Skip to main content
SpringerLink
Log in

Identification of QTLs for Ralstonia solanacearum race 3-phylotype II resistance in tomato

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Resistance against a Ralstonia solanacearum race 3-phylotype II strain JT516 was assessed in a F2:3 and a population of inbred lines (RIL), both derived from a cross between L. esculentum cv. Hawaii 7996 (partially resistant) and L. pimpinellifolium WVa700 (susceptible). Resistance criteria used were the percentage of wilted plants to calculate the AUDPC value, and bacterial colonization scores in roots and stem (hypocotyl and epicotyl) assessed in two independent greenhouse experiments conducted during the cool and hot seasons in Réunion Island, France. Symptoms were more severe during the cool season trials. Heritability estimates in individual seasons ranged from 0.82 to 0.88, depending on resistance criterion. A set of 76 molecular markers was used for quantitative trait loci (QTL) mapping using the single- and composite- interval mapping methods, as well as ANOVA. Four QTLs, named Bwr- followed by a number indicating their map location, were identified. They explained from 3.2 to 29.8% of the phenotypic variation, depending on the resistance criterion and the season. A major QTL, Bwr-6, and a minor one, Bwr-3, were detected in each season for all resistance criteria. Both QTLs showed stronger effects in the hot season than in the cool one. Their role in resistance to R. solanacearum race 3-phylotype II was subsequently confirmed in the RIL population derived from the same cross. Two other QTLs, Bwr-4 and Bwr-8, with intermediate and minor effects, respectively, were only detected in the hot season, demonstrating that environmental factors may strongly influence the expression of resistance against the race 3-phylotype II strain JT516. These QTLs were compared with those detected in the RIL population against race 1-phylotype I strain JT519 as well as those detected in other previous studies in the same genetic background against other race 1-phylotype I and II strains. This comparison revealed the possible occurrence of some phylotype-specific resistance QTLs in Hawaii 7996.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Acosta JC, Gilbert JC, Quinon VL (1964) Heritability of bacterial wilt resistance in tomato. P Am Soc Hortic Sci 84:455–462

    Google Scholar 

  • Anaïs G (1986) Utilisation de la résistance variétale dans la lutte contre le flétrissement bactérien de la tomate dû au Pseudomonas solanacearum. In: Smith EF (ed)INRA Bulletin Technique d’Information. Ministère de l’Agriculture, Paris, pp 409–411, 449–453

  • Anand N, Sadashiva AT, Tikoo SK, Ramkishun M, Reddy K (1993) Resistance to bacterial wilt in tomato: gene dosage effects. In: Hartman GL and Hayward AC (eds) Bacterial wilt. ACIAR Proceedings 45. Kaoshiung, Taiwan, pp 142–148

  • Basten CJ, Weir BS, Zeng ZB (2000) QTL cartographer. A reference manual and tutorial for QTL mapping. Department of Statistics, North Carolina State University, Raleigh, North Carolina

  • Buddenhagen IW (1986) Bacterial wilt revisited. In: Persley GJ (ed) Bacterial wilt in Asia and the South Pacific. ACIAR Proceedings, ACIAR, Camberra, pp 126–139

  • Buddenhagen IW, Kelman A (1964) Biological and physiological aspects of bacterial wilt caused by Pseudomonas solanacearum. Annu Rev Phytopathol 2:203–230

    Article  Google Scholar 

  • Buddenhagen I, Sequeira L, Kelman A (1962) Designation of races in Pseudomonas solanacearum. Phytopathology 52:726

    Google Scholar 

  • Carmeille A, Prior P, Kodja H, Chiroleu F, Luisetti J, Besse P (2006) Evaluation of resistance to race 3 biovar 2 of Ralstonia solanacearum in tomato germplasm. J Phytopathology 154:1–5

    Article  Google Scholar 

  • Cook D, Sequeira L (1991) Genetic and biochemical characterization of a Pseudomonas solanacearum gene cluster required for extracellular polysaccharide production and virulence. J Bacteriol 173:1654–1662

    PubMed  CAS  Google Scholar 

  • Cook D, Sequeira L (1994) Strain differentiation of Pseudomonas solanacearum by molecular genetics methods. In: Hayward AC and Hartman GL (eds) Bacterial wilt: the disease and its causative agent, Pseudomonas solanacearum. CAB International, Wallingford, UK, pp 77–93

    Google Scholar 

  • Cook D, Barlow E, Sequeira L (1989) Genetic diversity of Pseudomonas solanacearum: detection of restriction fragment length polymorphism with DNA that specify virulence and the hypersensitive response. Mol Plant Microbe Interact 2:113–121

    Google Scholar 

  • Cook D, Barlow E, Sequeira L (1991) DNA probes as tools for the study of host-pathogen evolution: the example of Pseudomonas solanacearum. In: Hennecke H, Verma DPS (eds) Advances in molecular genetics of plant microbe interactions. Kluwer, Dordrecht, pp 103–108

    Google Scholar 

  • Danesh D, Aarons S, McGill GE, Young ND (1994) Genetic dissection of oligogenic resistance to bacterial wilt in tomato. Mol Plant Microbe Interact 7:464–471

    PubMed  CAS  Google Scholar 

  • Fegan M, Prior P (2005) How complex is the " Ralstonia solanacearum species complex"? In: Allen C, Prior P and Hayward AC (eds) Bacterial wilt: The disease and Ralstonia solanacearum species complex. APS Press, St Paul, pp 449–461

    Google Scholar 

  • Fegan M, Taghavi L, Sly LI, Hayward AC (1998) Phylogeny, diversity and molecular diagnostics of Ralstonia solanacearum. In: Prior P, Allen C, Elphinstone J (eds) Bacterial wilt disease: molecular and ecological aspects. Springer, Berlin Heidelberg New York, pp 19–33

    Google Scholar 

  • French ER (1986) Interaction between strains of Pseudomonas solanacearum, its hosts and the environment. In: Persley GJ (ed) Bacterial wilt in Asia and South Pacific, ACIAR proceedings, ACIAR, Camberra, pp 99–104

  • Granada GA, Sequeira L (1983) Survival of Pseudomonas solanacearum in soil, rhizosphere and plant roots. Can J Microbiol 29:433–440

    Article  Google Scholar 

  • Grimault V, Prior P (1993) Bacterial wilt resistance in tomato associated with tolerance of vascular tissues to Pseudomonas solanacearum. Plant Pathol 42:589–594

    Article  Google Scholar 

  • Grimault V, Anaïs G, Prior P (1994) Distribution of Pseudomonas solanacearum in the stem tissues of tomato plants with different levels of resistance to bacterial wilt. Plant Pathol 43:663–668

    Article  Google Scholar 

  • Haldane J (1919) The combination of linkage values, and the calculation of distance between loci of linked factors. J Genet 8:299–309

    Article  Google Scholar 

  • Hayward AC (1964) Characteristics of Pseudomonas solanacearum. J Appl Bacteriol 27:265–277

    Google Scholar 

  • Hayward AC (1991) Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu Rev Phytopathol 29:65–87

    Article  PubMed  CAS  Google Scholar 

  • Hayward AC (1994) The hosts of Pseudomonas solanacearum. In: Hayward AC, Hartman GL (eds) Bacterial wilt: the disease and its causative agent, Pseudomonas solanacearum. CAB International, Wallingford, UK, pp 9–25

    Google Scholar 

  • He LY, Sequeira L, Kelman A (1983) Characteristics of strains of Pseudomonas solanacearum from China. Plant Dis 67:1357–1361

    Article  Google Scholar 

  • Janse JD (1996) Potato brown rot in Western Europe—history, present occurence and some remarks on possible origin, epidemiology and control strategies. EPPO Bull 26:679–695

    Article  Google Scholar 

  • Kelman A, Sequeira L (1965) Root-to-root spread of Pseudomonas solanacearum. Phytopathology 55:304–309

    Google Scholar 

  • Kim SH, Olson TN, Schaad NW, Moorman GW (2003) Ralstonia solanacearum race 3, biovar 2, the causal agent of brown rot of potato, identified in geraniums in Pennsylvania, Delaware, and Connecticut. Plant Dis 87:450

    Article  Google Scholar 

  • Knapp S, Stroup W, Ross W (1985) Exact confidence intervals for heritabiility on a progeny mean basis. Crop Sci 9:257–262

    Google Scholar 

  • Lander ES, Botstein D (1989) Mapping mendelian factors underlying quantitative trait using RFLP linkage maps. Genetics 121:185–199

    PubMed  CAS  Google Scholar 

  • Lander ES, Geen P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) Mapmaker: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  PubMed  CAS  Google Scholar 

  • Lefebvre V, Palloix A, Caranta C, Pochard E (1995) Construction of an interspecific integrated linkage map of pepper using molecular markers and doubled haploid progenies. Genome 38:112–121

    PubMed  CAS  Google Scholar 

  • Monma S, Sakata Y (1993) Inheritance of resistance to bacterial wilt in tomato. In: Hartman GL, Hayward AC (eds) Bacterial wilt. ACIAR proceedings, Kaoshiung, Taiwan, pp 149–153

    Google Scholar 

  • Nicole J-F (1995) Influence de facteurs biotiques ou abiotiques sur la dynamique des populations de Pseudomonas solanacearum au cours de l’infection et sur le développement de la maladie. PhD Thesis, University of Nantes, France, pp 93

  • Poussier S, Vandewalle P, Luisetti J (1999) Genetic diversity of african and world wide strains of Ralstonia solanacearum as determined by PCR-Restriction fragment length polymorphism analysis of the hrp gene region. Appl Environ Microbiol 65:2184–2194

    PubMed  CAS  Google Scholar 

  • Poussier S, Prior P, Luisetti J, Hayward AC, Fegan M (2000a) Partial sequencing of the hrpB and endoglucanase genes confirms and expands the known diversity within the Ralstonia solanacearum species complex. Syst Appl Microbiol 23:479–486

    CAS  Google Scholar 

  • Poussier S, Trigalet-Demery D, Vandewalle P, Goffinet B, Luisetti J, Trigalet A (2000b) Genetic diversity of Ralstonia solanacearum as assessed by PCR-RFLP of the hrp gene region, AFLP and 16S rRNA sequence analysis, and identification of an African subdivision. Microbiol 146:1679–1692

    CAS  Google Scholar 

  • Prior P, Allen C, Elphinstone J (1998) Bacterial wilt disease: molecular and ecological aspects. Springer, Berlin Heidelberg New York, pp 447

    Google Scholar 

  • Schmit J (1978) Microscopic study of early stages of infection by Pseudomonas solanacearum E.F.S. on "in vitro" grown tomato seedlings. In: Proceedings of the IVth international conference on plant pathogenic bacteria. INRA, Angers, pp 841–856

  • Shapiro SS, Wilk MB (1965) An analysis of variance for normality (complete samples). Biometrika 52:591–611

    Google Scholar 

  • Stuber CW, Edwards MD, Wendel JF (1987) Molecular marker facilitated investigations of quantitative trait loci in maize. II. Factors influencing yield and its component traits. Crop Sci 27:639–648

    Article  Google Scholar 

  • Thoquet P, Olivier J, Sperisen C, Rogowsky P, Laterrot H, Grimsley N (1996a) Quantitative trait loci determining resistance to bacterial wilt in tomato cultivar Hawaii 7996. Mol Plant Microbe Interact 9:826–836

    CAS  Google Scholar 

  • Thoquet P, Olivier J, Sperisen C, Rogowsky P, Prior P, Anaïs G, Mangin B, Bazin B, Nazer R, Grimsley N (1996b) Polygenic resistance of tomato plants to bacterial wilt in the French West Indies. Mol Plant Microbe Interact 9:837–842

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Williamson L, Nakaho K, Hudelson B, Allen C (2002) Ralstonia solanacearum Race 3, Biovar 2 strains isolated from geranium are pathogenic on potato. Plant Dis 86:987–991

    Article  CAS  Google Scholar 

  • Zeng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank F. Chiroleu and J. Veslot (CIRAD Réunion) for help in statistical analyses, J.-J. Chéron (CIRAD Réunion) for technical assistance in the greenhouse trials, SCEA Bassin Plat for maintaining plant cuttings, and H. Kodja (Université Réunion) for his interest in this work. We also thank N. Grimsley (INRA Toulouse) and J-F. Wang (AVRDC Taiwan) for providing seeds of the mapping populations and the genotypic molecular data. This work was partially supported by funds from the Conseil Général of Réunion Island.

Author information

Authors and Affiliations

  1. UMR 53 Université de La Réunion–CIRAD “Peuplements végétaux et bioagresseurs en milieu tropical”, Université de La Réunion, 15 avenue René Cassin, BP 7151, 97715, Saint-Denis Messag Cedex 9, La Réunion, France

    A. Carmeille & P. Besse

  2. Unité Génétique et Amélioration des Fruits et Légumes, INRA, Domaine St Maurice, BP 94, 84143, Montfavet Cedex, France

    C. Caranta

  3. UMR 53 Université de La Réunion–CIRAD “Peuplements végétaux et bioagresseurs en milieu tropical”, CIRAD, 7 chemin de l’IRAT, 97410, Saint-Pierre, La Réunion, France

    J. Dintinger, P. Prior & J. Luisetti

  4. Unité de Pathologie Végétale, INRA, Domaine St Maurice, BP 94, 84143, Montfavet Cedex, France

    P. Prior

Authors
  1. A. Carmeille
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. Caranta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Dintinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. Prior
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. Luisetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. P. Besse
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. Besse.

Additional information

Communicated by I. Paran

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carmeille, A., Caranta, C., Dintinger, J. et al. Identification of QTLs for Ralstonia solanacearum race 3-phylotype II resistance in tomato. Theor Appl Genet 113, 110–121 (2006). https://doi.org/10.1007/s00122-006-0277-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-006-0277-3

Keywords

Search

Navigation