Natural variation in the Pto pathogen resistance gene within species of wild tomato (Lycopersicon). I. Functional analysis of Pto alleles

Genetics

Volumn 171, Issue 1, 2005, Pages 345-357

  Rose, Laura E ^a,b   Langley, Charles H ^a   Bernal, Adriana J ^a   Michelmore, Richard W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Department Biologie II ^*  (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA;

ALLELE; AMINO ACID SUBSTITUTION; ARTICLE; DISEASE RESISTANCE; GENE; GENETIC VARIABILITY; NONHUMAN; PHENOTYPE; PLANT; PLANT PATHOGEN INTERACTION; POPULATION GENETICS; PRIORITY JOURNAL; PSEUDOMONAS SYRINGAE; PST GENE; PTO GENE; SITE DIRECTED MUTAGENESIS; SPECIES DIFFERENTIATION; TOMATO;

ALLELES; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; BLOTTING, SOUTHERN; DNA, PLANT; GENE DELETION; GEOGRAPHY; IMMUNITY, NATURAL; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT DISEASES; PLANT PROTEINS; PROTEIN-SERINE-THREONINE KINASES; PSEUDOGENES; PSEUDOMONAS SYRINGAE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; SOUTH AMERICA; SPECIES SPECIFICITY; VARIATION (GENETICS); VIRULENCE;

AGROBACTERIUM; BACTERIA (MICROORGANISMS); LYCOPERSICON; LYCOPERSICON ESCULENTUM; LYCOPERSICON PIMPINELLIFOLIUM; PSEUDOMONAS SYRINGAE PV. TOMATO;

EID: 26444440571     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.104.039339     Document Type: Article

References (57)

1. BARRETT, J. A., 1988 Frequency-dependent selection in plant-fungal interactions. Philos. Trans. R. Soc. Lond. B 319: 473-484.
2. BERNAL, A., Q. PAN, J. POLLACK, L. ROSE, A. KOZIK et al., 2005 Functional analysis of the plant resistance gene Pto using DNA shuffling. J. Biol. Chem. 280: 23073-23083.
3. BOGDANOVE, A. J., 2002 Pto update: recent progress on an ancient plant defence response signalling pathway. Mol. Plant Pathol. 3: 283-288.
4. CAICEDO, A. L., B. A. SCHAAL and B. N. KUNKEL, 1999 Diversity and molecular evolution of the RPS2 resistance gene in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 96: 302-306.
5. CHANG, J. H., Y.-S. TAI, A. J. BERNAL, D. T. LAVELLE, B. J. STASKAWICZ et al., 2002 Functional analyses of the Pto resistance gene family in tomato and the identification of a minor resistance determinant in a susceptible haplotype. Mol. Plant-Microbe Interact. 15: 281-291.
6. COLLMER, A., M. LINDEBERG, T. PETNICKI-OCWIEJA, D. J. SCHNEIDER and J. R. ALFANO, 2002 Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol. 10: 462-469.
7. DANGL, J. L., and J. D. G. JONES, 2001 Plant pathogens and integrated defence responses to infection. Nature 411: 826-833.
8. DENG, W. L., A. H. REHM, A. O. CHARKOWSKI, C. M. ROJAS and A. COLLMER, 2003 Pseudomonas syringae exchangeable effector loci: sequence diversity in representative pathovars and virulence function in P. syringae pv. syringae B728a. J. Bacteriol. 185: 2592-2602.
9. DOYLE, J. J., and J. L. DOYLE, 1987 A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19: 11-15.
10. FLOR, H. H., 1956 The complementary genetic systems in flax and flax rust. Adv. Genet. 8: 29-54.
11. FLOR, H. H., 1971 The current status of the gene for gene concept. Annu. Rev. Phytopathol. 9: 275-296.
12. FRANK, S. A., 1992 Models of plant-pathogen coevolution. Trends Genet. 8: 213-219.
13. FREDERICK, R. D., R. L. THILMONY, G. SESSA and G. B. MARTIN, 1998 Recognition specificity for the bacterial avirulence protein AvrPto is determined by Thr-204 in the activation loop of the tomato Pto kinase. Mol. Cell 2: 241-245.
14. GRANT, M. R., J. M. MCDOWELL, A. G. SHARPE, Z. M. DETORRES, D. J. LYDIATE et al., 1998 Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis. Proc. Natl. Acad. Sci. USA 95: 15843-15848.
15. GUTTMAN, D. S., B. A. VINATZER, S. F. SARKAR, M. V. RANALL, G. KETTLER et al., 2002 A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295: 1722-1726.
16. HALDANE, J. B. S., 1949 Disease and evolution. Ric. Sci. Suppl. 19: 1-11.
17. HAMMOND-KOSACK, K. E., and J. E. PARKER, 2003 Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr. Opin. Biotechnol. 14: 177-193.
18. HANKS, S. K., and T. HUNTER, 1995 The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 9: 576-596.
19. INNES, R. W., 2004 Guarding the goods. New Insights into the central alarm system of plants. Plant Physiol. 135: 695-701.
20. ISLAM, M. R., and G. M. E. MAYO, 1990 A compendium on host genes in flax conferring resistance to flax rust. Plant Breed. 104: 89-100.
21. ISLAM, M. R., and K. W. SHEPHERD, 1991 Present status of genetics of rust resistance in flax. Euphytica 55: 255-268.
22. JIN, Q., R. THILMONY, J. ZWIESLER-VOLLICK and S.-Y. HE, 2003 Type III protein secretion in Pseudomonas syringae. Microbes Infect. 5: 301-310.
23. KIM, Y. J., N.-C. LIN and G. B. MARTIN, 2002 Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109: 589-598.
24. KISHINO, H., and M. HASEGAWA, 1989 Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data and the branching order in Hominoidea. J. Mol. Evol. 29: 170-179.
25. LEONARD, K. J., 1994 Stability of equilibria in a gene-for-gene coevolution model of host-parasite interactions. Phytopathology 84: 70-77.
26. LOH, Y.-T., and G. B. MARTIN, 1995 The Pto bacterial resistance gene and the Fen insecticide sensitivity gene encode functional protein kinases with serine/threonine specificity. Plant Physiol. 108: 1735-1739.
27. MARTIN, G. B., M. C. DEVICENTE and S. D. TANSLEY, 1993 High-resolution linkage analysis and physical characterization of the Pto bacterial resistance locus in tomato. Mol. Plant Pathol. 6: 26-34.
28. MARTIN, G. B., A. FRARY, T. WU, S. BROMMONSCHENKEL, J. CHUNWONGSE et al., 1994 A member of the tomato Pto gene family confers sensitivity to fenthion resulting in rapid cell death. Plant Cell 6: 1543-1552.
29. MAURICIO, R., E. A. STAHL, T. KORVES, D. TIAN, M. KREITMAN et al., 2003 Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis thaliana. Genetics 163: 735-746.
30. MAY, R. M., and R. M. ANDERSON, 1983 Parasite-host coevolution, pp. 186-206 in Coevolution, edited by D. FUTUYAMA and M. SLATKIN. Sinauer, Sunderland, MA.
31. MEYERS, B. C., K. A. SHEN, P. ROHANI, B. S. GAUT and R. W. MICHELMORE, 1998 Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell 10: 1833-1846.
32. MILLER, J. C., and S. D. TANKSLEY, 1990 RFLP analysis of phylogenetic relationships and genetic variation in the genus Lycopersicon. Theor. Appl. Genet. 80: 437-448.
33. MONFORTE, A. J., and S. D. TANKSLEY, 2000 Development of a set of near isogenic and backcross recombinant inbred lines containing most of the Lycopersicon hirsutum genome in a L. esculentum genetic background: a tool for gene mapping and gene discovery. Genome 43: 803-813.
34. NOEL, L., T. L. MOORES, E. A. VAN DER BIEZEN, M. PARNISKE, M. J. DANIELS et al., 1999 Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell 11: 2099-2111.
35. PILOWSKY, M., and D. ZUTRA, 1982 Screening wild tomatoes for resistance to bacterial speck pathogen (Pseudomonas tomato). Plant Dis. 66: 46-47.
36. PILOWSKY, M., and D. ZUTRA, 1986 Reaction of different tomato genotypes to the bacterial speck pathogen (Pseudomonas syringae pv. tomato). Phytoparasitica 14: 39-42.
37. PRYOR, T., 1987 The origin and structure of fungal disease resistance genes in plants. Trends Genet. 3: 157-161.
38. RATHJEN, J. P., J. H. CHANG, B. J. STASKAWICZ and R. W. MICHELMORE, 1999 Constitutively active Pto induces a Prf-dependent hypersensitive response in the absence of avrPto. EMBO J. 18: 3232-3240.
39. RIELY, B. K., and G. B. MARTIN, 2001 Ancient origin of pathogen recognition specificity conferred by the tomato disease resistance gene Pto. Proc. Natl. Acad. Sci. USA 98: 2059-2064.
40. RONALD, P. C., J. M. SALMERON, F. M. CARLAND and B. J. STASKAWICZ, 1992 The cloned avirulence gene avrPto induces disease resistance in tomato cultivars containing the Pto disease resistance gene. J. Bacteriol. 174: 1604-1611.
41. SCOFIELD, S. R., C. M. TOBIAS, J. P. RATHJEN, J. H. CHANG, D. T. LAVELLE et al., 1996 Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274: 2063-2065.
42. SEGER, J., 1988 Dynamics of some simple host-parasite models with more than two genotypes in each species. Philos. Trans. R. Soc. Lond. B 319: 541-556.
43. SESSA, G., and G. B. MARTIN, 2000 Signal recognition and transduction mediated by the tomato Pto kinase: a paradigm of innate immunity in plants. Microbes Infect. 2: 1591-1597.
44. SESSA, G., M. D'ASCENZO and G. B. MARTIN, 2000 Thr38 and Ser198 are Pto autophosphorylation sites required for the AvrPto-Pto-mediated hypersensitive response. EMBO J. 19: 2257-2269.
45. STAHL, E. A., G. DWYER, R. MAURICIO, M. KREITMAN and J. BERGELSON, 1999 Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400: 667-671.
46. STOCKINGER, E. J., and L. L. WALLING, 1994 Pto3 and Pto4: novel genes from Lycopersicon hirsutum var. glabratum that confer resistance to Pseudomonas syringae pv tomato. Theor. Appl. Genet. 89: 879-884.
47. SWOFFORD, D., 1999 PAUP* Version4.0b10. Sinauer Associates, Sunderland, MA.
48. TANG, X., R. D. FREDERICK, J. ZHOU, D. A. HALTERMAN, Y. JIA et al., 1996 Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274: 2060-2063.
49. TANKSLEY, S. D., M. W. GANAL, J. P. PRINCE, M. C. DEVICENTE, M. W. BONIERBALE et al., 1992 High density molecular linkage maps of the tomato and potato genomes. Genetics 132: 1141-1160.
50. THOMPSON, J. D., T. J. GIBSON, F. PLEWNIAK, F. JEANMOUGIN and D. G. HIGGINS, 1997 The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24: 4876-4882.
51. TIAN, D., H. ARAKI, E. STAHL, J. BERGELSON and M. KREITMAN, 2002 Signature of balancing selection in Arabidopsis. Proc. Natl. Acad. Sci. USA 99: 11525-11530.
52. TIAN, D., M. B. TRAW, J. Q. CHEN, M. KREITMAN and J. BERGELSON, 2003 Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423: 74-77.
53. VAN DER HOORN, R. A. L., M. KRUIJT, R. ROTH, B. F. BRANDWAGT, M. H. A. J. JOOSTEN et al., 2001 Intragenic recombination generated two distinct Cf genes that mediate AVR9 recognition in the natural population of Lycopersicon pimpinellifolium. Proc. Natl. Acad. Sci. USA 98: 10493-10498.
54. VAN OOIJEN, J. M., J. M. SANDBRINK, M. VRIELINK, R. VERKERK, P. ZABEL et al., 1994 An RFLP linkage map of Lycopersicon peruvianum. Theor. Appl. Genet. 89: 1007-1013.
55. WANG, G.-L., D.-L. RUAN, W.-Y. SONG, S. SIDERIS, L. CHEN et al., 1998 Xa21D encodes a receptor-like molecule with a leucine-rich repeat domain that determines race-specific recognition and is subject to adaptive evolution. Plant Cell 10: 765-779.
56. WU, A., V. ANDRIOTIS, M. DURRANT and J. P. RATHJEN, 2004 A patch of surface-exposed residues mediates negative regulation of immune signaling by tomato Pto kinase. Plant Cell 16: 2809-2821.
57. XIANG, C., P. HAN, I. LUTZIGER, K. WANG and D. J. OLIVER, 1999 A mini binary vector series for plant transformation. Plant Mol. Biol. 40: 711-717.