Transcriptome sequencing of wild chickpea as a rich resource for marker development
Shalu Jhanwar,
Pushp Priya,
Rohini Garg,
Swarup K. Parida,
Akhilesh K. Tyagi,
Mukesh Jain,
Shalu Jhanwar
National Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi, India
Search for more papers by this authorPushp Priya
National Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi, India
Search for more papers by this authorRohini Garg
National Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi, India
Search for more papers by this authorSwarup K. Parida
National Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi, India
Search for more papers by this authorAkhilesh K. Tyagi
National Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi, India
Search for more papers by this authorCorresponding Author
Mukesh Jain
(Tel 91 11 26735182; fax 91 11 26741658; email [email protected])Search for more papers by this authorShalu Jhanwar,
Pushp Priya,
Rohini Garg,
Swarup K. Parida,
Akhilesh K. Tyagi,
Mukesh Jain,
Shalu Jhanwar
National Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi, India
Search for more papers by this authorPushp Priya
National Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi, India
Search for more papers by this authorRohini Garg
National Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi, India
Search for more papers by this authorSwarup K. Parida
National Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi, India
Search for more papers by this authorAkhilesh K. Tyagi
National Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi, India
Search for more papers by this authorCorresponding Author
Mukesh Jain
(Tel 91 11 26735182; fax 91 11 26741658; email [email protected])Search for more papers by this authorSummary
The transcriptome of cultivated chickpea (Cicer arietinum L.), an important crop legume, has recently been sequenced. Here, we report sequencing of the transcriptome of wild chickpea, C. reticulatum (PI489777), the progenitor of cultivated chickpea, by GS-FLX 454 technology. The optimized assembly of C. reticulatum transcriptome generated 37 265 transcripts in total with an average length of 946 bp. A total of 4072 simple sequence repeats (SSRs) could be identified in these transcript sequences, of which at least 561 SSRs were polymorphic between C. arietinum and C. reticulatum. In addition, a total of 36 446 single-nucleotide polymorphisms (SNPs) were identified after optimization of probability score, quality score, read depth and consensus base ratio. Several of these SSRs and SNPs could be associated with tissue-specific and transcription factor encoding transcripts. A high proportion (92–94%) of polymorphic SSRs and SNPs identified between the two chickpea species were validated successfully. Further, the estimation of synonymous substitution rates of orthologous transcript pairs suggested that the speciation event for divergence of C. arietinum and C. reticulatum may have happened approximately 0.53 million years ago. The results of our study provide a rich resource for exploiting genetic variations in chickpea for breeding programmes.
Supporting Information
Figure S1 Length (A) and average quality score (B) distribution of total number of high-quality reads generated for Cicer reticulatum.
Figure S2 Length distribution (A) and read depth distribution (B) of C. reticulatum transcripts generated from optimized assembly.
Figure S3 GC content of C. arietinum and C. reticulatum transcripts. The average GC content of each transcript was calculated and percentage of transcripts with GC content within a range are represented.
Figure S4 Functional annotation of C. arietinum and C. reticulatum transcripts. GOSlim term assignment to the transcripts in different categories of biological process, molecular function and cellular component.
Figure S5 Distribution of polymorphic SSRs at various transcript positions.
Figure S6 Number of SNPs as a function of probability (A) and average Phred quality score (B) cut-off.
Figure S7 Number of SNPs and SNP containing transcripts as a function of read depth at base consensus ratio of 0.9 (A) and 1.0 (B).
Figure S8 Distribution of SNPs at various transcript positions.
Table S1 Statistics of SSRs identified in C. reticulatum transcripts.
Table S2 Frequency of SSRs identified in C. reticulatum transcripts.
Table S3 List of polymorphic SSRs identified between C. arietinum and C. reticulatum.
Table S4 List of SNPs identified between C. arietinum and C. reticulatum.
Table S5 Validation of 96 selected polymorphic SSRs between C. arietinum and C. reticulatum.
Table S6 Validation of 24 selected SNPs between C. arietinum and C. reticulatum using CAPS genotyping assay.
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| PBI_712_sm_FigS1-S8-TableS1-S3-S5-S6.pdf1.7 MB | Supporting info item |
| PBI_712_sm_TableS4.pdf3 MB | Supporting info item |
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References
- Ahmad, F., Gaur, P.M. and Slinkard, A.E. (1992) Isozyme polymorphism and phylogenetic interpretations in the genus Cicer L. Theor. Appl. Genet. 83, 620–627.
- Aluko, G., Martinez, C., Tohme, J., Castano, C., Bergman, C. and Oard, J.H. (2004) QTL mapping of grain quality traits from the interspecific cross Oryza sativa x O. glaberrima. Theor. Appl. Genet. 109, 630–639.
- Barbazuk, W.B., Emrich, S.J., Chen, H.D., Li, L. and Schnable, P.S. (2007) SNP discovery via 454 transcriptome sequencing. Plant J. 51, 910–918.
- Blanc, G. and Wolfe, K.H. (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell, 16, 1667–1678.
- Buell, C.R. (2009) Poaceae genomes: going from unattainable to becoming a model clade for comparative plant genomics. Plant Physiol. 149, 111–116.
- Bundock, P.C., Eliott, F.G., Ablett, G., Benson, A.D., Casu, R.E., Aitken, K.S. and Henry, R.J. (2009) Targeted single nucleotide polymorphism (SNP) discovery in a highly polyploid plant species using 454 sequencing. Plant Biotechnol. J. 7, 347–354.
- Choi, I.Y., Hyten, D.L., Matukumalli, L.K., Song, Q., Chaky, J.M., Quigley, C.V., Chase, K., Lark, K.G., Reiter, R.S., Yoon, M.S., Hwang, E.Y., Yi, S.I., Young, N.D., Shoemaker, R.C., van Tassell, C.P., Specht, J.E. and Cregan, P.B. (2007) A soybean transcript map: gene distribution, haplotype and single-nucleotide polymorphism analysis. Genetics, 176, 685–696.
- Choudhary, S., Sethy, N.K., Shokeen, B. and Bhatia, S. (2009) Development of chickpea EST-SSR markers and analysis of allelic variation across related species. Theor. Appl. Genet. 118, 591–608.
- Collard, B.C.Y., Ades, P.K., Pang, E.C.K., Brouwer, J.B. and Taylor, P.W.J. (2001) Prospecting for sources of resistance to aschochyta blight in wild Cicer species. Aust. Plant Pathol. 30, 271–276.
- Duran, C., Appleby, N., Clark, T., Wood, D., Imelfort, M., Batley, J. and Edwards, D. (2009) AutoSNPdb: an annotated single nucleotide polymorphism database for crop plants. Nucleic Acids Res. 37, D951–D953.
- Galasso, I., Pignone, D., Frediani, M., Maggiani, M. and Cremonini, R. (1996) Chromatin characterization by banding techniques, in situ hybridization, and nuclear DNA content in Cicer L. (Leguminosae). Genome, 39, 258–265.
- Garg, R., Sahoo, A., Tyagi, A.K. and Jain, M. (2010) Validation of internal control genes for quantitative gene expression studies in chickpea (Cicer arietinum L.). Biochem. Biophys. Res. Commun. 396, 283–288.
- Garg, R., Patel, R.K., Jhanwar, S., Priya, P., Bhattacharjee, A., Yadav, G., Bhatia, S., Chattopadhyay, D., Tyagi, A.K. and Jain, M. (2011a) Gene discovery and tissue-specific transcriptome analysis in chickpea with massively parallel pyrosequencing and web resource development. Plant Physiol. 156, 1661–1678.
- Garg, R., Patel, R.K., Tyagi, A.K. and Jain, M. (2011b) De novo assembly of chickpea transcriptome using short reads for gene discovery and marker identification. DNA Res. 18, 53–63.
- Grover, A., Aishwarya, V. and Sharma, P.C. (2007) Biased distribution of microsatellite motifs in the rice genome. Mol. Genet. Genomics 277, 469–480.
- Gujaria, N., Kumar, A., Dauthal, P., Dubey, A., Hiremath, P., Bhanu Prakash, A., Farmer, A., Bhide, M., Shah, T., Gaur, P.M., Upadhyaya, H.D., Bhatia, S., Cook, D.R., May, G.D. and Varshney, R.K. (2011) Development and use of genic molecular markers (GMMs) for construction of a transcript map of chickpea (Cicer arietinum L.). Theor. Appl. Genet. 122, 1577–1589.
- Guo, M., Rupe, M.A., Danilevskaya, O.N., Yang, X. and Hu, Z. (2003) Genome-wide mRNA profiling reveals heterochronic allelic variation and a new imprinted gene in hybrid maize endosperm. Plant J. 36, 30–44.
- Haware, M.P., Narayana, R.J. and Pundir, R.P.S. (1992) Evaluation of wild Cicer species for resistance to four chickpea diseases. Int. Chickpea Newslett. 27, 16–18.
- Hillier, L.W., Marth, G.T., Quinlan, A.R., Dooling, D., Fewell, G., Barnett, D., Fox, P., Glasscock, J.I., Hickenbotham, M., Huang, W., Magrini, V.J., Richt, R.J., Sander, S.N., Stewart, D.A., Stromberg, M., Tsung, E.F., Wylie, T., Schedl, T., Wilson, R.K. and Mardis, E.R. (2008) Whole-genome sequencing and variant discovery in C. elegans. Nat. Methods, 5, 183–188.
- Hiremath, P.J., Farmer, A., Cannon, S.B., Woodward, J., Kudapa, H., Tuteja, R., Kumar, A., Bhanuprakash, A., Mulaosmanovic, B., Gujaria, N., Krishnamurthy, L., Gaur, P.M., Kavikishor, P.B., Shah, T., Srinivasan, R., Lohse, M., Xiao, Y., Town, C.D., Cook, D.R., May, G.D. and Varshney, R.K. (2011) Large-scale transcriptome analysis in chickpea (Cicer arietinum L.), an orphan legume crop of the semi-arid tropics of Asia and Africa. Plant Biotechnol. J. 9, 922–931.
- Hisano, H., Sato, S., Isobe, S., Sasamoto, S., Wada, T., Matsuno, A., Fujishiro, T., Yamada, M., Nakayama, S., Nakamura, Y., Watanabe, S., Harada, K. and Tabata, S. (2007) Characterization of the soybean genome using EST-derived microsatellite markers. DNA Res. 14, 271–281.
- Hüttel, B., Winter, P., Weising, K., Choumane, W., Weigand, F. and Kahl, G. (1999) Sequence-tagged microsatellite site markers for chickpea (Cicer arietinum L.). Genome, 42, 210–217.
- Iruela, M., Rubio, J., Cubero, J.I., Gil, J. and Millan, T. (2002) Phylogenetic analysis in the genus Cicer and cultivated chickpea using RAPD and ISSR markers. Theor. Appl. Genet. 104, 643–651.
- Kashi, Y. and King, D.G. (2006) Simple sequence repeats as advantageous mutators in evolution. Trends Genet. 22, 253–259.
- Kim, M.Y., Lee, S., Van, K., Kim, T.H., Jeong, S.C., Choi, I.Y., Kim, D.S., Lee, Y.S., Park, D., Ma, J., Kim, W.Y., Kim, B.C., Park, S., Lee, K.A., Kim, D.H., Kim, K.H., Shin, J.H., Jang, Y.E., Kim, K.D., Liu, W.X., Chaisan, T., Kang, Y.J., Lee, Y.H., Moon, J.K., Schmutz, J., Jackson, S.A., Bhak, J. and Lee, S.H. (2010) Whole-genome sequencing and intensive analysis of the undomesticated soybean (Glycine soja Sieb. and Zucc.) genome. Proc. Natl. Acad. Sci. USA 107, 22032–22037.
- Koch, M.A., Haubold, B. and Mitchell-Olds, T. (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol. Biol. Evol. 17, 1483–1498.
- Koski, L.B., Gray, M.W., Lang, B.F. and Burger, G. (2005) AutoFACT: an automatic functional annotation and classification tool. BMC Bioinformatics, 6, 151.
- La Rota, M., Kantety, R.V., Yu, J.K. and Sorrells, M.E. (2005) Nonrandom distribution and frequencies of genomic and EST-derived microsatellite markers in rice, wheat, and barley. BMC Genomics, 6, 23.
- Labdi, M., Robertson, L.D., Singh, K.B. and Charrier, A. (1996) Genetic diversity and phylogenetic relationships among the annual Cicer species as revealed by isozyme polymorphisms. Euphytica, 88, 181–188.
- Lichtenzveig, J., Scheuring, C., Dodge, J., Abbo, S. and Zhang, H.B. (2005) Construction of BAC and BIBAC libraries and their applications for generation of SSR markers for genome analysis of chickpea, Cicer arietinum L. Theor. Appl. Genet. 110, 492–510.
- Lowe, K.M. and Walker, M.A. (2006) Genetic linkage map of the interspecific grape rootstock cross Ramsey (Vitis champinii) x Riparia Gloire (Vitis riparia). Theor. Appl. Genet. 112, 1582–1592.
- Margulies, M., Egholm, M., Altman, W.E., Attiya, S., Bader, J.S., Bemben, L.A., Berka, J., Braverman, M.S., Chen, Y.J., Chen, Z., Dewell, S.B., Du, L., Fierro, J.M., Gomes, X.V., Godwin, B.C., He, W., Helgesen, S., Ho, C.H., Irzyk, G.P., Jando, S.C., Alenquer, M.L., Jarvie, T.P., Jirage, K.B., Kim, J.B., Knight, J.R., Lanza, J.R., Leamon, J.H., Lefkowitz, S.M., Lei, M., Li, J., Lohman, K.L., Lu, H., Makhijani, V.B., McDade, K.E., McKenna, M.P., Myers, E.W., Nickerson, E., Nobile, J.R., Plant, R., Puc, B.P., Ronan, M.T., Roth, G.T., Sarkis, G.J., Simons, J.F., Simpson, J.W., Srinivasan, M., Tartaro, K.R., Tomasz, A., Vogt, K.A., Volkmer, G.A., Wang, S.H., Wang, Y., Weiner, M.P., Yu, P., Begley, R.F. and Rothberg, J.M. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature, 437, 376–380.
- Marth, G.T., Korf, I., Yandell, M.D., Yeh, R.T., Gu, Z., Zakeri, H., Stitziel, N.O., Hillier, L., Kwok, P.Y. and Gish, W.R. (1999) A general approach to single-nucleotide polymorphism discovery. Nat. Genet. 23, 452–456.
- McNally, K.L., Childs, K.L., Bohnert, R., Davidson, R.M., Zhao, K., Ulat, V.J., Zeller, G., Clark, R.M., Hoen, D.R., Bureau, T.E., Stokowski, R., Ballinger, D.G., Frazer, K.A., Cox, D.R., Padhukasahasram, B., Bustamante, C.D., Weigel, D., Mackill, D.J., Bruskiewich, R.M., Rätsch, G., Buell, C.R., Leung, H. and Leach, J.E. (2009) Genome wide SNP variation reveals relationships among landraces and modern varieties of rice. Proc. Natl. Acad. Sci. USA 106, 12273–12278.
- Metzgar, D., Bytof, J. and Wills, C. (2000) Selection against frameshift mutations limits microsatellite expansion in coding DNA. Genome Res. 10, 72–80.
- Milano, I., Babbucci, M., Panitz, F., Ogden, R., Nielsen, R.O., Taylor, M.I., Helyar, S.J., Carvalho, G.R., Espiñeira, M., Atanassova, M., Tinti, F., Maes, G.E., Patarnello, T., FishPopTrace Consortium and Bargelloni, L. (2011) Novel tools for conservation genomics: comparing two high-throughput approaches for SNP discovery in the transcriptome of the European hake. PLoS ONE, 6, e28008.
- Nayak, S.N., Zhu, H., Varghese, N., Datta, S., Choi, H.-K., Horres, R., Jüngling, R., Singh, J., Kavi Kishor, P.B., Sivaramakrihnan, S., Hoisington, D.A., Kahl, G., Winter, P., Cook, D.R. and Varshney, R.K. (2010) Integration of novel SSR and gene-based SNP marker loci in the chickpea genetic map and establishment of new anchor points with Medicago truncatula genome. Theor. Appl.Genet. 120, 1415–1441.
- Nelson, J.C., Wang, S., Wu, Y., Li, X., Antony, G., White, F.F. and Yu, J. (2011) Single-nucleotide polymorphism discovery by high-throughput sequencing in sorghum. BMC Genomics, 12, 352.
- Nguyen, T.T., Taylor, P.W.J., Redden, R.J. and Ford, R. (2004) Genetic diversity estimates in Cicer using AFLP analysis. Plant Breeding, 123, 173–179.
- Novaes, E., Drost, D.R., Farmerie, W.G., Pappas Jr, G.J., Grattapaglia, D., Sederoff, R.R. and Kirst, M. (2008) High-throughput gene and SNP discovery in Eucalyptus grandis, an uncharacterized genome. BMC Genomics, 9, 312.
- Parida, S.K., Anand, R.K.K., Dalal, V., Singh, N.K. and Mohapatra, T. (2006) Unigene derived microsatellite markers for the cereal genomes. Theor. Appl. Genet. 112, 808–817.
- Patel, R.K. and Jain, M. (2012) NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS ONE, 7, e30619.
- Picoult-Newberg, L., Ideker, T.E., Pohl, M.G., Taylor, S.L., Donaldson, M.A., Nickerson, D.A. and Boyce-Jacino, M. (1999) Mining SNPs from EST databases. Genome Res. 9, 167–174.
- Radhika, P., Gowda, S.J., Kadoo, N.Y., Mhase, L.B., Jamadagni, B.M., Sainani, M.N., Chandra, S. and Gupta, V.S. (2007) Development of an integrated intraspecific map of chickpea (Cicer arietinum L.) using two recombinant inbred line populations. Theor. Appl. Genet. 115, 209–216.
- Rafalski, A. (2002) Applications of single nucleotide polymorphisms in crop genetics. Curr. Opin. Plant Biol. 5, 94–100.
- Ragoussis, J. (2009) Genotyping technologies for genetic research. Annu. Rev. Genomics Hum. Genet. 10, 117–133.
- Schlueter, J.A., Dixon, P., Granger, C., Grant, D., Clark, L., Doyle, J.J. and Shoemaker, R.C. (2004) Mining EST databases to resolve evolutionary events in major crop species. Genome 47, 868–876.
- Schmutz, J., Cannon, S.B., Schlueter, J., Ma, J., Mitros, T., Nelson, W., Hyten, D.L., Song, Q., Thelen, J.J., Cheng, J., Xu, D., Hellsten, U., May, G.D., Yu, Y., Sakurai, T., Umezawa, T., Bhattacharyya, M.K., 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, X.C., Shinozaki, K., Nguyen, H.T., Wing, R.A., Cregan, P., Specht, J., Grimwood, J., Rokhsar, D., Stacey, G., Shoemaker, R.C. and Jackson, S.A. (2010) Genome sequence of the palaeopolyploid soybean. Nature, 463, 178–183.
- Sethy, N.K., Choudhary, S., Shokeen, B. and Bhatia, S. (2006a) Identification of microsatellite markers from Cicer reticulatum: molecular variation and phylogenetic analysis. Theor. Appl. Genet. 112, 347–357.
- Sethy, N.K., Shokeen, B., Edwards, K.J. and Bhatia, S. (2006b) Development of microsatellite markers and analysis of intraspecific genetic variability in chickpea (Cicer arietinum L.). Theor. Appl. Genet. 112, 1416–1428.
- Sharma, H.C., Pampapathy, G., Lanka, S.K. and Ridsdill-Smith, T.J. (2005) Exploitation of wild Cicer reticulatum germplasm for resistance to Helicoverpa armigera. J. Econ. Entomol. 98, 2246–2253.
- Singh, K.B., Malhotra, R.S., Halila, M.H., Knights, E.J. and Verma, M.M. (1994) Current status and future strategy in breeding chickpea for resistance to biotic and abiotic stresses. Euphytica, 73, 137–149.
- Singh, K.B., Ocampo, B. and Robertson, L.D. (1998) Diversity for abiotic and biotic stress resistance in the wild annual Cicer species. Genet. Resour. Crop Evol. 45, 9–17.
- Singh, R., Sharma, P., Varshney, R.K., Sharma, S.K. and Singh, N.K. (2008) Chickpea improvement: role of wild species and genetic markers. Biotechnol. Genet. Eng. Rev. 25, 267–314.
- Smith, D.R., Quinlan, A.R., Peckham, H.E., Makowsky, K., Tao, W., Woolf, B., Shen, L., Donahue, W.F., Tusneem, N., Stromberg, M.P., Stewart, D.A., Zhang, L., Ranade, S.S., Warne, r.J.B., Lee, C.C., Coleman, B.E., Zhang, Z., McLaughlin, S.F., Malek, J.A., Sorenson, J.M., Blanchard, A.P., Chapman, J., Hillman, D., Chen, F., Rokhsar, D.S., McKernan, K.J., Jeffries, T.W., Marth, G.T. and Richardson, P.M. (2008) Rapid whole-genome mutational profiling using next-generation sequencing technologies. Genome Res. 18, 1638–1642.
- Srivastava, A., Rogers, W.L., Breton, C.M., Cai, L. and Malmberg, R.L. (2011) Transcriptome analysis of Sarracenia, an insectivorous plant. DNA Res. 18, 253–261.
- Stupar, R.M. and Springer, N.M. (2006) Cis-transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid. Genetics, 173, 2199–2210.
- Suyama, M., Torrents, D. and Bork, P. (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34, W609–W612.
- Tang, J., Baldwin, S.J., Jacobs, J.M., Linden, C.G., Voorrips, R.E., Leunissen, J.A., van Eck, H. and Vosman, B. (2008) Large-scale identification of polymorphic microsatellites using an in silico approach. BMC Bioinformatics, 9, 374.
- Tayyar, R.I., Lukaszewski, A.J. and Waines, J.G. (1994) Chromosome banding patterns in the annual species of Cicer. Genome, 37, 656–663.
- Thiel, T., Michalek, W., Varshney, R.K. and Graner, A. (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor. Appl. Genet. 106, 411–422.
- Udupa, S.M., Sharma, A., Sharma, A.P. and Pai, R.A. (1993) Narrow genetic variability in Cicer arietinum L. as revealed by RFLP analysis. J. Plant Biochem. Biotechnol. 2, 83–86.
- Varshney, R.K., Graner, A. and Sorrells, M.E. (2005) Genic microsatellite markers in plants: features and applications. Trends Biotechnol. 23, 48–55.
- Varshney, R.K., Thiel, T., Sretenovic-Rajicic, T., Baum, M., Valkoun, J., Guo, P., Grando, S., Ceccarelli, S. and Graner, A. (2008) Identification and validation of a core set of informative genic SSR and SNP markers for assaying functional diversity in barley. Mol. Breed. 22, 1–13.
- Winter, P., Pfaff, T., Udupa, S.M., Hüttel, B., Sharma, P.C., Sahi, S., Arreguin-Espinoza, R., Weigand, F., Muehlbauer, F.J. and Kahl, G. (1999) Characterization and mapping of sequence-tagged microsatellite sites in the chickpea (Cicer arietinum L.) genome. Mol. Gen. Genet. 262, 90–101.
- Wu, X., Ren, C., Joshi, T., Vuong, T., Xu, D. and Nguyen, H.T. (2010) SNP discovery by high-throughput sequencing in soybean. BMC Genomics, 11, 469.
- Yamamoto, T., Kimura, T., Shoda, M., Imai, T., Saito, T., Sawamura, Y., Kotobuki, K., Hayashi, T. and Matsuta, N. (2002) Genetic linkage maps constructed by using an interspecific cross between Japanese and European pears. Theor. Appl. Genet. 106, 9–18.
- Yang, Z. (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591.
- Zhang, Z., Deng, Y., Tan, J., Hu, S., Yu, J. and Xue, Q. (2007) A genome-wide microsatellite polymorphism database for the indica and japonica rice. DNA Res. 14, 37–45.
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