Association Analysis against Bacterial Wilt Resistance in Tomato Cultivars by Association Mapping Method
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Published:
May 31, 2021
Keywords:
SSR marker COS marker TASSEL program quantitative trait bacterial wilt
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Abstract
Association mapping based on linkage disequilibrium in diverse population could significantly improve the resolution and accuracy of marker–trait associations compared with linkage analysis. Therefore, this study aimed to identify quantitative trait loci (QTL) for bacterial wilt resistance through positional candidate loci and functional candidate genes using association mapping method. A total of 92 tomato cultivars consisting of 51 international resistance, 2 Thai commercial resistance cultivars and 39 susceptible lines were used for analysis with general linear model using TASSEL program. The association between markers and bacterial wilt resistance was determined by probability at P < 0.05. The results revealed that most of significant associated markers were correlated to previously QTL reports i.e., TG48 (Chromosome 2), TG118, CP18 (Chromosome 6) and T0989 (Chromosome 12). Furthermore, moderate significant level of new QTL on chromosome 1 was identified for SSR134, SSR572, SSR117 and SSR65 markers. For the association analysis by functional candidate gene, four disease resistance genes, LRR, ascorbate peroxidase, jasmonate and ethylene, were related to bacterial wilt resistance. Therefore, this study confirmed that association mapping is a method that could be used to detect QTL as same as the linkage analysis in bi–parental population.
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Research article
References
Acosta, J.C. 1963. Genetic Analysis of Bacterial Wilt Resistance and Certain Other Characters in a Tomato Cross, Lycopersicon esculentum Mill. × L. pimpinellifolium Mill. PhD Thesis, University of Hawaii, Hawaii.
Acosta, J.C., J.C Gilbert and V.L. Quinon. 1964. Heritability of bacterial wilt resistance in tomato. Proc. Am. Soc. Hortic. Sci. 84: 455–462.
Almagro, L., L.V. Gomez Ros, S. Belchi–Navarro, R. Bru, A. Ros Barcelo and M.A. Pedreno. 2009. Class III peroxidases in plant defence reactions. J. Exp. Bot. 60(2): 377–390.
Anand, N., A.T. Sadashiva, S.K. Tikoo, Ramkishun and K.M. Reddy. 1993. Resistance to bacterial wilt in tomato: gene dosage effects, pp. 142–148. In G.L. Hartman and A.C. Hayward, eds. Bacterial Wilt. ACIAR Proc. No. 45. Brisbane, Australia.
Andolfo, G., W. Sanseverino, S. Rombauts, J. Van der Peer, J.M. Bradeen, D. Carputo, L. Frusciante and M.R. Ercolano. 2013. Overview of tomato (Solanum lycopersicum) candidate pathogen recognition genes reveals important Solanum R locus dynamics. New Phytol. 197: 223–237.
Baichoo, Z. and Y. Jaufeerally–Fakim. 2017. Ralstonia solanacearum upregulates marker genes of the salicylic acid and ethylene signaling pathways but not those of the jasmonic acid pathway in leaflets of Solanum lines during early stage of infection. Eur. J. Plant Pathol. 147: 615–625.
Bradbury, P.J., Z. Zhang, D.E. Kroon, T.M. Casstevens, Y. Ramdoss and E.S. Buckler. 2007. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19): 2633–2635.
Buckler IV, E.S. and J.M. Thornsberry. 2002. Plant molecular diversity and applications to genomics. Curr. Opin. Plant Biol. 5: 107–111.
Butsarakul, S., S. Pisil, P. Siritorn and K. Lertrat. 1997. Resolution of bacterial wilt resistant–tomato varieties in the international set of resistance in tomato to bacterial wilt under the northeast condition. Report of Khon Kaen University, Khon Kaen. (in Thai)
Carmeille, A., C. Caranta, J. Dintinger, P. Prior, J. Luisetti and P. Besse. 2006. Identification of QTLs for Ralstonia solanacearum race 3–phylotype II resistance in tomato. Theor. Appl. Genet. 113(1): 110–121.
Danesh, D., S. Aarons, G.E. Mcgill and N.D. Young. 1994. Genetic dissection of oligogenic resistance to bacterial wilt in tomato. Mol. Plant Microbe. Interact. 7(4): 464–471.
Dara–Carlos, L. 1998. Mapping of Bacterial Wilt Resistance Genes Tomato (Lycopersicon esculentum Mill.) using AFLP Markers. MS Thesis, University of the Philippines Los Banos, Los Banos.
Flint–Garcia, S.A., J.M. Thornsberry and E.S. Buckler IV. 2003. Structure of linkage disequilibrium in plants. Annu. Rev. Plant Biol. 53: 357–374.
Fulton, T.M., J. Chunwongse and S.D. Tanksley. 1995. Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol. Biol. Rep. 13(3): 207–209.
Fulton, T.M., R. Van der Hoeven, N.T. Eannetta and S.D. Tanksley. 2002. Identification, analysis, and utilization of conserved ortholog set markers for comparative genomics in higher plants. Plant Cell 14: 1457–1467.
Garris, A.J., S.R. McCouch and S. Kresovich. 2003. Population structure and its effects on haplotype diversity and linkage disequilibrium surrounding the xa5 locus of rice (Oryza sativa L.). Genetics 165: 759–769.
Gebhardt, C., A. Ballvora, B. Walkemeier, P. Oberhagemann and K. Schuler. 2004. Assessing genetic potential in germplasm collections of crop plants by marker–trait association: a case study for potatoes with quantitative variation of resistance to late blight and maturity type. Mol. Breed. 13: 93–102.
Hai, T.T.H., E. Esch and J.F. Wang. 2008. Resistance to Taiwanese race 1 strains of Ralstonia solanacearum in wild tomato germplasm. Eur. J. Plant Pathol. 122: 471–479.
Hanson, P.M., J.F. Wang, O. Licardo, Hanudin, S.Y. Mah, G.L. Harthman, Y.C. Lin and J.T. Chen. 1996. Variable reaction of tomato lines to bacterial wilt evaluated at several locations in southeast Asia. Hort. Sci. 31: 143–146.
Hanson, P.M., O. Licardo, Hanudin, J.F. Wang and J.T. Chen. 1998. Diallel analysis of bacterial wilt resistance in tomato derived from different sources. Plant Dis. 82: 74–78.
Hayward, A.C. 1991. Biological and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu. Rev. Phytopathol. 29: 65–87.
Ivandic, V.C., A. Hackett, E. Nevo, R. Keith, W.T.B. Thomas and B.P. Foster. 2002. Analysis of simple sequence repeat (SSRs) in wild barley from the Fertile Crescent: associations with ecology, geography and flowering time. Plant Mol. Biol. 48: 511–527.
Kelman, A. 1953. The Bacterial Wilt Caused by Pseudomonas solanacearum. North Carolina Agricultural Experiment Station, USA. 194 pp.
Kruger, S.A., J.A. Able, K.J. Chalmers and P. Langridge. 2004. Linkage disequilibrium analysis of hexaploid wheat. In Proc. the Plant and Animal Genomes XII Conference, 10–14 January 2004. p. 321.
Marker to sequence. Available Source: https://www.eusol.wur.nl/marker2seq/, May 22, 2013.
Mazzucato, A., R. Papa, E. Bitocchi, P. Mosconi, L. Nanni, V. Negri, M.E. Picarella, F. Siligato, G.P. Soressi, B. Tiranti and F. Veronesi. 2008. Genetic diversity, structure and marker–trait associations in a collection of Italian tomato (Solanum lycopersicum L.) landraces. Theor. Appl. Genet. 116: 657–669.
Morel, J.B. and J.L. Dangl. 1997. The hypersensitive response and the induction of cell death in plants. Cell Death Differ. 4: 671–683.
Noctor, G. and C.H. Foyer. 1998. Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 249–279.
Nordborg, M., J.O. Borevitz, J. Bergelson, C.C. Berry, J. Chory, J. Hagenblad, M. Kreitman, J.N. Maloof, T. Noyes, P. Oefner, E.A. Stahl and D. Weigel. 2002. The extent of linkage disequilibrium in Arabidopsis thaliana. Nat. Genet. 30: 190–193.
Palaisa, K., M. Morgante, M. Williams and A. Rafalski. 2003. Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci. Plant Cell 15: 1795–1806.
Palaisa, K., M. Morgante, S. Tingey and A. Rafalski. 2004. Long–range patterns of diversity and linkage disequilibrium surrounding the maize Y1 gene are indicative of an asymmetric selective sweep. Proc. Natl. Acad. Sci. 101(26): 9885–9890.
Ranc, N., S. Muños, J. Xu, M.C. Le Paslier, A. Chauveau, R. Bounon, S. Rolland, J.P. Bouchet, D. Brunel and M. Causse. 2012. Genome–wide association mapping in tomato (Solanum lycopersicum) is possible using genome admixture of Solanum lycopersicum var. cerasiforme. G3 (Bethesda) 2: 853–864.
Remington, D.L., J.M. Thornsberry, Y. Matsuoka, L.M. Wilson, S.R. Whitt, J. Doebley, S. Kresovich, M.M. Goodman and E.S. Buckler IV. 2001. Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc. Natl. Acad. Sci. 98: 11479–11484.
Ruggieri, V., G. Francese, A. Sacco, A. D’Alessandro, M.M. Rigano, M. Parisi, M. Milone, G. Mennella and A. Barone. 2014. An association mapping approach to identify favorable alleles for tomato fruit quality breeding. BMC Plant Biol. 14: 337.
Smirnoff, N. 2000. Ascorbic acid: metabolism and functions of a multi–facetted molecule. Curr. Opin. Plant Biol. 3: 229–235.
Sol Genomics Network. Available Source: https://solgenomics.net/, May 12, 2013.
Srisawad, N. 2012. Identifying of Bacterial Wilt Resistance Haplotype in Tomato using Association Analysis. PhD Thesis, Kasetsart University, Bangkok. (in Thai)
Srisawad, N., C. Leksomboon and J. Chunwongse. 2012. Evaluation of bacterial wilt resistance level in international resistant tomato lines using some isolates of Ralstonia solanacearum from growing areas in Thailand. Agricultural Sci. J. 43(2–3): 325–337. (in Thai)
Thaveechai, N., W. Kositratana and C. Leksomboon. 1992. Bacterial wilt of tomato in Thailand. The AVNET Phase–I Final Workshop and AVNET Phase–II Joint Planning Meeting. Lembang, Indonesia. p. 24.
Thoquet, P., J. Oliver, C. Sperisen, P. Rogowsky, H. Laterrot and N. Grimsley. 1996a. Quantitative trait loci determining resistance to bacterial wilt in tomato cultivar H7996. Mol. Plant Microbe. Interact. 9(9): 826–836.
Thoquet, P., J. Oliver, C. Sperisen, P. Rogowsky, P. Prior, G. Anais, B. Mangin, B. Bazin, R. Nazer and N. Grimsley. 1996b. Polygenic resistance of tomato plants to bacterial wilt in the French West Indies. Mol. Plant Microbe. Interact. 9(9): 837–842.
Thornsberry, J.M., M.M. Goodman, J. Doebley, S. Kresovich, D. Nielsen and E.S. Buckler IV. 2001. Dwarf8 polymorphisms associate with variation in flowering time. Nat. Genet. 28: 286–289.
Vudhivanich, S. and S. Soontarasing. 1996. Screening for bacterial wilt resistance of tomato by scalpel leaf–clip method, pp. 183–192. In Proc. the 34th Kasetsart University Annual Conference, 30 January – 1 February 1996. (in Thai)
Wang, J.F., J. Olivier, P. Thoquet, B. Mangin, L. Sauviac and N.H. Grimsley. 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. 7: 464–471.
Wang, J.F., P. Hanson and J.A. Barnes. 1998. Worldwide evaluation of an international set of resistance sources to bacterial wilt in tomato, pp 269–275. In P. Prior, C. Allen and J. Elphinstone, eds. Bacterial Wilt Disease. Springer, Berlin, Heidelberg.
Winstead, N.N. and A. Kelman. 1952. Inoculation techniques for evaluating resistance to Pseudomonas solanacearum. Phytopathology 42: 628–634.
Wu, F.N., L.A. Mueller, D. Crouzillat, V. Petiard and S.D. Tanksley. 2006. Combining bioinformatics and phylogenetics to identify large sets of single–copy orthologous genes (COSII) for comparative, evolutionary and systematic studies: a test case in the euasterid plant clade. Genetics 174(3): 1407–1420.
Xu, J., N. Ranc, S. Muños, S. Rolland, J. Bouchet, N. Desplat, M.C. Le Paslier, Y. Liang, D. Brunel and M. Causse. 2013. Phenotypic diversity and association mapping for fruit quality traits in cultivated tomato and related species. Theor. Appl. Genet. 126: 567–581.
You, F.M., N. Huo, Y.Q Gu, M.C. Luo, Y. Ma, D. Hane, G.R. Lazo, J. Dvorak and O.D. Anderson. 2008. BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinformatics 9: 253.
Zhang, J., J. Zhao, Y. Liang and Z. Zou. 2015a. Genome–wide association–mapping for fruit quality traits in tomato. Euphytica 207: 439–451.
Zhang, J., J. Zhao, Y. Xu, J. Liang, P. Chang, F. Yan, M. Li, Y. Liang and Z. Zou. 2015b. Genome–wide association mapping for tomato volatiles positively contributing to tomato flavor. Front. Plant Sci. 6: 1042.
Zhang, Z., E. Ersoz, C.Q. Lai, R.J. Todhunter, H.K. Tiwari, M.A. Gore, P.J. Bradbury, J. Yu, D.K. Arnett, J.M. Ordovas and E.S. Buckler. 2010. Mixed linear model approach adapted for genome–wide association studies. Nat. Genet. 42: 355–360.
Acosta, J.C., J.C Gilbert and V.L. Quinon. 1964. Heritability of bacterial wilt resistance in tomato. Proc. Am. Soc. Hortic. Sci. 84: 455–462.
Almagro, L., L.V. Gomez Ros, S. Belchi–Navarro, R. Bru, A. Ros Barcelo and M.A. Pedreno. 2009. Class III peroxidases in plant defence reactions. J. Exp. Bot. 60(2): 377–390.
Anand, N., A.T. Sadashiva, S.K. Tikoo, Ramkishun and K.M. Reddy. 1993. Resistance to bacterial wilt in tomato: gene dosage effects, pp. 142–148. In G.L. Hartman and A.C. Hayward, eds. Bacterial Wilt. ACIAR Proc. No. 45. Brisbane, Australia.
Andolfo, G., W. Sanseverino, S. Rombauts, J. Van der Peer, J.M. Bradeen, D. Carputo, L. Frusciante and M.R. Ercolano. 2013. Overview of tomato (Solanum lycopersicum) candidate pathogen recognition genes reveals important Solanum R locus dynamics. New Phytol. 197: 223–237.
Baichoo, Z. and Y. Jaufeerally–Fakim. 2017. Ralstonia solanacearum upregulates marker genes of the salicylic acid and ethylene signaling pathways but not those of the jasmonic acid pathway in leaflets of Solanum lines during early stage of infection. Eur. J. Plant Pathol. 147: 615–625.
Bradbury, P.J., Z. Zhang, D.E. Kroon, T.M. Casstevens, Y. Ramdoss and E.S. Buckler. 2007. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19): 2633–2635.
Buckler IV, E.S. and J.M. Thornsberry. 2002. Plant molecular diversity and applications to genomics. Curr. Opin. Plant Biol. 5: 107–111.
Butsarakul, S., S. Pisil, P. Siritorn and K. Lertrat. 1997. Resolution of bacterial wilt resistant–tomato varieties in the international set of resistance in tomato to bacterial wilt under the northeast condition. Report of Khon Kaen University, Khon Kaen. (in Thai)
Carmeille, A., C. Caranta, J. Dintinger, P. Prior, J. Luisetti and P. Besse. 2006. Identification of QTLs for Ralstonia solanacearum race 3–phylotype II resistance in tomato. Theor. Appl. Genet. 113(1): 110–121.
Danesh, D., S. Aarons, G.E. Mcgill and N.D. Young. 1994. Genetic dissection of oligogenic resistance to bacterial wilt in tomato. Mol. Plant Microbe. Interact. 7(4): 464–471.
Dara–Carlos, L. 1998. Mapping of Bacterial Wilt Resistance Genes Tomato (Lycopersicon esculentum Mill.) using AFLP Markers. MS Thesis, University of the Philippines Los Banos, Los Banos.
Flint–Garcia, S.A., J.M. Thornsberry and E.S. Buckler IV. 2003. Structure of linkage disequilibrium in plants. Annu. Rev. Plant Biol. 53: 357–374.
Fulton, T.M., J. Chunwongse and S.D. Tanksley. 1995. Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol. Biol. Rep. 13(3): 207–209.
Fulton, T.M., R. Van der Hoeven, N.T. Eannetta and S.D. Tanksley. 2002. Identification, analysis, and utilization of conserved ortholog set markers for comparative genomics in higher plants. Plant Cell 14: 1457–1467.
Garris, A.J., S.R. McCouch and S. Kresovich. 2003. Population structure and its effects on haplotype diversity and linkage disequilibrium surrounding the xa5 locus of rice (Oryza sativa L.). Genetics 165: 759–769.
Gebhardt, C., A. Ballvora, B. Walkemeier, P. Oberhagemann and K. Schuler. 2004. Assessing genetic potential in germplasm collections of crop plants by marker–trait association: a case study for potatoes with quantitative variation of resistance to late blight and maturity type. Mol. Breed. 13: 93–102.
Hai, T.T.H., E. Esch and J.F. Wang. 2008. Resistance to Taiwanese race 1 strains of Ralstonia solanacearum in wild tomato germplasm. Eur. J. Plant Pathol. 122: 471–479.
Hanson, P.M., J.F. Wang, O. Licardo, Hanudin, S.Y. Mah, G.L. Harthman, Y.C. Lin and J.T. Chen. 1996. Variable reaction of tomato lines to bacterial wilt evaluated at several locations in southeast Asia. Hort. Sci. 31: 143–146.
Hanson, P.M., O. Licardo, Hanudin, J.F. Wang and J.T. Chen. 1998. Diallel analysis of bacterial wilt resistance in tomato derived from different sources. Plant Dis. 82: 74–78.
Hayward, A.C. 1991. Biological and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu. Rev. Phytopathol. 29: 65–87.
Ivandic, V.C., A. Hackett, E. Nevo, R. Keith, W.T.B. Thomas and B.P. Foster. 2002. Analysis of simple sequence repeat (SSRs) in wild barley from the Fertile Crescent: associations with ecology, geography and flowering time. Plant Mol. Biol. 48: 511–527.
Kelman, A. 1953. The Bacterial Wilt Caused by Pseudomonas solanacearum. North Carolina Agricultural Experiment Station, USA. 194 pp.
Kruger, S.A., J.A. Able, K.J. Chalmers and P. Langridge. 2004. Linkage disequilibrium analysis of hexaploid wheat. In Proc. the Plant and Animal Genomes XII Conference, 10–14 January 2004. p. 321.
Marker to sequence. Available Source: https://www.eusol.wur.nl/marker2seq/, May 22, 2013.
Mazzucato, A., R. Papa, E. Bitocchi, P. Mosconi, L. Nanni, V. Negri, M.E. Picarella, F. Siligato, G.P. Soressi, B. Tiranti and F. Veronesi. 2008. Genetic diversity, structure and marker–trait associations in a collection of Italian tomato (Solanum lycopersicum L.) landraces. Theor. Appl. Genet. 116: 657–669.
Morel, J.B. and J.L. Dangl. 1997. The hypersensitive response and the induction of cell death in plants. Cell Death Differ. 4: 671–683.
Noctor, G. and C.H. Foyer. 1998. Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 249–279.
Nordborg, M., J.O. Borevitz, J. Bergelson, C.C. Berry, J. Chory, J. Hagenblad, M. Kreitman, J.N. Maloof, T. Noyes, P. Oefner, E.A. Stahl and D. Weigel. 2002. The extent of linkage disequilibrium in Arabidopsis thaliana. Nat. Genet. 30: 190–193.
Palaisa, K., M. Morgante, M. Williams and A. Rafalski. 2003. Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci. Plant Cell 15: 1795–1806.
Palaisa, K., M. Morgante, S. Tingey and A. Rafalski. 2004. Long–range patterns of diversity and linkage disequilibrium surrounding the maize Y1 gene are indicative of an asymmetric selective sweep. Proc. Natl. Acad. Sci. 101(26): 9885–9890.
Ranc, N., S. Muños, J. Xu, M.C. Le Paslier, A. Chauveau, R. Bounon, S. Rolland, J.P. Bouchet, D. Brunel and M. Causse. 2012. Genome–wide association mapping in tomato (Solanum lycopersicum) is possible using genome admixture of Solanum lycopersicum var. cerasiforme. G3 (Bethesda) 2: 853–864.
Remington, D.L., J.M. Thornsberry, Y. Matsuoka, L.M. Wilson, S.R. Whitt, J. Doebley, S. Kresovich, M.M. Goodman and E.S. Buckler IV. 2001. Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc. Natl. Acad. Sci. 98: 11479–11484.
Ruggieri, V., G. Francese, A. Sacco, A. D’Alessandro, M.M. Rigano, M. Parisi, M. Milone, G. Mennella and A. Barone. 2014. An association mapping approach to identify favorable alleles for tomato fruit quality breeding. BMC Plant Biol. 14: 337.
Smirnoff, N. 2000. Ascorbic acid: metabolism and functions of a multi–facetted molecule. Curr. Opin. Plant Biol. 3: 229–235.
Sol Genomics Network. Available Source: https://solgenomics.net/, May 12, 2013.
Srisawad, N. 2012. Identifying of Bacterial Wilt Resistance Haplotype in Tomato using Association Analysis. PhD Thesis, Kasetsart University, Bangkok. (in Thai)
Srisawad, N., C. Leksomboon and J. Chunwongse. 2012. Evaluation of bacterial wilt resistance level in international resistant tomato lines using some isolates of Ralstonia solanacearum from growing areas in Thailand. Agricultural Sci. J. 43(2–3): 325–337. (in Thai)
Thaveechai, N., W. Kositratana and C. Leksomboon. 1992. Bacterial wilt of tomato in Thailand. The AVNET Phase–I Final Workshop and AVNET Phase–II Joint Planning Meeting. Lembang, Indonesia. p. 24.
Thoquet, P., J. Oliver, C. Sperisen, P. Rogowsky, H. Laterrot and N. Grimsley. 1996a. Quantitative trait loci determining resistance to bacterial wilt in tomato cultivar H7996. Mol. Plant Microbe. Interact. 9(9): 826–836.
Thoquet, P., J. Oliver, C. Sperisen, P. Rogowsky, P. Prior, G. Anais, B. Mangin, B. Bazin, R. Nazer and N. Grimsley. 1996b. Polygenic resistance of tomato plants to bacterial wilt in the French West Indies. Mol. Plant Microbe. Interact. 9(9): 837–842.
Thornsberry, J.M., M.M. Goodman, J. Doebley, S. Kresovich, D. Nielsen and E.S. Buckler IV. 2001. Dwarf8 polymorphisms associate with variation in flowering time. Nat. Genet. 28: 286–289.
Vudhivanich, S. and S. Soontarasing. 1996. Screening for bacterial wilt resistance of tomato by scalpel leaf–clip method, pp. 183–192. In Proc. the 34th Kasetsart University Annual Conference, 30 January – 1 February 1996. (in Thai)
Wang, J.F., J. Olivier, P. Thoquet, B. Mangin, L. Sauviac and N.H. Grimsley. 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. 7: 464–471.
Wang, J.F., P. Hanson and J.A. Barnes. 1998. Worldwide evaluation of an international set of resistance sources to bacterial wilt in tomato, pp 269–275. In P. Prior, C. Allen and J. Elphinstone, eds. Bacterial Wilt Disease. Springer, Berlin, Heidelberg.
Winstead, N.N. and A. Kelman. 1952. Inoculation techniques for evaluating resistance to Pseudomonas solanacearum. Phytopathology 42: 628–634.
Wu, F.N., L.A. Mueller, D. Crouzillat, V. Petiard and S.D. Tanksley. 2006. Combining bioinformatics and phylogenetics to identify large sets of single–copy orthologous genes (COSII) for comparative, evolutionary and systematic studies: a test case in the euasterid plant clade. Genetics 174(3): 1407–1420.
Xu, J., N. Ranc, S. Muños, S. Rolland, J. Bouchet, N. Desplat, M.C. Le Paslier, Y. Liang, D. Brunel and M. Causse. 2013. Phenotypic diversity and association mapping for fruit quality traits in cultivated tomato and related species. Theor. Appl. Genet. 126: 567–581.
You, F.M., N. Huo, Y.Q Gu, M.C. Luo, Y. Ma, D. Hane, G.R. Lazo, J. Dvorak and O.D. Anderson. 2008. BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinformatics 9: 253.
Zhang, J., J. Zhao, Y. Liang and Z. Zou. 2015a. Genome–wide association–mapping for fruit quality traits in tomato. Euphytica 207: 439–451.
Zhang, J., J. Zhao, Y. Xu, J. Liang, P. Chang, F. Yan, M. Li, Y. Liang and Z. Zou. 2015b. Genome–wide association mapping for tomato volatiles positively contributing to tomato flavor. Front. Plant Sci. 6: 1042.
Zhang, Z., E. Ersoz, C.Q. Lai, R.J. Todhunter, H.K. Tiwari, M.A. Gore, P.J. Bradbury, J. Yu, D.K. Arnett, J.M. Ordovas and E.S. Buckler. 2010. Mixed linear model approach adapted for genome–wide association studies. Nat. Genet. 42: 355–360.
