Skip to main content
Log in

Resistance to Colletotrichum lindemuthianum in Phaseolus vulgaris: a case study for mapping two independent genes

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

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.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

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

    Article  PubMed  CAS  Google Scholar 

  • Allard RW (1956) Formulas and tables to facilitate the calculation of recombination values in heredity. Hilgardia 24:235–278

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bannerot H (1965) Résultat de l’infection d’une collection de haricots par six races physiologiques d’anthracnose. Ann Amélior Plantes 15:201–222

    Google Scholar 

  • 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

    Google Scholar 

  • Barrus MF (1911) Variation of varieties of beans in their susceptibility to anthracnose. Phytopathology 1:190–195

    Google Scholar 

  • Barrus MF (1915) An anthracnose-resistant red kidney bean. Phytopathology 5:303–311

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Broughton WJ, Hernandez G, Blair M, Beebe S, Gepts P, Vanderleyden J (2003) Beans (Phaseolus spp.)—model food legumes. Plant Soil 252:55–128

    Article  CAS  Google Scholar 

  • 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

    Article  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 

  • 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

    Article  CAS  Google Scholar 

  • Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Flor HH (1955) Host–parasite interaction in flax rust. Its genetics and other implications. Phytopathology 45:680–685

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Haldane JBS, Waddington CH (1931) Inbreeding and linkage. Genetics 16:357–374

    PubMed  CAS  Google Scholar 

  • Hammond Kosack KE, Parker JE (2003) Deciphering plant–pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotech 14:177–193

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 39:285–312

    Article  PubMed  CAS  Google Scholar 

  • Kelly JD, Vallejo VA (2004) A comprehensive review of the major genes conditioning resistance to anthracnose in common bean. HortScience 39:1196–1207

    CAS  Google Scholar 

  • Kelly JD, Young RA (1996) Proposed symbols for anthracnose resistance genes. Annu Rep Bean Improve Coop 39:20–24

    Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Martin OC, Hospital F (2006) Two- and three-locus tests for linkage analysis using recombinant inbred lines. Genetics 173:451–459

    Article  PubMed  CAS  Google Scholar 

  • Mastenbroek C (1960) A breeding programs for resistance to anthracnose in dry shell haricot beans, based on a new gene. Euphytica 9:177–184

    Article  Google Scholar 

  • McHale L, Tan XP, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212

    Article  PubMed  CAS  Google Scholar 

  • McRostie GP (1919) Inheritance of anthracnose resistance as indicated by a cross between a resistant and a susceptible bean. Phytopathology 9:141–148

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Meyers BC, Kaushik S, Nandety RS (2005) Evolving disease resistance genes. Curr Opin Plant Biol 8:129–134

    Article  PubMed  CAS  Google Scholar 

  • Michelmore RW (2003) The impact zone: genomics and breeding for durable disease resistance. Curr Opin Plant Biol 6:397–404

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Nobuta K, Meyers BC (2005) Pseudomonas versus Arabidopsis: models for genomic research into plant disease resistance. Bioscience 55:679–686

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Pastor-Corrales MA, Erazo OA, Estrada EI, Singh SP (1994) Inheritance of anthracnose resistance in common bean accession G2333. Plant Dis 78:959–962

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Vallejos CE, Sakiyama NS, Chase CD (1992) A molecular marker-based linkage map of Phaseolus vulgaris L. Genetics 131:733–740

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Young RA, Kelly JD (1996) Characterization of the genetic resistance to Colletotrichum lindemuthianum in common bean differential cultivars. Plant Dis 80:650–654

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Valérie Geffroy.

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:

$$ P(r) = \frac{{{\left( {a + b + c + d} \right)}!}} {{a!b!c!d!}}t^{a} z^{b} y^{c} x^{d} $$

The value of r maximizing the LOD score is given by substituting (d, c, b, a) for (a, b, c, d) in Eq. (2)

Table 7 Frequencies of phenotypic classes, when two complementary resistance genes are present in parent A and that there is a recombination rate r between G1 and marker M

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-007-0678-y

Keywords

Navigation