Theoretical and Applied Genetics

, Volume 131, Issue 5, pp 1017–1030 | Cite as

Identification of a molecular marker tightly linked to bacterial wilt resistance in tomato by genome-wide SNP analysis

  • Boyoung Kim
  • In Sun Hwang
  • Hyung Jin Lee
  • Je Min Lee
  • Eunyoung Seo
  • Doil Choi
  • Chang-Sik Oh
Original Article
  • 365 Downloads

Abstract

Key message

Genotyping of disease resistance to bacterial wilt in tomato by a genome-wide SNP analysis

Abstract

Bacterial wilt caused by Ralstonia pseudosolanacearum is one of the destructive diseases in tomato. The previous studies have identified Bwr-6 (chromosome 6) and Bwr-12 (chromosome 12) loci as the major quantitative trait loci (QTLs) contributing to resistance against bacterial wilt in tomato cultivar ‘Hawaii7996’. However, the genetic identities of two QTLs have not been uncovered yet. In this study, using whole-genome resequencing, we analyzed genome-wide single-nucleotide polymorphisms (SNPs) that can distinguish a resistant group, including seven tomato varieties resistant to bacterial wilt, from a susceptible group, including two susceptible to the same disease. In total, 5259 non-synonymous SNPs were found between the two groups. Among them, only 265 SNPs were located in the coding DNA sequences, and the majority of these SNPs were located on chromosomes 6 and 12. The genes that both carry SNP(s) and are near Bwr-6 and Bwr-12 were selected. In particular, four genes in chromosome 12 encode putative leucine-rich repeat (LRR) receptor-like proteins. SNPs within these four genes were used to develop SNP markers, and each SNP marker was validated by a high-resolution melting method. Consequently, one SNP marker, including a functional SNP in a gene, Solyc12g009690.1, could efficiently distinguish tomato varieties resistant to bacterial wilt from susceptible varieties. These results indicate that Solyc12g009690.1, the gene encoding a putative LRR receptor-like protein, might be tightly linked to Bwr-12, and the SNP marker developed in this study will be useful for selection of tomato cultivars resistant to bacterial wilt.

Notes

Acknowledgements

We are grateful to Dr. Young Hoon Park and RDA-Gene Bank for providing tomato seeds. This work was supported by the Golden Seed Project (Center for Horticultural Seed Development No. 213003-04-4-SBG20 and No. 213007-05-1-SBF20), Ministry of Agriculture, Food and Rural Affairs (MAFRA), Ministry of Oceans and Fisheries (MOF), Rural Development Administration (RDA), and Korea Forest Service (KFS) and also by the National Research Foundation of Korea (NRF) Grant funded by the Korean government (MSIP) (No. 2016R1A2B4011566).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

122_2018_3054_MOESM1_ESM.pdf (368 kb)
Supplementary material 1 (PDF 368 kb)

References

  1. Bentley DR (2006) Whole-genome re-sequencing. Curr Opin Genet Dev 16:545–552.  https://doi.org/10.1016/j.gde.2006.10.009 CrossRefPubMedGoogle Scholar
  2. Caldwell D, Kim B-S, Iyer-Pascuzzi AS (2017) Ralstonia solanacearum differentially colonizes roots of resistant and susceptible tomato plants. Phytopathology 107:528–536.  https://doi.org/10.1094/PHYTO-09-16-0353-R CrossRefPubMedGoogle Scholar
  3. Carmeille A, Caranta C, Dintinger J, Prior P, Luisetti J, Besse P (2006a) Identification of QTLs for Ralstonia solanacearum race 3-phylotype II resistance in tomato. Theor Appl Genet 113:110–121.  https://doi.org/10.1007/s00122-006-0277-3 CrossRefPubMedGoogle Scholar
  4. Carmeille A, Prior P, Kodja H, Chiroleu F, Luisetti J, Besse P (2006b) Evaluation of resistance to race 3, biovar 2 of Ralstonia solanacearum in tomato germplasm. J Phytopathol 154:398–402.  https://doi.org/10.1111/j.1439-0434.2006.01112.x CrossRefGoogle Scholar
  5. Collard B, Jahufer M, Brouwer J, Pang E (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: the basic concepts. Euphytica 142:169–196.  https://doi.org/10.1007/s10681-005-1681-5 CrossRefGoogle Scholar
  6. Cox MP, Peterson DA, Biggs PJ (2010) SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinform 11:485.  https://doi.org/10.1186/1471-2105-11-485 CrossRefGoogle Scholar
  7. Danesh D, Aarons S, McGill GE, Young ND (1994) Genetic dissection of oligogenic resistance to bacterial wilt in tomato. Mol Plant Microbe Interact 7:464–471CrossRefPubMedGoogle Scholar
  8. Dannon EA, Wydra K (2004) Interaction between silicon amendment, bacterial wilt development and phenotype of Ralstonia solanacearum in tomato genotypes. Physiol Mol Plant Pathol 64:233–243.  https://doi.org/10.1016/j.pmpp.2004.09.006 CrossRefGoogle Scholar
  9. Denny T (2007) Plant pathogenic Ralstonia species. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer, Dordrecht, pp 573–644Google Scholar
  10. Eshed Y, Zamir D (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141:1147–1162PubMedPubMedCentralGoogle Scholar
  11. Foolad MR, Panthee DR (2012) Marker-assisted selection in tomato breeding. CRC Crit Rev Plant Sci 31:93–123.  https://doi.org/10.1080/07352689.2011.616057 CrossRefGoogle Scholar
  12. Ganal MW, Altmann T, Röder MS (2009) SNP identification in crop plants. Curr Opin Plant Biol 12:211–217.  https://doi.org/10.1016/j.pbi.2008.12.009 CrossRefPubMedGoogle Scholar
  13. Geethanjali S, Chen K-Y, Pastrana DV, Wang J-F (2010) Development and characterization of tomato SSR markers from genomic sequences of anchored BAC clones on chromosome 6. Euphytica 173:85–97.  https://doi.org/10.1007/s10681-010-0125-z CrossRefGoogle Scholar
  14. Geethanjali S, Kadirvel P, de la Peña R, Rao ES, Wang J-F (2011) Development of tomato SSR markers from anchored BAC clones of chromosome 12 and their application for genetic diversity analysis and linkage mapping. Euphytica 178:283–295.  https://doi.org/10.1007/s10681-010-0331-8 CrossRefGoogle Scholar
  15. Hayward A (1991) Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu Rev Phytopathol 29:65–87.  https://doi.org/10.1146/annurev.py.29.090191.000433 CrossRefPubMedGoogle Scholar
  16. Huet G (2014) Breeding for resistances to Ralstonia solanacearum. Front Plant Sci 5:715.  https://doi.org/10.3389/fpls.2014.00715 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Hwang J, Kim H, Chae Y, Choi H, Kim M, Park Y (2012) Evaluation of germplasm and development of SSR markers for marker-assisted backcross in tomato. Korean J Hortic Sci Technol 30:557–567.  https://doi.org/10.7235/hort.2012.12032 CrossRefGoogle Scholar
  18. Jones N, Ougham H, Thomas H, Pašakinskienė I (2009) Markers and mapping revisited: finding your gene. New Phytol 183:935–966.  https://doi.org/10.1111/j.1469-8137.2009.02933.x CrossRefPubMedGoogle Scholar
  19. Kelman A (1954) The relationship of pathogenicity of Pseudomonas solanacearum to colony appearance in a tetrazolium medium. Phytopathology 44:693–695Google Scholar
  20. Kim J-E, Oh S-K, Lee J-H, Lee B-M, Jo S-H (2014) Genome-wide SNP calling using next generation sequencing data in tomato. Mol Cells 37:36–42.  https://doi.org/10.14348/molcells.2014.2241 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Kim B, Hwang IS, Lee H-J, Oh C-S (2017) Combination of newly developed SNP and InDel markers for genotyping the Cf-9 locus conferring disease resistance to leaf mold disease in tomato. Mol Breed 37:59.  https://doi.org/10.1007/s11032-017-0663-3 CrossRefGoogle Scholar
  22. Lee H-J, Jo E-J, Kim N-H, Chae Y, Lee S-W (2011) Disease responses of tomato pure lines against Ralstonia solanacearum strains from Korea and susceptibility at high temperature. Res Plant Dis 17:326–333.  https://doi.org/10.5423/RPD.2011.17.3.326 CrossRefGoogle Scholar
  23. Lehmensiek A, Sutherland MW, McNamara RB (2008) The use of high resolution melting (HRM) to map single nucleotide polymorphism markers linked to a covered smut resistance gene in barley. Theor Appl Genet 117:721–728.  https://doi.org/10.1007/s00122-008-0813-4 CrossRefPubMedGoogle Scholar
  24. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760.  https://doi.org/10.1093/bioinformatics/btp324 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Li H et al (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079.  https://doi.org/10.1093/bioinformatics/btp352 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Liu W-Y, Kang J-H, Jeong H-S, Choi H-J, Yang H-B, Kim K-T, Choi D, Choi GJ, Jahn M, Kang B-C (2014) Combined use of bulked segregant analysis and microarrays reveals SNP markers pinpointing a major QTL for resistance to Phytophthora capsici in pepper. Theor Appl Genet 127:2503–2513.  https://doi.org/10.1007/s00122-014-2394-8 CrossRefPubMedGoogle Scholar
  27. Mammadov J, Aggarwal R, Buyyarapu R, Kumpatla S (2012) SNP markers and their impact on plant breeding. Int J Plant Genom 2012:728398.  https://doi.org/10.1155/2012/728398 Google Scholar
  28. Miao L, Shou S, Cai J, Jiang F, Zhu Z, Li H (2009) Identification of two AFLP markers linked to bacterial wilt resistance in tomato and conversion to SCAR markers. Mol Biol Rep 36:479–486.  https://doi.org/10.1007/s11033-007-9204-1 CrossRefPubMedGoogle Scholar
  29. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326.  https://doi.org/10.1093/nar/8.19.4321 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Parniske M, Hammond-Kosack KE, Golstein C, Thomas CM, Jones DA, Harrison K, Wulff BB, Jones JDG (1997) Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91:821–832.  https://doi.org/10.1016/S0092-8674(00)80470-5 CrossRefPubMedGoogle Scholar
  31. Peeters N, Guidot A, Vailleau F, Valls M (2013) Ralstonia solanacearum, a widespread bacterial plant pathogen in the post-genomic era. Mol Plant Pathol 14:651–662.  https://doi.org/10.1111/mpp.12038 CrossRefPubMedGoogle Scholar
  32. Ribaut J-M, Hoisington D (1998) Marker-assisted selection: new tools and strategies. Trends Plant Sci 3:236–239.  https://doi.org/10.1016/S1360-1385(98)01240-0 CrossRefGoogle Scholar
  33. Safni I, Cleenwerck I, De Vos P, Fegan M, Sly L, Kappler U (2014) Polyphasic taxonomic revision of the Ralstonia solanacearum species complex: proposal to emend the descriptions of Ralstonia solanacearum and Ralstonia syzygii and reclassify current R. syzygii strains as Ralstonia syzygii subsp. syzygii subsp. nov., R. solanacearum phylotype IV strains as Ralstonia syzygii subsp. indonesiensis subsp. nov., banana blood disease bacterium strains as Ralstonia syzygii subsp. celebesensis subsp. nov. and R. solanacearum phylotype I and III strains as Ralstonia pseudosolanacearum sp. nov. Int J Syst Evol Microbiol 64:3087–3103.  https://doi.org/10.1099/ijs.0.066712-0 CrossRefPubMedGoogle Scholar
  34. Salgon S, Jourda C, Sauvage C, Daunay M-C, Reynaud B, Wicker E, Dintinger J (2017) Eggplant resistance to the Ralstonia solanacearum species complex involves both broad-spectrum and strain-specific quantitative trait loci. Trends Plant Sci 8:828.  https://doi.org/10.3389/fpls.2017.00828 Google Scholar
  35. Silva J, Scheffler B, Sanabria Y, De Guzman C, Galam D, Farmer A, Woodward J, May G, Oard J (2012) Identification of candidate genes in rice for resistance to sheath blight disease by whole genome sequencing. Theor Appl Genet 124:63–74.  https://doi.org/10.1007/s00122-011-1687-4 CrossRefPubMedGoogle Scholar
  36. Stratton M (2008) Genome resequencing and genetic variation. Nat Biotechnol 26:65–66.  https://doi.org/10.1038/nbt0108-65 CrossRefPubMedGoogle Scholar
  37. Subbaiyan GK, Waters DL, 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.  https://doi.org/10.1111/j.1467-7652.2011.00676.x CrossRefPubMedGoogle Scholar
  38. Thomson MJ (2014) High-throughput SNP genotyping to accelerate crop improvement. Plant Breed Biotechnol 2:195–212.  https://doi.org/10.9787/PBB.2014.2.3.195 CrossRefGoogle Scholar
  39. Thoquet P, Olivier J, Sperisen C, Rogowsky P, Laterrot H, Grimsley N (1996a) Quantitative trait loci determining resistance to bacterial wilt in tomato cultivar Hawaii7996. Mol Plant Microbe Interact 9:826–836.  https://doi.org/10.1094/MPMI-9-0826 CrossRefGoogle Scholar
  40. Thoquet P et al (1996b) Polygenic resistance of tomato plants to bacterial wilt in the French West Indies. Mol Plant Microbe Interact 9:837–842.  https://doi.org/10.1094/MPMI-9-0837 CrossRefGoogle Scholar
  41. Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635.  https://doi.org/10.1038/nature11119 CrossRefGoogle Scholar
  42. Truong HTH, Graham E, Esch E, Wang J-F, Hanson P (2010) Distribution of DArT markers in a genetic linkage map of tomato. Korean J Hortic Sci Technol 28:664–671Google Scholar
  43. Vasse J, Frey P, Trigalet A (1995) Microscopic studies of intercellular infection and protoxylem invasion of tomato roots by Pseudomonas solanacearum. Mol Plant Microbe Interact 8:241–251.  https://doi.org/10.1094/MPMI-8-0241 CrossRefGoogle Scholar
  44. Wang J-F, Hanson P, Barnes J (1998) Worldwide evaluation of an international set of resistance sources to bacterial wilt in tomato. In: Prior P, Allen C, Elphinstone J (eds) Bacterial wilt disease. Springer, Berlin, pp 269–275CrossRefGoogle Scholar
  45. Wang J-F, Olivier J, Thoquet P, Mangin B, Sauviac L, Grimsley NH (2000) Resistance of tomato line Hawaii7996 to Ralstonia solanacearum Pss4 in Taiwan is controlled mainly by a major strain-specific locus. Mol Plant Microbe Interact 13:6–13.  https://doi.org/10.1094/MPMI.2000.13.1.6 CrossRefPubMedGoogle Scholar
  46. Wang J-F, Ho F-I, Truong HTH, Huang S-M, Balatero CH, Dittapongpitch V, Hidayati N (2013) Identification of major QTLs associated with stable resistance of tomato cultivar ‘Hawaii 7996’ to Ralstonia solanacearum. Euphytica 190:241–252.  https://doi.org/10.1007/s10681-012-0830-x CrossRefGoogle Scholar
  47. Wicker E, Grassart L, Coranson-Beaudu R, Mian D, Guilbaud C, Fegan M, Prior P (2007) Ralstonia solanacearum strains from Martinique (French West Indies) exhibiting a new pathogenic potential. Appl Environ Microbiol 73:6790–6801.  https://doi.org/10.1128/AEM.00841-07 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Wulff BB, Heese A, Tomlinson-Buhot L, Jones DA, de la Peña M, Jones JDG (2009) The major specificity-determining amino acids of the tomato Cf-9 disease resistance protein are at hypervariable solvent-exposed positions in the central leucine-rich repeats. Mol Plant Microbe Interact 22:1203–1213.  https://doi.org/10.1094/MPMI-22-10-1203 CrossRefPubMedGoogle Scholar
  49. Yang X, Deng F, Ramonell KM (2012) Receptor-like kinases and receptor-like proteins: keys to pathogen recognition and defense signaling in plant innate immunity. Front Biol 7:155–166.  https://doi.org/10.1007/s11515-011-1185-8 CrossRefGoogle Scholar
  50. Zalapa JE et al (2012) Using next-generation sequencing approaches to isolate simple sequence repeat (SSR) loci in the plant sciences. Am J Bot 99:193–208.  https://doi.org/10.3732/ajb.1100394 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Boyoung Kim
    • 1
  • In Sun Hwang
    • 1
  • Hyung Jin Lee
    • 1
  • Je Min Lee
    • 2
  • Eunyoung Seo
    • 3
  • Doil Choi
    • 3
  • Chang-Sik Oh
    • 1
  1. 1.Department of Horticultural Biotechnology, College of Life ScienceKyung Hee UniversityYonginSouth Korea
  2. 2.Department of Horticultural ScienceKyungpook National UniversityDaeguSouth Korea
  3. 3.Department of Plant ScienceSeoul National UniversitySeoulSouth Korea

Personalised recommendations