Horticulture, Environment, and Biotechnology

, Volume 56, Issue 6, pp 800–810 | Cite as

Assessing the genetic variation in cultivated tomatoes (Solanum lycopersicum L.) using genome-wide single nucleotide polymorphisms

  • Sung-Chur Sim
  • Myungkwon Kim
  • Sang-Min Chung
  • Younghoon Park
Research Report

Abstract

Tomato (Solanum lycopersicum L.) is an economically important vegetable crop worldwide. Recently, a high-density single nucleotide polymorphism (SNP) array was developed based on genome-wide SNPs in tomato. In this study, we genotyped a collection of 48 Korean elite tomato varieties (26 fresh market and 22 cultivated cherry) using 7,720 SNPs of this array. Out of 6,652 polymorphic SNPs (86.1%) in the entire collection, there were 6,589 SNPs with < 10% missing data. The number of polymorphic SNPs in the fresh market and cultivated cherry subpopulations were 4,733 (61.3%) and 6,087 (78.8%), respectively. To examine the genetic variation between sub-populations, the SNP genotypes of the Korean tomato germplasm were analyzed along with the previously reported data on SNPs of the 277 Solanaceae Agricultural Coordinated Project (SolCAP) varieties (109 fresh market, 27 cultivated cherry, and 141 processing). Principal component analysis, pairwise Fst, and Nei’s standard genetic distance revealed genetic differentiation between these five sub-populations. Moreover, we validated another division within the Korean cherry varieties using the unweighted pair group mean algorithm (UPGMA). The genetic diversity of each sub-population was estimated based on allelic richness and expected heterozygosity. The fresh market and cultivated cherry sub-populations in the Korean tomato germplasm showed similar levels of genetic diversity as the corresponding SolCAP sub-populations. Visualization of the polymorphic information revealed genomic regions that differed between the two sub-populations in the Korean tomato germplasm. These results suggest that diversifying selection for market niches and environmental adaptation has led to allelic variation in cultivated tomatoes in Korea.

Additional key words

genetic differentiation genetic diversity population level analysis SNP variation 

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Literature Cited

  1. Agarwal, S. and A.V. Rao. 2000. Tomato lycopene and its role in human health and chronic diseases. Can. Med. Assoc. J. 163:739–744.Google Scholar
  2. Barrantes, W., A. Fernandez-del-Carmen, G. Lopez-Casado, M.A. Gonzalez-Sanchez, R. Fernandez-Munoz, A. Granell, and A.J. Monforte. 2014. Highly efficient genomics-assisted development of a library of introgression lines of Solanum pimpinellifolium. Mol. Breed. 34:1817–1831.CrossRefGoogle Scholar
  3. Blanca, J., J. Canizares, L. Cordero, L. Pascual, M.J. Diez, and F. Nuez. 2012. Variation revealed by SNP genotyping and morphology provides insight into the origin of the tomato. PLoS ONE 7:e48198.Google Scholar
  4. Blanca, J., J. Montero-Pau, C. Sauvage, G. Bauchet, E. Illa, M.J. Diez, D. Francis, M. Causse, E. van der Knaap, and J. Canizares. 2015. Genomic variation in tomato, from wild ancestors to contemporary breeding accessions. BMC Genomics 16:257.Google Scholar
  5. Botstein, D., R.L. White, M. Skolnick, and R.W. Davis. 1980. Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am. J. Hum. Genet. 32:314–331.PubMedPubMedCentralGoogle Scholar
  6. Corrado, G., P. Piffanelli, M. Caramante, M. Coppola, and R. Rao. 2013. SNP genotyping reveals genetic diversity between cultivated landraces and contemporary varieties of tomato. BMC Genomics 14:835.PubMedPubMedCentralCrossRefGoogle Scholar
  7. Dieringer, D. and C. Schlotterer. 2003. MICROSATELLITE ANALYSER (MSA): a platform independent analysis tool for large microsatellite data sets. Mol. Ecol. Notes 3:167–169.CrossRefGoogle Scholar
  8. El Mousadik, A. and R.J. Petit. 1996. High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L) Skeels] endemic to Morocco. Theor. Appl. Genet. 92:832–839.PubMedCrossRefGoogle Scholar
  9. Gupta, P.K., S. Rustgi, and R.R. Mir. 2008. Array-based high-throughput DNA markers for crop improvement. Heredity 101:5–18.PubMedCrossRefGoogle Scholar
  10. Hamilton, J.P., S.C. Sim, K. Stoffel, A. Van Deynze, C.R. Buell, and D.M. Francis. 2012. Single nucleotide polymorphism discovery in cultivated tomato via sequencing by synthesis. The Plant Genome 5:17–29.CrossRefGoogle Scholar
  11. Hurlbert, S.H. 1971. The nonconcept of species diversity: a critique and alternative parameters. Ecology 52:577–586.CrossRefGoogle Scholar
  12. Jiménez-Gómez, J. and J. Maloof. 2009. Sequence diversity in three tomato species: SNPs, markers, and molecular evolution. BMC Plant Biol. 9:85.PubMedPubMedCentralCrossRefGoogle Scholar
  13. Jones, D.A., C.M. Thomas, K.E. Hammondkosack, P.J. Balintkurti, and J.D.G. Jones. 1994. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789–793.PubMedCrossRefGoogle Scholar
  14. Kawchuk, L.M., J. Hachey, D.R. Lynch, F. Kulcsar, G. van Rooijen, D.R. Waterer, A. Robertson, E. Kokko, R. Byers, R.J. Howard, R. Fischer, and D. Prufer. 2001. Tomato Ve disease resistance genes encode cell surface-like receptors. Proc. Natl. Acad. Sci. USA 98:6511–6515.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Krzywinski, M.I., J.E. Schein, I. Birol, J. Connors, R. Gascoyne, D. Horsman, S.J. Jones, and M.A. Marra. 2009. Circos: An information aesthetic for comparative genomics. Genome Res. 19:1639–1645.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Labate, J.A. and A.M. Baldo. 2005. Tomato SNP discovery by EST mining and resequencing. Mol. Breed. 16:343–349.CrossRefGoogle Scholar
  17. Labate, J.A., L.D. Robertson, F.N. Wu, S.D. Tanksley, and A.M. Baldo. 2009. EST, COSII, and arbitrary gene markers give similar estimates of nucleotide diversity in cultivated tomato (Solanum lycopersicum L.). Theor. Appl. Genet. 118:1005–1014.PubMedCrossRefGoogle Scholar
  18. Lin, T., G. Zhu, J. Zhang, X. Xu, Q. Yu, Z. Zheng, Z. Zhang, Y. Lun, S. Li, X. Wang, Z. Huang, J. Li, C. Zhang, T. Wang, Y. Zhang, A. Wang, Y. Zhang, K. Lin, C. Li, G. Xiong, Y. Xue, A. Mazzucato, M. Causse, Z. Fei, J. J. Giovannoni, R. T. Chetelat, D. Zamir, T. Stadler, J. Li, Z. Ye, Y. Du, and S. Huang. 2014. Genomic analyses provide insights into the history of tomato breeding. Nat. Genet. 46:1220–1226.PubMedCrossRefGoogle Scholar
  19. Martin, G.B., S.H. Brommonschenkel, J. Chunwongse, A. Frary, M.W. Ganal, R. Spivey, T. Wu, E.D. Earle, and S.D. Tanksley. 1993. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–1436.PubMedCrossRefGoogle Scholar
  20. Miller, J.C., and S.D. Tanksley. 1990. RFLP analysis of phylogenetic relationships and genetic variation in the genus Lycopersicon. Theor. Appl. Genet. 80:437–448.PubMedGoogle Scholar
  21. Milligan, S.B., J. Bodeau, J. Yaghoobi, I. Kaloshian, P. Zabel, and V.M. Williamson. 1998. The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–1319.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590.PubMedPubMedCentralGoogle Scholar
  23. Park, Y.H., M.A.L. West, and D.A. St Clair. 2004. Evaluation of AFLPs for germplasm fingerprinting and assessment of genetic diversity in cultivars of tomato (Lycopersicon esculentum L.). Genome 47:510–518.PubMedCrossRefGoogle Scholar
  24. Pnueli, L., L. CarmelGoren, D. Hareven, T. Gutfinger, J. Alvarez, M. Ganal, D. Zamir, and E. Lifschitz. 1998. The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development 125:1979–1989.PubMedGoogle Scholar
  25. R Development Core Team. 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
  26. Rodriguez, G.R., H.J. Kim, and E. van der Knaap. 2013. Mapping of two suppressors of OVATE (sov) loci in tomato. Heredity 111:256–264.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Rohlf, F.J. 2008. NTSYSpc: Numerical taxonomy system, ver. 2.20. Exeter Publishing Ltd., Setauket, NY, USA.Google Scholar
  28. Ronen, G., L. Carmel-Goren, D. Zamir, and J. Hirschberg. 2000. An alternative pathway to beta-carotene formation in plant chromoplasts discovered by map-based cloning of Beta and old-gold color mutations in tomato. Proc. Natl. Acad. Sci. USA 97:11102–11107.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Ruggieri, V., G. Francese, A. Sacco, A. D'Alessandro, M.M. Rigano, M. Parisi, M. Milone, T. Cardi, G. Mennella, and A. Barone. 2014. An association mapping approach to identify favourable alleles for tomato fruit quality breeding. BMC Plant Biol. 14.Google Scholar
  30. Sauvage, C., V. Segura, G. Bauchet, R. Stevens, P.T. Do, Z. Nikoloski, A.R. Fernie, and M. Causse. 2014. Genome-wide association in tomato reveals 44 candidate loci for fruit metabolic traits. Plant Physiol. 165:1120–1132.PubMedPubMedCentralCrossRefGoogle Scholar
  31. Sherman, J.D. and S.M. Stack. 1992. Two-dimensional spreads of synaptonemal complexes from solanaceous plants. 5. Tomato (Lycopersicon esculentum) karyotype and idiogram. Genome 35:354–359.CrossRefGoogle Scholar
  32. Sim, S., G. Durstewitz, J. Plieske, R. Wieseke, M. Ganal, A. Van Deynze, J. Hamilton, C.R. Buell, M. Causse, S. Wijeratne, and D. Francis. 2012a. Development of a large SNP genotyping array and generation of high-density genetic maps in tomato. PLoS ONE 7:e40563.PubMedPubMedCentralCrossRefGoogle Scholar
  33. Sim, S., A. Van Deynze, K. Stoffel, D. Douches, D. Zarka, M. Ganal, R. Chetelat, S.F. Hutton, J.W. Scott, R.G. Gardner, D. Panthee, M. Mutschler, J.R. Myers, and D.M. Francis. 2012b. High-density SNP genotyping of tomato (Solanum lycopersicum L.) reveals patterns of genetic variation due to breeding. PLoS ONE 7:e45520.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Sim, S.C., M.D. Robbins, C. Chilcott, T. Zhu, and D.M. Francis. 2009. Oligonucleotide array discovery of polymorphisms in cultivated tomato (Solanum lycopersicum L.) reveals patterns of SNP variation associated with breeding. BMC Genomics 10:10.CrossRefGoogle Scholar
  35. Sim, S.C., M.D. Robbins, A. Van Deynze, A.P. Michel, and D.M. Francis. 2011. Population structure and genetic differentiation associated with breeding history and selection in tomato (Solanum lycopersicum L.). Heredity 106:927–935.PubMedPubMedCentralCrossRefGoogle Scholar
  36. Stack, S.M., S.M. Royer, L.A. Shearer, S.B. Chang, J.J. Giovannoni, D.H. Westfall, R.A. White, and L.K. Anderson. 2009. Role of fluorescence in situ hybridization in sequencing the tomato Genome. Cytogenet. Genome Res. 124:339–350.PubMedCrossRefGoogle Scholar
  37. Stacklies, W., H. Redestig, M. Scholz, D. Walther, and J. Selbig. 2007. pcaMethods -a bioconductor package providing PCA methods for incomplete data. Bioinformatics 23:1164–1167.PubMedCrossRefGoogle Scholar
  38. Tanksley, S.D., M.W. Ganal, J.P. Prince, M.C. Devicente, M.W. Bonierbale, P. Broun, T.M. Fulton, J.J. Giovannoni, S. Grandillo, G.B. Martin, R. Messeguer, J.C. Miller, L. Miller, A.H. Paterson, O. Pineda, M.S. Roder, R.A. Wing, W. Wu, and N.D. Young. 1992. High-density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160.PubMedPubMedCentralGoogle Scholar
  39. The Tomato Genome Consortium. 2012. The tomato genome sequence provides insights into fleshy fruit tomato. Nature 485:635–641Google Scholar
  40. The 100 Tomato Genome Sequencing Consortium, D., S. Aflitos, E. Schijlen, H. de Jong, D. de Ridder, S. Smit, R. Finkers, J. Wang, G. Zhang, N. Li, L. Mao, F. Bakker, R. Dirks, T. Breit, B. Gravendeel, H. Huits, D. Struss, R. Swanson-Wagner, H. van Leeuwen, R.C. van Ham, L. Fito, L. Guignier, M. Sevilla, P. Ellul, E. Ganko, A. Kapur, E. Reclus, B. de Geus, H. van de Geest, B. Te Lintel Hekkert, J. van Haarst, L. Smits, A. Koops, G. Sanchez-Perez, A.W. van Heusden, R. Visser, Z. Quan, J. Min, L. Liao, X. Wang, G. Wang, Z. Yue, X. Yang, N. Xu, E. Schranz, E. Smets, R. Vos, J. Rauwerda, R. Ursem, C. Schuit, M. Kerns, J. van den Berg, W. Vriezen, A. Janssen, E. Datema, T. Jahrman, F. Moquet, J. Bonnet, and S. Peters. 2014. Exploring genetic variation in the tomato (Solanum section Lycopersicon) clade by whole-genome sequencing. Plant J. 80:136–148.CrossRefGoogle Scholar
  41. Troyanskaya, O., M. Cantor, G. Sherlock, P. Brown, T. Hastie, R. Tibshirani, D. Botstein, and R.B. Altman. 2001. Missing value estimation methods for DNA microarrays. Bioinformatics 17:520–525.PubMedCrossRefGoogle Scholar
  42. Van Deynze, A., K. Stoffel, C.R. Buell, A. Kozik, J. Liu, E. van der Knaap, and D. Francis. 2007. Diversity in conserved genes in tomato. BMC Genomics 8:465.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Weir, B.S. and C.C. Cockerham. 1984. Estimating F-statistics for the analysis of populatoin structure. Evolution 38:1358–1370.CrossRefGoogle Scholar
  44. Williams, C.E. and D.A. St. Clair. 1993. Phenetic relationships and levels of variability detected by restriction fragment length polymorphism and random amplified polymorphic DNA analysis of cultivated and wild accessions of Lycopersicon esculentum. Genome 36:619–630.PubMedCrossRefGoogle Scholar
  45. Xiao, H., N. Jiang, E. Schaffner, E.J. Stockinger, and E. van der Knaap. 2008. A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science 319:1527–1530.PubMedCrossRefGoogle Scholar
  46. Yang, W., X.D. Bai, E. Kabelka, C. Eaton, S. Kamoun, E. van der Knaap, and D. Francis. 2004. Discovery of single nucleotide polymorphisms in Lycopersicon esculentum by computer aided analysis of expressed sequence tags. Mol. Breed. 14:21–34.CrossRefGoogle Scholar

Copyright information

© Korean Society for Horticultural Science and Springer-Verlag GmbH 2015

Authors and Affiliations

  • Sung-Chur Sim
    • 1
  • Myungkwon Kim
    • 2
  • Sang-Min Chung
    • 3
  • Younghoon Park
    • 4
    • 5
  1. 1.Department of Bioresources EngineeringSejong UniversitySeoulKorea
  2. 2.Tomato Life Science & ResearchChungbukKorea
  3. 3.Department of Life ScienceDongguk University-SeoulSeoulKorea
  4. 4.Department of Horticultural BiosciencePusan National UniversityMiryangKorea
  5. 5.Life and Industry Convergence Research InstitutePusan National UniversityMiryangKorea

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