Abstract
Anthracnose, caused by the hemibiotrophic fungal pathogen Colletotrichum lindemuthianum is a devastating disease of common bean. Resistant cultivars are economical means for defense against this pathogen. In the present study, we mapped resistance specificities against 7 C. lindemuthianum strains of various geographical origins revealing differential reactions on BAT93 and JaloEEP558, two parents of a recombinant inbred lines (RILs) population, of Meso-american and Andean origin, respectively. Six strains revealed the segregation of two independent resistance genes. A specific numerical code calculating the LOD score in the case of two independent segregating genes (i.e. genes with duplicate effects) in a RILs population was developed in order to provide a recombination value (r) between each of the two resistance genes and the tested marker. We mapped two closely linked Andean resistance genes (Co-x, Co-w) at the end of linkage group (LG) B1 and mapped one Meso-american resistance genes (Co-u) at the end of LG B2. We also confirmed the complexity of the previously identified B4 resistance gene cluster, because four of the seven tested strains revealed a resistance specificity near Co-y from JaloEEP558 and two strains identified a resistance specificity near Co-9 from BAT93. Resistance genes found within the same cluster confer resistance to different strains of a single pathogen such as the two anthracnose specificities Co-x and Co-w clustered at the end of LG B1. Clustering of resistance specificities to multiple pathogens such as fungi (Co-u) and viruses (I) was also observed at the end of LG B2.
Similar content being viewed by others
References
Adam-Blondon AF, Sevignac M, Dron M (1994) A genetic map of common bean to localize specific resistance genes against anthracnose. Genome 37:915–924
Allard RW (1956) Formulas and tables to facilitate the calculation of recombination values in heredity. Hilgardia 24:235–278
Alzate-Marin AL, Baia GS, de Paula Junior TJ, de Carvalho GA, de Baros EG, Moreira MA (1997) Inheritance of anthracnose resistance in common bean differential cultivar AB 136. Plant Disease 81:996–998
Alzate Marin AL, Costa MR, Arruda KM, de Barros EG, Moreira MA (2003) Characterization of the anthracnose resistance gene present in Ouro Negro (Honduras 35) common bean cultivar. Euphytica 133:165–169
Ashfield T, Bocian A, Held D, Henk AD, Marek LF, Danesh D, Penuela S, Meksem K, Lightfoot DA, Young ND, Shoemaker RC, Innes RW (2003) Genetic and physical localization of the soybean Rpg1-b disease resistance gene reveals a complex locus containing several tightly linked families of NBS-LRR genes. Mol Plant Microbe Interact 16:817–826
Bannerot H (1965) Résultat de l’infection d’une collection de haricots par six races physiologiques d’anthracnose. Ann Amélior Plantes 15:201–222
Bannerot H, Derieux M, Fouilloux G (1971) Mise en évidence d’un second gène de résistance totale à l’anthracnose chez le haricot. Ann Amélior Plantes 21:83–85
Barrus MF (1911) Variation of varieties of beans in their susceptibility to anthracnose. Phytopathology 1:190–195
Barrus MF (1915) An anthracnose-resistant red kidney bean. Phytopathology 5:303–311
Bennetzen JL, Hulbert SH (1992) Extramarital sex amongst the beets—organization, instability and evolution of plant-disease resistance genes. Plant Mol Biol 20:575–578
Blair MW, Pedraza F, Buendia HF, Gaitan Solis E, Beebe SE, Gepts P, Tohme J (2003) Development of a genome-wide anchored microsatellite map for common bean (Phaseolus vulgaris L.). Theor Appl Genet 107:1362–1374
Broughton WJ, Hernandez G, Blair M, Beebe S, Gepts P, Vanderleyden J (2003) Beans (Phaseolus spp.)—model food legumes. Plant Soil 252:55–128
Caranta C, Palloix A, Gebre-Selassie K, Lefebvre V, Moury B, Daubèze AM (1996) A complementation of two genes originating from susceptible Capsicum annum lines confers a new and complete resistance to pepper veinal mottle virus. Phytopathololy 86:739–743
Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host–microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814
Concibido VC, Young ND, Lange DA, Denny RL, Danesh D, Orf JH (1996) Targeted comparative genome analysis and qualitative mapping of a major partial-resistance gene to the soybean cyst nematode. Theor Appl Genet 93:234–241
Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833
Ferrier-Cana E, Geffroy V, Macadre C, Creusot F, Imbert-Bollore P, Sevignac M, Langin T (2003) Characterization of expressed NBS-LRR resistance gene candidates from common bean. Theor Appl Genet 106:251–261
Ferrier Cana E, Macadre C, Sevignac M, David P, Langin T, Geffroy V (2005) Distinct post-transcriptional modifications result into seven alternative transcripts of the CC-NBS-LRR gene JA1tr of Phaseolus vulgaris. Theor Appl Genet 110:895–905
Flor HH (1955) Host–parasite interaction in flax rust. Its genetics and other implications. Phytopathology 45:680–685
Foster Hartnett D, Mudge J, Larsen D, Danesh D, Yan HH, Denny R, Penuela S, Young ND (2002) Comparative genomic analysis of sequences sampled from a small region on soybean (Glycine max) molecular linkage group G. Genome 45:634–645
Fouilloux G (1976) L’anthracnose du haricot (Colletotrichum lindemuthianum, Sacc et Magn.): nouvelles sources de résistance et nouvelles races physiologiques. Ann Amélior Plantes 26:443–453
Fouilloux G (1979) New races of bean anthracnose and consequences on our breeding programs. In: Maraitre H, Meyer JA (eds) Disease of tropical food crops. Université Catholique de Louvain la Neuve, Belgium, pp 221–235
Freyre R, Skroch PW, Geffroy V, AdamBlondon AF, Shirmohamadali A, Johnson WC, Llaca V, Nodari RO, Pereira PA, Tsai SM, Tohme J, Dron M, Nienhuis J, Vallejos CE, 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
Geffroy V, Sicard D, de Oliveira JCF, Sevignac M, Cohen S, Gepts P, Neema C, Langin T, Dron M (1999) Identification of an ancestral resistance gene cluster involved in the coevolution process between Phaseolus vulgaris and its fungal pathogen Colletotrichum lindemuthianum. Mol Plant Microbe Interact 12:774–784
Geffroy V, Sevignac M, DeOliveira JCF, Fouilloux G, Skroch P, Thoquet P, Gepts P, Langin T, Dron M (2000) Inheritance of partial resistance against Colletotrichum lindemuthianum in Phaseolus vulgaris and co-localization of quantitative trait loci with genes involved in specific resistance. Mol Plant Microbe Interact 13:287–296
Haldane JBS, Waddington CH (1931) Inbreeding and linkage. Genetics 16:357–374
Hammond Kosack KE, Parker JE (2003) Deciphering plant–pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotech 14:177–193
Hayes AJ, Jeong SC, Gore MA, Yu YG, Buss GR, Tolin SA, Maroof MAS (2004) Recombination within a nucleotide-binding-site/leucine-rich-repeat gene cluster produces new variants conditioning resistance to soybean mosaic virus in soybeans. Genetics 166:493–503
Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 39:285–312
Kelly JD, Vallejo VA (2004) A comprehensive review of the major genes conditioning resistance to anthracnose in common bean. HortScience 39:1196–1207
Kelly JD, Young RA (1996) Proposed symbols for anthracnose resistance genes. Annu Rep Bean Improve Coop 39:20–24
Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175
Lander ES, Green 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
Lefebvre V (2004) Molecular markers for genetics and breeding: development and use in pepper (Capsicum spp.). In: Lörz H, Wenze G (eds) Biotechnology in agriculture and forestry molecular marker systems. Springer, Heidelberg, pp 189–214
Leister D, Kurth J, Laurie DA, Yano M, Sasaki T, Devos K, Graner A, SchulzeLefert P (1998) Rapid reorganization of resistance gene homologues in cereal genomes. Proc Natl Acad Sci USA 95:370–375
Marczewski W, Strzelczyk-Zyta D, Hennig J, Witek K, Gebhardt C (2006) Potato chromosomes IX and XI carry genes for resistance to potato virus M. Theor Appl Genet 112:1232–1238
Martin OC, Hospital F (2006) Two- and three-locus tests for linkage analysis using recombinant inbred lines. Genetics 173:451–459
Mastenbroek C (1960) A breeding programs for resistance to anthracnose in dry shell haricot beans, based on a new gene. Euphytica 9:177–184
McHale L, Tan XP, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212
McRostie GP (1919) Inheritance of anthracnose resistance as indicated by a cross between a resistant and a susceptible bean. Phytopathology 9:141–148
Melotto M, Kelly JD (2000) An allelic series at the Co-1 locus conditioning resistance to anthracnose in common bean of Andean origin. Euphytica 116:143–149
Meyers BC, Kozik A, Griego A, Kuang HH, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834
Meyers BC, Kaushik S, Nandety RS (2005) Evolving disease resistance genes. Curr Opin Plant Biol 8:129–134
Michelmore RW (2003) The impact zone: genomics and breeding for durable disease resistance. Curr Opin Plant Biol 6:397–404
Mudge J, Cannon SB, Kalo P, Oldroyd GE, Roe BA, Town CD, Young ND (2005) Highly syntenic regions in the genomes of soybean, Medicago truncatula, and Arabidopsis thaliana. BMC Plant Biol 5:15
Murray J, Larsen J, Michaels TE, Schaafsma A, Vallejos CE, Pauls KP (2002) Identification of putative genes in bean (Phaseolus vulgaris) genomic (Bng) RFLP clones and their conversion to STSs. Genome 45:1013–1024
Nobuta K, Meyers BC (2005) Pseudomonas versus Arabidopsis: models for genomic research into plant disease resistance. Bioscience 55:679–686
Pastor-Corrales MA, Tu JC (1989) Anthracnose. In: Schwartz HF, Pastor-Corrales MA (eds) Bean production problems in the tropics, 2nd edn. Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia, pp 77–104
Pastor-Corrales MA, Erazo OA, Estrada EI, Singh SP (1994) Inheritance of anthracnose resistance in common bean accession G2333. Plant Dis 78:959–962
Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, Depamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam Faridi N, Jones S, Jones Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, de Peer YV, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. and Gray). Science 313:1596–1604
Vallejos CE, Sakiyama NS, Chase CD (1992) A molecular marker-based linkage map of Phaseolus vulgaris L. Genetics 131:733–740
Vallejos CE, Astua Monge G, Jones V, Plyler TR, Sakiyama NS, Mackenzie SA (2006) Genetic and molecular characterization of the I locus of Phaseolus vulgaris. Genetics 172:1229–1242
Young RA, Kelly JD (1996) Characterization of the genetic resistance to Colletotrichum lindemuthianum in common bean differential cultivars. Plant Dis 80:650–654
Young RA, Melotto M, Nodari RO, Kelly JD (1998) Marker-assisted dissection of the oligogenic anthracnose resistance in the common bean cultivar, “G2333”. Theor Appl Genet 96:87–94
Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, Jiang K, Shen J, Tian D (2004) Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol Gen Genomics 271:402–415
Acknowledgment
We thank Guy Fouilloux for helpful discussions. The research was supported by INRA-DGAP, CNRS and Ministère de la recherche.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by D. Mather.
Appendix
Appendix
In the case of two complementary resistance genes (case of complementary epistasis), the same procedure as described previously for two independent genes can be used. The frequency of the different genotypic classes are given in Table 7, which is identical as in Table 4 except that the lines MM/mm and the columns Resistant/Susceptible are inverted, i.e. (x, y, z, t) change to (t, z, y, x). The probability of linkage is:
The value of r maximizing the LOD score is given by substituting (d, c, b, a) for (a, b, c, d) in Eq. (2)
Rights and permissions
About this article
Cite this article
Geffroy, V., Sévignac, M., Billant, P. et al. Resistance to Colletotrichum lindemuthianum in Phaseolus vulgaris: a case study for mapping two independent genes. Theor Appl Genet 116, 407–415 (2008). https://doi.org/10.1007/s00122-007-0678-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-007-0678-y