Identification of an ancestral resistance gene cluster involved in the coevolution process between Phaseolus vulgaris and its fungal pathogen Colletotrichum lindemuthianum

Molecular Plant-Microbe Interactions

Volumn 12, Issue 9, 1999, Pages 774-784

  Geffroy, Valérìe ^a,c   Sicard, Delphine ^a,b   De Oliveira, Julio C F ^a   Sévignac, Mireille ^a   Cohen, Séverine ^a   Gepts, Paul ^b   Neema, Claire ^a,d   Langin, Thierry ^a   Dron, Michel ^a,e  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CEMAGREF   (France)

^d AGROPARISTECH   (France)

^e CIRAD   (France)

Author keywords

Common bean; Mapping

Indexed keywords

DISEASE RESISTANCE; GENE CLUSTER; GENE POOL; INBRED LINE; MOLECULAR CLONING; MYCOSIS; PLANT DISEASE; PLANT GENETICS; PLANT PATHOGEN INTERACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM;

COLLETOTRICHUM LINDEMUTHIANUM; EMBRYOPHYTA; PHASEOLUS (ANGIOSPERM); PHASEOLUS VULGARIS;

EID: 0033198092     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI.1999.12.9.774     Document Type: Article

References (93)

1. Aarts, M. G. M., te Lintel Hekkert, B., Holub, E. B., Beynon, J. L., Stiekema, W. J., and Pereira, A. 1998. Identification of R-gene homologous DNA fragments genetically linked to disease resistance loci in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 11:251-258.
2. Adam-Blondon, A. F., Sévignac, M., Dron, M., and Bannerot, H. 1994. A genetic map of common bean to localize specific resistance genes against anthracnose. Genome 37:915-924.
3. Altschul, S. F., Gish, W., Miller, M., Myers, E. W., and Lipman, D. J. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
4. Alzate-Marin, A. L., Baia, G. S., de Paula Junior, T. J., de Carvalho, G. A., de Baros, E. G., and Moreira, M. A. 1997. Inheritance of anthracnose resistance in common bean differential cultivar AB 136. Plant Dis. 81:996-998.
5. Barrett, J. A. 1985. The gene-for-gene hypothesis: Parable or paradigm. Pages 215-225 in: Ecology and Genetics of Host-Parasite Interactions. D. Rollinson and R. M. Anderson, eds. Academic, New York.
6. Becerra-Velásquez, V. L., and Gepts, P. 1994. RFLP diversity of common bean (Phaseolus vulgaris) in its centres of origin. Genome 37: 256-263.
7. Bent, A. F., Kunkel, B. N., Dahlbeck, D., Brown, K. L., Schmidt, R., Giraudat, J., Leung, J., and Staskawicz, B. J. 1994. RPS2 of Arabidopsis thaliana: A leucine-rich repeat class of plant disease resistance genes. Science 265:1856-1860.
8. Borst, P., and Greaves, D. R. 1987. Programmed gene rearrangements altering expression. Science 235:658-667.
9. Botella, M. A., Coleman, M. J., Hughes, D. E., Nishimura, M. T., Jones, J. D. G., and Somerville, S. C. 1997. Map positions of 47 Arabidopsis sequences with sequence similarity to disease resistance genes. Plant J. 12:1197-1211.
10. Burdon, J. J. 1994. The distribution and origin of genes for race-specific resistance to Melampsora lini in Linum marginale. Evolution 48: 1564-1575.
11. Burdon, J. J. 1996. The role of race specific resistance in natural populations. Oikos 76:411-416.
12. Burdon, J. J. 1997. The evolution of gene-for-gene interactions in natural pathosystems. Pages 245-262 in: The Gene-for-Gene Relationship in Plant-Parasite Interactions. I. R. Crute, E. B. Holub, and J. J. Burdon, eds. CAB Int., Wallingford, UK.
13. Burdon, J. J., and Jarosz, A. M. 1991. Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini: I. Patterns of resistance and racial variation in a large host population. Evolution 45:205-217.
14. Burdon, J. J. and Thompson, J. N. 1995. Changed patterns of resistance in a population of Linum marginale and the rust pathogen Melampsora lini. J. Ecol. 83:199-206.
15. Chaboudez, P., and Burdon, J. J. 1995. Frequency-dependent selection in a wild plant-pathogen system. Oecologia 102:490-493.
16. Clarke, D. D. 1997. The genetic structure of natural pathosystems. Pages 231-243 in: The Gene-for-Gene Relationship in Plant-Parasite Interactions. I. R. Crute, E. B. Holub, and J. J. Burdon, eds. CAB Int., Wallingford, UK.
17. Crute, I. R., and Pink, D. A. C. 1996. Genetics and utilization of pathogen resistance in plants. Plant Cell 8:1747-1755.
18. Debouck, D. G., Toro, O., Paredes, O. M., Johnson, W. C., and Gepts, P. 1993. Genetic diversity and ecological distribution of Phaseolus vulgaris (Fabaceae) in northern South America. Econ. Bot. 47:408-423.
19. Delgado-Salinas, A., Bonet, A., and Gepts, P. 1988. The wild relative of Phaseolus vulgaris in Middle America. Pages 163-184 in: Genetic Resources of Phaseolus Beans. P. Gepts, eds. Kluwer Academic Pub., London.
20. Dickinson, M. J., Jones, D. A., and Jones, J. D. G. 1993. Close linkage between the Cf-2/Cf-5 and Mi resistance loci in tomato. Mol. Plant-Microbe Interact. 6:341-347.
21. Ellis, J. G., Lawrence, E. J., Finnegan, E. J., and Anderson, P. A. 1995. Contrasting complexity of two rust resistance loci in flax. Proc. Natl. Acad. Sci. USA 92:4185-4188.
22. Fabre, J. V., Julien, J., Parisot, D., and Dron, M. 1995. Analysis of diverse isolates of Colletotrichum lindemuthianum infecting common bean using molecular markers. Mycol. Res. 99:429-435.
23. Flor, H. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275-296.
24. Fouilloux, G. 1976. L'anthracnose du haricot (Colletotrichum lindemuthianum, Sacc et Magn.): Nouvelles sources de resistance et nouvelles races physiologiques. Ann. Amélior. Plant. 26:443-453.
25. Frank, S. A. 1992. Models of plant-pathogen coevolution. Trends Genet. 8:213-219.
26. Frank, S. A. 1997. Spatial processes in host-parasite genetics. Pages 325-352 in: Metapopulation Dynamics: Ecology, Genetics, Evolution. I. Hanski and M. E. Gilpin, eds. Academic Press, New York.
27. Frederick, R. D., Thilmony, R. L., Sessa, G., and Martin, G. B. 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.
28. Freyre, R., Skroch, P., Geffroy, V., Adam-Blondon, A. F., Shirmohamadali, A., Johnson, W. C., Llaca, V., Nodari, R. O., Pereira, P. A., Tsai, S. M., Tohme, J., Dron, M., Nienhuis, J., Vallejos, C. E., and Gepts, P. 1998. Towards an integrated linkage map of common bean. 4. Development of a core linkage map and alignment of RFLP maps. Theor. Appl, Genet. 97:847-856.
29. Gandon, S., Capowiez, Y., Dubois, Y., Michalakis, Y., and Olivieri, I. 1996. Local adaptation and gene-for-gene coevolution in a meta-population model. Proc. R. Soc. Lond. B 263:1003-1009.
30. Geffroy, V., Creusot, F., Falquet, J., Séviguac, M., Adam-Blondon, A. F., Bannerot, H., Gepts, P., and Dron, M. 1998. A family of LRR sequences in the vicinity of the Co-2 locus for anthracnose resistance in Phaseolus vulgaris and its potential use in marker-assisted selection. Theor. Appl. Genet. 96:494-502.
31. Gepts, P. 1988. Phaseolin as an evolutionary marker. Pages 215-241 in: Genetic Resources of Phaseolus Beans. P. Gepts, eds. Kluwer Academic Pub., London.
32. Gepts, P. 1993. The use of molecular and biochemical markers in crop evolution studies. Evol. Biol. 27:51-94.
33. Gepts, P. 1998. Origin and evolution of common bean: Past events and recent trends. HortScience 33:1124-1130.
34. Gepts, P., and Bliss, F. A. 1988. Dissemination pathways of common bean (Phaseolus vulgaris, Fabaceae) deduced from phaseolin electrophoretic variability. II Europe and Africa. Econ. Bot. 42:86-104.
35. Gepts, P., and Debouck, D. 1991. Origin, domestication, and evolution of the common bean (Phaseolus vulgaris L.). Pages 7-53 in: Common Beans: Research for Crop Improvement. A. Van Schoonhoven and O. Voysest, eds. CAB Int., Wallingford, UK.
36. Grant, M. R., Godiard, L., Straube, E., Ashfield, T., Lewald, J., Sattler, A., Innes, R. W., and Dangl, J. L. 1995. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269: 843-846.
37. Guzmán, P., Gilbertson, R. L., Nodari, R., Johnson, W. C., Temple, S. R., Mandala, D., Mkandawire, A. B. C., and Gepts, P. 1995. Characterization of variability in the fungus Phaeoisariopsis griseola suggests coevolution with the common bean (Phaseolus vulgaris). Phytopathology 85:600-607.
38. Hammond-Kosack, K. E. and Jones, J. D. G. 1997. Plant disease resistance genes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:575-607.
39. Higgins, D. G., and Sharp, P. M. 1988. CLUSTAL: A package for performing multiple sequence alignments on a microcomputer. Gene 73:237-244.
40. Jana, S., and Nevo, E. 1991. Variation in response to infection with Erysiphe graminis hordei and Puccinia hordei in some wild barley populations in a centre of diversity. Euphytica 57:130-140.
41. Jarosz, A. M., and Burdon, J. J. 1991. Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini: II. Local and regional variation in patterns of resistance and racial structure. Evolution 47:1618-1627.
42. Jorgensen, J. H. 1992. Multigene families of powdery mildew resistance genes in locus Mla on barley chromosome 5. Plant Breed. 108:53-59.
43. Kaloshian, I., Lange, W. H., and Williamson, V. M. 1995. An aphid-resistance locus is tightly linked to the nematode-resistance gene, Mi, in tomato. Proc. Natl. Acad. Sci. USA 92:622-625.
44. Kaltz, O., and Shykoff, J. A. 1998. Local adaptation in host-parasite systems. Heredity 81:361-370.
45. Kami, J., Velasquez, V. B., Debouck, D. G., and Gepts, P. 1995. Identification of presumed ancestral DNA sequences of phaseolin in Phaseolus vulgaris. Proc. Natl. Acad. Sci. USA 92:1101-1104.
46. Kanazin, V., Marek, L. F., and Shoemaker, R. C. 1996. Resistance gene analogs are conserved and clustered in soybean. Proc. Natl. Acad. Sci. USA 93:11746-11750.
47. Kearney, B., and Staskawicz, B. J. 1990. Widespread distribution and fitness contribution of Xanthomonas campestris avirulence avrBs2. Nature 346:385-386.
48. Kelly, J. D., and Young, R. A. 1996. Proposed symbols for anthracnose resistance genes. Annu. Rep. Bean Improv. Coop. 39:20-24.
49. Kobe, B., and Deisenhofer, J. 1994. The leucine-rich repeat: A versatile binding motif. Trends Biochem. Sci. 19:415-421.
50. Koenig, R., and Gepts, P. 1989. Allozyme diversity in wild Phaseolus vulgaris: Further evidence for two major centers of genetic diversity. Theor. Appl. Genet. 78:809-817.
51. Kosambi, D. D. 1944. The estimation of map distances from recombination values. Ann. Eug. 12:172-175.
52. Lander, E. S., Green, P., Abrahamson, J., A., B., Daly, M. J., Lincoln, S. E., and Newburg, L. 1987. MAPMAKER: An interactive computer package for constructing primary generic linkage maps of experimental and natural populations. Genomics 1:174-181.
53. Lauge, R., Joosten, M. H. A. J., Haanstra, J. P. W., Goodwin, P. H., Lindhout, P., and DeWit, P. J. G. M. 1998. Successful search for a resistance gene in tomato targeted against a virulence factor of a fungal pathogen. Proc. Natl. Acad. Sci. USA 95:9014-9018.
54. Leister, D., Ballvora, A., Salamini, F., and Gebhardt, C. 1996. A PCR-based approach for isolating pathogen resistance genes from potato with potential for wide application in plants. Nature Genet. 14:421-429.
55. Leister, D., Kurth, J., Laurie, D. A., Yano, M., Sasaki, T., Devos, K., Graner, A., and Schulze-Lefert, P. 1998. Rapid reorganization of resistance gene homologues in cereal genomes. Proc. Natl. Acad. Sci. USA 95:370-375.
56. Lenné, J. M. 1988. Variation in reaction to anthracnose within native Stylosanthes capitata populations in Minas Gerais, Brazil. Phytopathology 78:131-134.
57. Meyers, B. C., Chin, D. B., Shen, K. A., Sivaramakrishman, S., Lavelle, D. O., Zhang, Z., and Michelmore, R. W. 1998. The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell. 10:1817-1832.
58. Michelmore, R. W., and Meyers, B. C. 1998. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 8:1113-1130.
59. Mindrinos, M., Katagiri, F., Yu, G. L., and Ausubel, F. M. 1994. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78:1089-1099.
60. Nodari, R. O., Koinange, E. M. K., Kelly, J. D., and Gepts, P. 1992. Towards an integrated linkage map of common bean. 1. Development of genomic DNA probes and levels of restriction fragment length polymorphism. Theor. Appl. Genet. 84:186-192.
61. Nodari, R. O., Tsai, S. M., Gilbertson, R. L., and Gepts, P. 1993. Towards an integrated linkage map of common bean. 2. Development of an RFLP-based linkage map. Theor. Appl. Genet. 85:513-520.
62. Parker, M. A. 1985. Local population differentiation for compatibility in an annual legume and its host-specific fungal pathogen. Evolution 39:713-723.
63. Parniske, M., Hammond-Kosack, K. E., Golstein, C., Thomas, C. M., Jones, D. A., Harrison, K., Wulff, B. B. H., and Jones, J. D. G. 1997. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91:821-832.
64. Pastor-Corrales, M. A., Otoya, M. M., Molina, A., and Singh, S. P. 1995. Resistance to Colletotrichum lindemuthianum isolates from Middle America and Andean South America in different common bean races. Plant Dis. 79:63-67.
65. Pedersen, W. L., and Leath, S. 1988. Pyramiding major genes for resistance to maintain residual effects. Annu. Rev. Phytopathol. 26:369-378.
66. Pryor, T. 1987. The origin and structure of fungal disease resistance genes in plants. Trends Genet. 3:157-161
67. Pryor, T., and Ellis, J. 1993. The genetic complexity of fungal resistance genes in plants. Adv. Plant Pathol. 10:281-305.
68. Richter, T. E., Pryor, T. J., Bennetzen, J. L., and Hulbert, S. H. 1995. New rust resistance specificities associated with recombination in the Rp1 complex in maize. Genetics 141:373-381.
69. Rohe, M., Gierlich, A., Hermann, H., Hahn, M., Schmidt, B., Rosahl, S., and Knogge, W. 1995. The race-specific elicitor, NIP1, from the barley pathogen, Rhynchosporium secalis, determines avirulence on host plants of the Rrs1 resistance genotypes. EMBO J. 14:4168-4177.
70. Ronald, P. C. 1998. Resistance gene evolution. Curr. Opin. Plant Biol. 1: 294-298.
71. Shapiro, S. S., and Wilk, M. B. 1965. An analysis of variance test for normality (complete samples). Biometrika 52:591-611.
72. Shen, K. A., Meyers, B. C., Islam-Faridi, M. N., Chin, D. B., Stelly, D. M., and Michelmore, R. W. 1998. Resistance gene candidates identified by PCR with degenerate oligonucleotide primers map to clusters of resistance genes in lettuce. Mol. Plant-Microbe Interact. 11:815-823.
73. Sicard, D., Michalakis, Y, Dron, M., and Neema, C. 1997. Genetic diversity and pathogenic variation of Colletotrichum lindemuthianum in the three centers of diversity of its host, Phaseolus vulgaris. Phytopathology 87:807-813.
74. Simms, E. L. 1996. The evolutionary genetics of plant-pathogen systems. BioScience 46:136-145
75. Singh, S. P., Nodari, R., and Gepts, P. 1991. Genetic diversity in cultivated common bean. I. Allozymes. Crop Sci. 31:19-23.
76. Song, W. Y., Pi, L. Y., Wang, G. L., Gardner, J., Holsten, T., and Ronald, P. C. 1997. Evolution of the rice Xa21 disease resistance gene family. Plant Cell 9:1279-1287.
77. Sonnante, G., Stockton, T., Nodari, R. O., Becerra-Velasquez, V. L., and Gepts, P. 1994. Evolution of genetic diversity during the domestication of common bean (Phaseolus vulgaris L.). Theor. Appl. Genet. 89:629-635.
78. Speulman, E., Bouchez, D., Holub, E. B., and Beynon, J. L. 1998. Disease resistance gene homologs correlate with disease resistance loci of Arabidopsis thaliana. Plant J. 14:467-474.
79. Steadman, J. R., Beaver, J., Boudreau, M., Coyne, D., Groth, J., Kelly, J., McMillan, M., McMillan, R., Miklas, P., Pastor-Corrales, M., Schwartz, H., and Stavely, J. 1995. Progress reported at the 2nd international bean rust workshop. Annu. Rep. Bean Improv. Coop. 38:1-10.
80. Sudupak, M. A., Bennetzen, J. L., and Hulbert, S. H. 1993. Unequal exchange and meiotic instability of disease-resistance genes in the Rp1 region of maize. Genetics 133:119-125.
81. Sweigard, J. A., Carrol, A. M., Kang, S., Farrali, L., and Chumley, F. G. 1995. Identification, cloning and characterization of PWL2, a gene for host specificity in the rice blast fungus. Plant Cell 7:1221-1233.
82. Thomas, C. M., Jones, D. A., Parniske, M., Harrison, K., Balint-Kurti, P. J., Hatzixanthis, K., and Jones, J. D. G. 1997. Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell 9:2209-2224.
83. Thompson, J. N., and Burdon, J. J. 1992. Gene-for-gene coevolution between plants and parasites. Nature 360:121-125.
84. Thrall, P. H., and Burdon, J. J. 1997. Host-pathogen dynamics in a metapopulation context: The ecological and evolutionary consequences of being spatial. J. Ecol. 85:743-753.
85. Tu, J. C. 1992. Colletotrichum lindemuthianum on bean: Population dynamics of the pathogen and breeding for disease resistance. Pages 203-224 in: Colletotrichum: Biology, Pathology and Control. J. A. Bailey and M. J. Jegger, eds. CAB Int., Wallingford, UK.
86. Vanderbeek, J. G., Pet, G., and Lindhout, P. 1994. Resistance to powdery mildew (Oidium lycopersicum) in Lycopersicon hirsutum is controlled by an incompletely dominant gene Ol-1 on chromosome 6. Theor. Appl. Genet. 89:467-473.
87. Velasquez, V. L. B., and Gepts, P. 1994. RFLP diversity of common bean (Phaseolus vulgaris) in its centres of origin. Genome 37:256-263.
88. Wang, G. L., Ruan, D. L., Song, W. Y., Sideris, S., Chen, L. L., Pi, L. Y., Zhang, S. P., Zhang, Z., Fauquet, C., Gaut, B. S., Whalen, M. C., and Ronald, P. C. 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.
89. Whitham, S., McCormick, S., and Baker, B. 1996. The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato. Proc. Natl. Acad. Sci. USA 93:8776-8781.
90. Witsenboer, H., Kesseli, R. V., Fortin, M. G., Stanghellini, M., and Michelmore, R. W. 1995. Sources and genetic structure of a cluster of genes for resistance to three pathogens in lettuce. Theor. Appl. Genet. 91:178-188.
91. Young, R. A., Melotto, M., Nodari, R. O., and Kelly, J. D. 1998. Marker-assisted dissection of the oligogenic anthracnose resistance in the common bean cultivar, "G2333." Theor. Appl. Genet. 96:87-94.
92. Yu, Y. G., Buss, G. R., and Saghai Maroof, M. A. 1996. Isolation of a superfamily of candidate disease-resistance genes in soybean based on a conserved nucleotide-binding site. Proc. Natl. Acad. Sci. USA 93: 11751-11756.
93. Zamir, D., Ekstein-Michelson, I., Zakay, Y., Navot, N., Zeidan, M., Sarfatti, M., Eshed, Y., Harel, E., Pleban, T., Vanoss, H., Kedar, N., Rabinowitch, H. D., and Czosnek, H. 1994. Mapping and introgression of a tomato yellow leaf curl virus tolerance gene, TY-1. Theor. Appl. Genet. 88:141-146.