Theoretical and Applied Genetics

, Volume 121, Issue 7, pp 1275–1287 | Cite as

Identification of QTL associated with resistance to bacterial spot race T4 in tomato

  • Samuel F. Hutton
  • Jay W. Scott
  • Wencai Yang
  • Sung-Chur Sim
  • David M. Francis
  • Jeffrey B. Jones
Original Paper

Abstract

Bacterial spot of tomato (Solanum lycopersicum L.), caused by several Xanthomonas sp., is a serious but difficult disease to control by chemical means. Development of resistance has been hindered by emergence of races virulent to tomato, by the quantitative inheritance of resistance, and by a low correlation between seedling assays and resistance in the field. Resistance to multiple races, including race T4, has been described in the S. lycopersicum var. cerasiformae accession PI 114490. We used molecular markers to identify associations with quantitative trait loci (QTL) in an elite inbred backcross (IBC) population derived from OH 9242, PI 114490 and Fla. 7600, a breeding line with tomato accession Hawaii 7998 (H7998) in its pedigree. Race T4 resistance has also been described in the advanced breeding lines Fla. 8233, Fla. 8517, and Fla. 8326, and a selective genotyping approach was used to identify introgressions associated with resistance in segregating progeny derived from crosses with these lines. In the IBC population, loci on chromosomes 11 and 3, respectively, explained as much as 29.4 and 4.8% of resistance variation. Both these loci were also confirmed by selective genotyping: PI 114490 and H7998 alleles on chromosome 11 each provided resistance. The PI 114490 allele on chromosome 3 was confirmed in the Fla. 8517 population, and an allele of undetermined descent was confirmed at this locus in the Fla. 8326 population. A chromosome 12 allele was associated with susceptibility in the Fla. 8517 population. Additional loci contributing minor effects were also implicated in the IBC population or by selective genotyping. Selection for the major QTL in a marker-directed phenotyping approach should significantly improve the efficiency of breeding for resistance to bacterial spot race T4, although as yet undetected QTL would be necessary to carry out strict marker assisted selection.

Supplementary material

122_2010_1387_MOESM1_ESM.pdf (237 kb)
Supplementary material 1 (PDF 236 kb)
122_2010_1387_MOESM2_ESM.pdf (224 kb)
Supplementary material 2 (PDF 224 kb)

References

  1. Astua-Monge G, Minsavage GV, Stall RE, Davis MJ, Bonas U, Jones JB (2000) Resistance of tomato and pepper to T3 strains of Xanthomonas campestris pv. vesicatoria is specified by a plant-inducible avirulence gene. Mol Plant Microbe Interact 13:911–921CrossRefPubMedGoogle Scholar
  2. Bouzar H, Jones JB, Minsavage GV, Stall RE, Scott JW (1994a) Proteins unique to phenotypically distinct groups of Xanthomonas campestris pv. vesicatoria revealed by silver staining. Phytopathology 84:39–44CrossRefGoogle Scholar
  3. Bouzar H, Jones JB, Stall RE, Hodge NC, Minsavage GV, Benedict AA, Alvarez AM (1994b) Physiological, chemical, serological, and pathogenic analyses of a world-wide collection of Xanthomonas campestris pv. vesicatoria strains. Phytopathology 84:663–671CrossRefGoogle Scholar
  4. Bouzar H, Jones JB, Stall RE, Louws FJ, Schneider M, Rademaker JLW, de Bruijn FJ, Jackson LE (1999) Multiphasic analysis of xanthomonads causing bacterial spot disease on tomato and pepper in the Caribbean and Central America: evidence for common lineages within and between countries. Phytopathology 89:328–335CrossRefPubMedGoogle Scholar
  5. Canteros B (1990) Diversity of plasmids and plasmid-encoded phenotypic traits in Xanthomonas campestris pv. vesicatoria. Dissertation, University of FloridaGoogle Scholar
  6. Conover RA, Gerhold NR (1981) Mixtures of copper and maneb or mancozeb for control of bacterial spot of tomato and their compatibility for control of fungus diseases. Proc Fla State Hort Soc 94:154–156Google Scholar
  7. Francis DM, Berry S, Aldrich T, Scaife K, Bash W (2002) ‘Ohio OX 150’ processing tomato. Rpt Tomato Genet Coop 52:36–37Google Scholar
  8. Fulton TM, Chunwongse J, Tanksley SD (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Biol Rptr 13:207–209CrossRefGoogle Scholar
  9. George V, Tiwari HK, Zhu X, Elston RC (1999) A test of transmission/disequilibrium for quantitative traits in pedigree data, by multiple regression. Am J Hum Genet 65:236–245CrossRefPubMedGoogle Scholar
  10. Horsfall JG, Barratt RW (1945) An improved grading system for measuring plant diseases. Phytopathology 35:655Google Scholar
  11. Hutton SF (2008) Inheritance and mapping of resistance to bacterial spot race T4 (Xanthomonas perforans) in tomato, and its relationship to race T3 hypersensitivity, and inheritance of race T3 hypersensitivity from PI 126932. Dissertation, University of FloridaGoogle Scholar
  12. Hutton SF, Scott JW, Jones JB (2010) Inheritance of resistance to bacterial spot race T4 from three tomato breeding lines with differing resistance backgrounds. J Am Soc Hortic Sci 135:150–158Google Scholar
  13. Jones JB, Jones JP (1985) The effect of bactericides, tank mixing time and spray schedule on bacterial leaf spot of tomato. Proc Fla State Hortic Soc 98:244–247Google Scholar
  14. Jones JB, Scott JW (1986) Hypersensitive response in tomato to Xanthomonas campestris pv. vesicatoria. Plant Dis 70:337–339CrossRefGoogle Scholar
  15. Jones JB, Minsavage GV, Stall RE, Kelly RO, Bouzar H (1993) Genetic analysis of a DNA region involved in expression of two epitopes associated with lipopolysaccharide in Xanthomonas campestris pv. vesicatoria. Phytopathology 83:551–556CrossRefGoogle Scholar
  16. Jones JB, Stall RE, Scott JW, Somodi GC, Bouzar H, Hodge NC (1995) A third tomato race of Xanthomonas campestris pv. vesicatoria. Plant Dis 79:395–398CrossRefGoogle Scholar
  17. Jones JB, Bouzar H, Somodi GC, Stall RE, Pernezny K, El-Morsy G, Scott JW (1998a) Evidence for the preemptive nature of tomato race 3 of Xanthomonas campestris pv. vesicatoria in Florida. Phytopathology 88:33–38CrossRefPubMedGoogle Scholar
  18. Jones JB, Stall RE, Bouzar H (1998b) Diversity among Xanthomonads pathogenic on pepper and tomato. Annu Rev Phytopathol 36:41–58CrossRefPubMedGoogle Scholar
  19. Jones JB, Bouzar H, Stall RE, Almira EC, Roberts PD, Bowen BW, Sudberry J, Strickler PM, Chun J (2000) Systematic analysis of xanthomonads (Xanthomonas spp.) associated with pepper and tomato lesions. Int J Syst Evol Microbiol 50:1211–1219PubMedGoogle Scholar
  20. Jones JB, Lacy GH, Bouzar H, Minsavage GV, Stall RE, Schaad NW (2005) Bacterial spot-worldwide distribution, importance and review. Acta Hortic 695:27–33Google Scholar
  21. Jones JB, Lacy GH, Bouzar H (2006) Reclassification of the xanthomonads associated with bacterial spot disease of tomato and pepper. Syst Appl Microbiol 29:85–86CrossRefGoogle Scholar
  22. Kabelka E, Franchino B, Francis DM (2002) Two loci from Lycopersicon hirsutumconfer resistance to strains of Clavibacter michiganensis subsp. michiganensis. Phytopathol 92:504–510CrossRefGoogle Scholar
  23. Kavitha P, Umesha S (2008) Regulation of defense related enzymes associated with bacterial spot resistance in tomato. Phytoparasitica 36:144–159CrossRefGoogle Scholar
  24. Lee SH, Walker DR, Cregan PB, Boerma HR (2004) Comparison of four flow cytometric SNP detection assays and their use in plant improvement. Theor Appl Genet 110:167–174CrossRefPubMedGoogle Scholar
  25. Marco GM, Stall RE (1983) Control of bacterial spot of pepper initiated by strains of Xanthomonas campestris pv. vesicatoria that differ in sensitivity to copper. Plant Dis 67:779–891CrossRefGoogle Scholar
  26. Minsavage GV, Balogh B, Stall RE, Jones JB (2003) New tomato races of Xanthomonas campestris pv. vesicatoria associated with mutagenesis of tomato race 3 strains. Phytopathology 93:S62Google Scholar
  27. Netter J, Wasserman W, Kutner MH (1990) Applied linear statistical models. Richard D. Irwin, Homewood, ILGoogle Scholar
  28. Obradovic A, Jones JB, Momol MT, Olson SM, Jackson LE, Balogh B, Guven K, Iriarte FB (2005) Integration of biological control agents and systemic acquired resistance inducers against bacterial spot of tomato. Plant Dis 89:712–716CrossRefGoogle Scholar
  29. Robbins MD, Darriques A, Sim SC, Masud MAT, Francis DM (2009) Characterization of hypersensitive resistance to bacterial spot race T3 (Xanthomonas perforans) from tomato accession PI 128216. Phytopathology 99:1037–1044CrossRefPubMedGoogle Scholar
  30. Sahin F, Miller SA (1996) Characterization of Ohio strains of Xanthomonas campestris pv vesicatoria, causal agent of bacterial spot of pepper. Plant Dis 80:773–778CrossRefGoogle Scholar
  31. Scott JW (2004) Fla. 7946 tomato breeding line resistant to Fusarium oxysporum f.sp. lycopersici races 1, 2, and 3. HortScience 39:440–441Google Scholar
  32. Scott JW, Jones JB (1989) Inheritance of resistance to foliar bacterial spot of tomato incited by Xanthomonas campestris pv. vesicatoria. J Am Soc Hortic Sci 114:111–114Google Scholar
  33. Scott JW, Stall RE, Jones JB, Somodi GC (1996) A single gene controls the hypersensitive response of Hawaii 7981 to race 3 (T3) of the bacterial spot pathogen. Rpt Tomato Genet Coop 46:23Google Scholar
  34. Scott JW, Miller SA, Stall RE, Jones JB, Somodi GC, Barbosa V, Francis DL, Sahin F (1997) Resistance to race T2 of the bacterial spot pathogen in tomato. HortScience 32:724–727Google Scholar
  35. Scott JW, Jones JB, Somodi GC (2001) Inheritance of resistance in tomato to race T3 of the bacterial spot pathogen. J Am Soc Hortic Sci 126:436–441Google Scholar
  36. Scott JW, Francis DM, Miller SA, Somodi GC, Jones JB (2003) Tomato bacterial spot resistance derived from PI 114490; inheritance of resistance to race T2 and relationship across three pathogen races. J Am Soc Hortic Sci 128:698–703Google Scholar
  37. Scott JW, Hutton SF, Jones JB, Francis DM, Miller SA (2006a) Resistance to bacterial spot race T4 and breeding for durable, broad-spectrum resistance to other races. Rpt Tomato Genet Coop 56:33–36Google Scholar
  38. Scott JW, Olson SM, Bryan HH, Bartz JA, Maynard DN, Stofella PJ (2006b) Solar fire hybrid tomato: Fla. 7776 tomato breeding line. HortScience 41:1504–1505Google Scholar
  39. Somodi GC, Jones JB, Scott JW, Wang JF, Stall RE (1996) Relationship between the hypersensitive reaction and field resistance to tomato race 1 of Xanthomonas campestris pv. vesicatoria. Plant Dis 80:1151–1154CrossRefGoogle Scholar
  40. Stall RE, Beaulieu C, Egel D, Hodge NC, Leite RE, Minsavage GV, Bouzar H, Jones JB, Alvarez AM, Benedict AA (1994) Two genetically diverse strains are included in Xanthomonas campestris pv. vesicatoria. Int J Syst Bacteriol 44:47–53CrossRefGoogle Scholar
  41. Suliman-Pollatschek S, Kashkush K, Shats H, Hillel J, Lavi U (2002) Generation and mapping of AFLP, SSRs and SNPs in Solanum lycopersicum. Cell Mole Biol Lett 7:583–597Google Scholar
  42. van Deynze A, Stoffel K, Buell CR, Kozik A, Liu J, van der Knaap E, Francis D (2007) Diversity in conserved genes in tomato. BMC Genomics 8:465CrossRefPubMedGoogle Scholar
  43. Wang JF (1992) Resistance to Xanthomonas campestris pv. vesicatoria in tomato. Dissertation, University of FloridaGoogle Scholar
  44. Wang JF, Jones JB, Scott JW, Stall RE (1990) A new race of the tomato group of strains of Xanthomonas campestris pv. vesicatoria. Phytopathology 80:1070Google Scholar
  45. Wang JF, Jones JB, Scott JW, Stall RE (1994) Several genes in Lycopersicon esculentum control hypersensitivity to Xanthomonas campestris pv. vesicatoria. Phytopathology 84:702–706CrossRefGoogle Scholar
  46. Whalen MC, Wang JF, Carland FM, Heiskell ME, Dahlbeck D, Minsavage GV, Jones JB, Scott JW, Stall RE, Staskawicz BJ (1993) Avirulence gene avrRxv from Xanthomonas campestris pv. vesicatoria specifies resistance on tomato line Hawaii 7998. Mol Plant Microbe Interact 6:616–627PubMedGoogle Scholar
  47. Yang W, Bai X, Kabelka E, Eaton C, Kamoun S, van der Knaap E, Francis D (2004) Discovery of single nucleotide polymorphisms in Solanum lycopersicum by computer aided analysis of expressed sequence tags. Mol Breed 14:21–34CrossRefGoogle Scholar
  48. Yang W, Miller SA, Scott JW, Jones JB, Francis DM (2005a) Mining tomato genome sequence databases for molecular markers: application to bacterial resistance and marker assisted selection. Acta Hortic 695:241–250Google Scholar
  49. Yang WC, Sacks EJ, Ivey ML, Miller SA, Francis DM (2005b) Resistance in Lycopersicon esculentum intraspecific crosses to race T1 strains of Xanthomonas campestris pv. vesicatoria causing bacterial spot of tomato. Phytopathology 95:519–527CrossRefPubMedGoogle Scholar
  50. Yu ZH, Wang JF, Stall RE, Vallejos CE (1995) Genomic localization of genes that control a hypersensitive reaction to Xanthomonas campestris pv. vesicatoria (Doidge)Dye. Genetics 141:675–682PubMedGoogle Scholar
  51. Zhu X, Elston RE (2001) Transmission/disequilibrium test for quantitative traits. Genet Epidemiol 20:57–74CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Samuel F. Hutton
    • 1
  • Jay W. Scott
    • 1
  • Wencai Yang
    • 2
  • Sung-Chur Sim
    • 3
  • David M. Francis
    • 3
  • Jeffrey B. Jones
    • 4
  1. 1.Gulf Coast Research and Education Center, Institute of Food and Agricultural SciencesUniversity of FloridaWimaumaUSA
  2. 2.Department of Vegetable Science, College of Agronomy and BiotechnologyChina Agricultural UniversityBeijingPeople’s Republic of China
  3. 3.Department of Horticulture and Crop ScienceThe Ohio State University, Ohio Agricultural Research and Development CenterWoosterUSA
  4. 4.Plant Pathology DepartmentUniversity of FloridaGainesvilleUSA

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