genomics. AOCS Press, Champaign
McConnell M, Mamidi S, Lee R, Chikara S, Rossi M, Papa R, McClean P (2010) Syntenic relationships among legumes revealed using a gene-based genetic linkage map of common bean (Phaseolus vulgaris L.). Theor Appl Genet 121:1103–1116
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303
McNally KL, Childs KL, Bohnert R, Davidson RM, Zhao K, Ulat VJ, Zeller G, Clark RM, Hoen DR, Bureau TE, Stokowski R, Ballinger DG, Frazer KA, Cox DR, Padhukasahasram B, Bustamante CD, Weigel D, Mackill DJ, Bruskiewich RM, Rätsch G, Buell CR, Leung H, Leach JE (2009) Genomewide SNP variation reveals relationships among landraces and modern varieties of rice. Proc Natl Acad Sci USA 106:12273–12278
Nelson JC, Wang S, Wu Y, Li X, Antony G, White FF, Yu J (2011) Single-nucleotide polymorphism discovery by high-throughput sequencing in sorghum. BMC Genomics 12:352
Nielsen R, Paul JS, Albrechtsen A, Song YS (2011) Genotype and SNP calling from next-generation sequencing data. Nat Rev Genet 12:443–451
Oliver RE, Lazo GR, Lutz JD, Rubenfield MJ, Tinker NA, Anderson JM, Wisniewski Morehead NH, Adhikary D, Jellen EN, Maughan PJ, Brown Guedira GL, Chao S, Beattie AD, Carson ML, Rines HW, Obert DE, Bonman JM, Jackson EW (2011) Model SNP development for complex genomes based on hexaploid oat using high-throughput 454 sequencing technology. BMC Genomics 12:77
Ossowski S, Schneeberger K, Clark RM, Lanz C, Warthmann N, Weigel D (2008) Sequencing of natural strains of Arabidopsis thaliana with short reads. Genome Res 18:2024–2033
Ramírez M, Graham MA, Blanco-López L, Silvente S, Medrano-Soto A, Blair MW, Hernández G, Vance CP, Lara M (2005) Sequencing and analysis of common bean ESTs. Building a foundation for functional genomics. Plant Physiol 137:1211–1227
Ratan A, Zhang Y, Hayes VM, Schuster SC, Miller W (2010) Calling SNPs without a reference sequence. BMC Bioinformatics 11:130
Rivkin MI, Vallejos CE, McClean PE (1999) Disease-resistance related sequences in common bean. Genome 42:41–47
Salathia N, Lee HN, Sangster TA, Morneau K, Landry CR, Schellenberg K, Behere AS, Gunderson KL, Cavalieri D, Jander G, Queitsch C (2007) Indel arrays: an affordable alternative for genotyping. Plant J 51:727–737
Sasaki T (2005) The map-based sequence of the rice genome. Nature 436:793–800
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183
Shen YJ, Jiang H, Jin JP, Zhang ZB, Xi B, He YY, Wang G, Wang C, Qian L, Li X, Yu QB, Liu HJ, Chen DH, Gao JH, Huang H, Shi TL, Yang ZN (2004) Development of genome-wide DNA polymorphism database for map-based cloning of rice genes. Plant Physiol 135:1198–1205
Shendure J, Ji H (2008) Next-generation DNA sequencing. Nat Biotechnol 26:1135–1145
Shi C, Navabi A, Yu K (2011) Association mapping of common bacterial blight resistance QTL in Ontario bean breeding populations. BMC Plant Biol 11:52
Singh SP, Gepts P, Debouck DG (1991) Races of common bean (Phaseolus vulgaris, Fabaceae). Econ Bot 45:379–396
Souza TLPO, de Barros EG, Bellato CM, Hwang EY, Cregan PB, Pastor-Corrales MA (2012) Single nucleotide polymorphism discovery in common bean. Mol Breed 30:419–428
Subbaiyan GK, Waters DLE, Katiyar SK, Sadananda AR, Vaddadi S, Henry RJ (2012) Genome-wide DNA polymorphisms in elite indica rice inbreds discovered by whole-genome sequencing. Plant Biotechnol J 10:623–634
Treangen TJ, Salzberg SL (2012) Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat Rev Genet 13:36–46
Vallad G, Rivkin M, Vallejos C, McClean P (2001) Cloning and homology modelling of a Pto-like protein kinase family of common bean (Phaseolus vulgaris L.). Theor Appl Genet 103:1046–1058
Vallejos CE, Sakiyama NS, Chase CD (1992) A molecular marker-based linkage map of Phaseolus vulgaris L. Genetics 131:733–740
van Orsouw NJ, Hogers RCJ, Janssen A, Yalcin F, Snoeijers S, Verstege E, Schneiders H, van der Poel H, van Oeveren J, Verstegen H, van Eijk MJT (2007) Complexity reduction of polymorphic sequences (CRoPS™): a novel approach for large-scale polymorphism discovery in complex genomes. PLoS ONE 2:e1172
Van Tassell CP, Smith TPL, Matukumalli LK, Taylor JF, Schnabel RD, Lawley CT, Haudenschild CD, Moore SS, Warren WC, Sonstegard TS (2008) SNP discovery and allele frequency estimation by deep sequencing of reduced representation libraries. Nat Methods 5:247–252
Varshney RK, Nayak SN, May GD, Jackson SA (2009) Next-generation sequencing technologies and their implications for crop genetics and breeding. Trends Biotechnol 27:522–530
Wang DG, Fan JB, Siao CJ, Berno A, Young P, Sapolsky R, Ghandour G, Perkins N, Winchester E, Spencer J, Kruglyak L, Stein L, Hsie L, Topaloglou T, Hubbell E, Robinson E, Mittmann M, Morris MS, Shen N, Kilburn D, Rioux J, Nusbaum C, Rozen S, Hudson TJ, Lipshutz R, Chee M, Lander ES (1998) Large-scale identification, mapping, and genotyping of single- nucleotide polymorphisms in the human genome. Science 280:1077–1082
Wang K, Li M, Hakonarson H (2010) ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 38:e164
Wang Y, Yu KF, Poysa V, Shi C, Zhou YH (2012) A single point mutation in GmHMA3 affects Cadimum (Cd) translocation and accumulation in soybean seeds. Mol Plant 5:1154–1156
Wu X, Ren C, Joshi T, Vuong T, Xu D, Nguyen HT (2010) SNP discovery by high-throughput sequencing in soybean. BMC Genomics 11:469
You FM, Huo N, Deal KR, Gu YQ, Luo MC, McGuire PE, Dvorak J, Anderson OD (2011) Annotation-based genome-wide SNP discovery in the large and complex Aegilops tauschii genome using next-generation sequencing without a reference genome sequence. BMC Genomics 12:59
Zhu YL, Song QJ, Hyten DL, Van Tassell CP, Matukumalli LK, Grimm DR, Hyatt SM, Fickus EW, Young ND, Cregan PB (2003) Single-nucleotide polymorphisms in soybean. Genetics 163:1123–1134
Acknowledgments
We thank Dr. Sergio Pereira and the bioinformatics team at The Centre for Applied Genomics, The Hospital for Sick Children for the next-generation sequencing and data analysis. Phaseolus vulgaris v1.0 data were produced by the US Department of Energy Joint Genome Institute http://www.jgi.doe.gov/ in collaboration with the user community. This work is supported by Ontario Research Fund (ORF), Ontario White Bean Producers’ Marketing Board (OWBPMB), Ontario Colored Bean Growers’ Association (OCBGA), and Agriculture and Agri-Food Canada (AAFC).
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Zou, X., Shi, C., Austin, R.S. et al. Genome-wide single nucleotide polymorphism and Insertion-Deletion discovery through next-generation sequencing of reduced representation libraries in common bean. Mol Breeding 33, 769–778 (2014). https://doi.org/10.1007/s11032-013-9997-7
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DOI: https://doi.org/10.1007/s11032-013-9997-7