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Physical delimitation of the pepper Bs3 resistance gene specifying recognition of the AvrBs3 protein from Xanthomonas campestris pv. vesicatoria

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Abstract

The pepper (Capsicum annuum) Bs3 gene confers resistance to avrBs3-expressing strains of the bacterial spot pathogen Xanthomonas campestris pv. vesicatoria. To physically delimit Bs3, a pepper YAC library was screened with two flanking DNA markers that are separated from Bs3 by 1.0 and 1.2 cM, respectively resulting in the identification of three YAC clones. Genetic mapping of the corresponding YACends revealed however, that these YACs do not cover Bs3 and subsequent screens with newly developed YACend markers failed to identify new YAC clones. Marker saturation at the Bs3 locus was carried out by amplified fragment length polymorphism (AFLP). The analysis of 1,024 primer combinations resulted in the identification of 47 new Bs3-linked AFLPs. High-resolution linkage mapping of Bs3 was accomplished by inspecting more than 4,000 F2 segregants resulting in a genetic resolution of 0.01 cM. Using tightly Bs3-linked YACend- and AFLP-derived markers we established a Bs3-spanning BAC contig and physically delimited the target gene within one BAC clone. The analysis of the Bs3-containing genomic region revealed substantial local variation in the correlation of genetic and physical distances.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Ballvora A, Pierre M, Van den Ackerveken G, Schornack S, Rossier O, Ganal M, Lahaye T, Bonas U (2001) Genetic mapping and functional analysis of the tomato Bs4 locus, governing recognition of the Xanthomonas campestris pv. vesicatoria AvrBs4 protein. Mol Plant–Microbe Interact 14:629–638

    Article  PubMed  CAS  Google Scholar 

  • Bonas U, Stall RE, Staskawicz B (1989) Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Mol Gen Genet 218:127–136

    Article  PubMed  CAS  Google Scholar 

  • Bronson SK, Pei J, Taillon-Miller P, Chorney MJ, Geraghty DE, Chaplin DD (1991) Isolation and characterization of yeast artificial chromosome clones linking the HLA-B and HLA-C loci. Proc Natl Acad Sci USA 88:1676–1680

    Article  PubMed  CAS  Google Scholar 

  • Büttner D, Bonas U (2002) Port of entry—the type III secretion translocon. Trends Microbiol 10:186–192

    Article  PubMed  Google Scholar 

  • Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    Article  PubMed  CAS  Google Scholar 

  • Civardi L, Xia Y, Edwards KJ, Schnable PS, Nikolau BJ (1994) The relationship between genetic and physical distances in the cloned a1-sh2 interval of the Zea mays L. genome. Proc Natl Acad Sci USA 91:8268–8272

    Article  PubMed  CAS  Google Scholar 

  • Cook AA, Guevara YG (1984) Hypersensitivity in Capsicum chacoense to race 1 of the bacterial spot pathogen of pepper. Plant Dis 68:329–330

    Article  Google Scholar 

  • Cook AA, Stall RE (1982) Distribution of races of Xanthomonas vesicatoria pathogenic on pepper. Plant Dis 66:388–389

    Article  Google Scholar 

  • Da Cunha L, McFall AJ, Mackey D (2006) Innate immunity in plants: a continuum of layered defenses. Microbes Infect 8:1372–1381

    Article  PubMed  CAS  Google Scholar 

  • Edwards K, Johnstone C, Thompson C (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucl Acids Res 19:1349

    Article  PubMed  CAS  Google Scholar 

  • Gassmann W, Dahlbeck D, Chesnokova O, Minsavage GV, Jones JB, Staskawicz BJ (2000) Molecular evolution of virulence in natural field strains of Xanthomonas campestris pv. vesicatoria. J Bacteriol 182:7053–7059

    Article  PubMed  CAS  Google Scholar 

  • Giovannoni JJ, Wing RA, Ganal MW, Tanksley SD (1991) Isolation of molecular markers from specific chromosomal intervals using DNA pools from existing mapping populations. Nucl Acids Res 19:6553–6558

    Article  PubMed  CAS  Google Scholar 

  • Gu K, Yang B, Tian D, Wu L, Wang D, Sreekala C, Yang F, Chu Z, Wang GL, White FF, Yin Z (2005) R gene expression induced by a type-III effector triggers disease resistance in rice. Nature 435:1122–1125

    Article  PubMed  CAS  Google Scholar 

  • Gürlebeck D, Thieme F, Bonas U (2006) Type III effector proteins from the plant pathogen Xanthomonas and their role in the interaction with the host plant. J Plant Physiol 163:233–255

    Article  PubMed  CAS  Google Scholar 

  • Iyer AS, McCouch SR (2004) The rice bacterial blight resistance gene xa5 encodes a novel form of disease resistance. Mol Plant–Microbe Interact 17:1348–1354

    Article  PubMed  CAS  Google Scholar 

  • Kearney B, Staskawicz BJ (1990) Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene, avrBs2. Nature 346:385–386

    Article  PubMed  CAS  Google Scholar 

  • Kim BS, Hartmann RW (1985) Inheritance of a gene (Bs 3 ) conferring hypersensitive resistance to Xanthomonas campestris pv. vesicatoria in pepper (Capsicum annuum). Plant Dis 69:233–235

    Google Scholar 

  • Konieczny A, Ausubel FM (1993) A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J 4:403–410

    Article  PubMed  CAS  Google Scholar 

  • Lahaye T, Hartman S, Töpsch S, Freialdenhoven A, Yano M, Schulze-Lefert (1998) High-resolution genetic and physical mapping of the Rar1 locus in barley. Theor Appl Genet 97:526–534

    Article  CAS  Google Scholar 

  • Lam E (2004) Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol 5:305–315

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832

    Article  PubMed  CAS  Google Scholar 

  • Minsavage GV, Dahlbeck D, Whalen MC, Kearny B, Bonas U, Staskawicz BJ, Stall RE (1990) Gene-for-gene relationships specifying disease resistance in Xanthomonas campestris pv. vesicatoria–pepper interactions. Mol Plant–Microbe Interact 3:41–47

    CAS  Google Scholar 

  • Petes TD (2001) Meiotic recombination hot spots and cold spots. Nat Rev Genet 2:360–369

    Article  PubMed  CAS  Google Scholar 

  • Pierre M, Noël L, Lahaye T, Ballvora A, Veuskens J, Ganal M, Bonas U (2000) High-resolution genetic mapping of the pepper resistance locus Bs3 governing recognition of the Xanthomonas campestris pv. vesicatoria AvrBs3 protein. Theor Appl Genet 101:255–263

    Article  CAS  Google Scholar 

  • Ponciano G, Ishihara H, Tsuyumu S, Leach JE (2003) Bacterial effectors in plant disease and defense: Keys to durable resistance? Plant Dis 87:1272–1282

    Article  CAS  Google Scholar 

  • Ruffel S, Dussault MH, Palloix A, Moury B, Bendahmane A, Robaglia C, Caranta C (2002) A natural recessive resistance gene against potato virus Y in pepper corresponds to the eukaryotic initiation factor 4E (eIF4E). Plant J 32:1067–1075

    Article  PubMed  CAS  Google Scholar 

  • Schornack S, Ballvora A, Gürlebeck D, Peart J, Baulcombe D, Baker B, Ganal M, Bonas U, Lahaye T (2004) The tomato resistance protein Bs4 is a predicted non-nuclear TIR-NB-LRR protein that mediates defense responses to severely truncated derivatives of AvrBs4 and overexpressed AvrBs3. Plant J 37:46–60

    Article  PubMed  CAS  Google Scholar 

  • Schornack S, Peter K, Bonas U, Lahaye T (2005) Expression levels of avrBs3-like genes affect recognition specificity in tomato Bs4 but not in pepper Bs3 mediated perception. Mol Plant–Microbe Interact 18:1215–1225

    Article  PubMed  CAS  Google Scholar 

  • Schornack S, Meyer A, Römer P, Jordan T, Lahaye T (2006) Gene-for-gene mediated recognition of nuclear-targeted AvrBs3-like bacterial effector proteins. J Plant Physiol 163:256–272

    Article  PubMed  CAS  Google Scholar 

  • Stall RE (1995) Xanthomonas campestris pv. vesicatoria In: Singh US, Singh RP, Kohmoto K (eds) Pathogenesis and host specificity in plant diseases. Histopathological, biochemical, genetic and molecular bases. Elsevier, New York, p 167–181

    Google Scholar 

  • Szurek B, Rossier O, Hause G, Bonas U (2002) Type III-dependent translocation of the Xanthomonas AvrBs3 protein into the plant cell. Mol Microbiol 46:13–23

    Article  PubMed  CAS  Google Scholar 

  • Tai T, Staskawicz BJ (1999) Construction of a yeast artificial chromosome library of pepper (Capsicum annuum L.) and identification of clones from the Bs2 resistance locus. Theor Appl Genet 100:112–117

    Article  Google Scholar 

  • Van den Ackerveken G, Marois E, Bonas U (1996) Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell 87:1307–1316

    Article  PubMed  Google Scholar 

  • Van der Hoorn R, De Wit P, Joosten M (2002) Balancing selection favors guarding resistance proteins. Trends Plant Sci 7:67–71

    Article  PubMed  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, Van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucl Acids Res 23:4407–4414

    Article  PubMed  CAS  Google Scholar 

  • White FF, Yang B, Johnson LB (2000) Prospects for understanding avirulence gene function. Curr Opin Plant Biol 3:291–298

    Article  PubMed  CAS  Google Scholar 

  • Yoo EY, Kim S, Kim JY, Kim BD (2001) Construction and characterization of a bacterial artificial chromosome library from chili pepper. Mol Cell 12:117–120

    CAS  Google Scholar 

  • Yoo EY, Kim S, Kim YH, Lee CJ, Kim BD (2003) Construction of a deep coverage BAC library from Capsicum annuum, ‘CM334’. Theor Appl Genet 107:540-543

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Laura Rose for helpful comments on earlier versions of the manuscript. We acknowledge constructive comments of two anonymous reviewers. We thank Brian Staskawicz for providing pepper YAC clones. We would like to acknowledge contributions and technical support by C. Kretschmer, B. Rosinsky and M. Schulze. This work was supported by an EMBO short-term fellowship to T. J. and by grants of the Deutsche Forschungsgemeinschaft to T. L. (SFB 363 and LA 1338/2-2).

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Author notes

  1. Tina Jordan

    Present address: Institute of Plant Biology, University of Zürich, 8008, Zürich, Switzerland

  2. Michele Pierre

    Present address: Institut des Sciences du Végétal, CNRS, Avenue de la Terrasse Bât. 23, 91198, Gif-sur-Yvette Cédex, France

  3. Pietro Piffanelli

    Present address: Parco Tecnologico Padano, 26900, Lodi, Italy

Authors and Affiliations

  1. Institute of Genetics, Martin-Luther-Universität Halle-Wittenberg, 06099, Halle (Saale), Germany

    Tina Jordan, Patrick Römer, Annett Meyer, Robert Szczesny, Ulla Bonas & Thomas Lahaye

  2. Centre National de la Recherche Scientifique, Institut des Sciences Végétales, Avenue de la Terrasse, 91190, Gif-sur-Yvette Cédex, France

    Michele Pierre & Ulla Bonas

  3. Centre de Coopération Internationale en Recherche Agronomique pour le Developpement (CIRAD), UMR 1096, 34398, Montpellier Cédex 5, France

    Pietro Piffanelli

  4. INRA-URGV, 91057, Evry Cédex, France

    Abdel Bendahmane

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  1. Tina Jordan
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Correspondence to Thomas Lahaye.

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Communicated by I. Paran

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Jordan, T., Römer, P., Meyer, A. et al. Physical delimitation of the pepper Bs3 resistance gene specifying recognition of the AvrBs3 protein from Xanthomonas campestris pv. vesicatoria . Theor Appl Genet 113, 895–905 (2006). https://doi.org/10.1007/s00122-006-0349-4

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