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Co-segregation analysis and mapping of the anthracnose Co-10 and angular leaf spot Phg-ON disease-resistance genes in the common bean cultivar Ouro Negro

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Abstract

Anthracnose (ANT) and angular leaf spot (ALS) are devastating diseases of common bean (Phaseolus vulgaris L.). Ouro Negro is a highly productive common bean cultivar, which contains the Co-10 and Phg-ON genes for resistance to ANT and ALS, respectively. In this study, we performed a genetic co-segregation analysis of resistance to ANT and ALS using an F2 population from the Rudá × Ouro Negro cross and the F2:3 families from the AND 277 × Ouro Negro cross. Ouro Negro is resistant to races 7 and 73 of the ANT and race 63-39 of the ALS pathogens. Conversely, cultivars AND 277 and Rudá are susceptible to races 7 and 73 of ANT, respectively. Both cultivars are susceptible to race 63-39 of ALS. Co-segregation analysis revealed that Co-10 and Phg-ON were inherited together, conferring resistance to races 7 and 73 of ANT and race 63-39 of ALS. The Co-10 and Phg-ON genes were co-segregated and were tightly linked at a distance of 0.0 cM on chromosome Pv04. The molecular marker g2303 was linked to Co-10 and Phg-ON at a distance of 0.0 cM. Because of their physical linkage in a cis configuration, the Co-10 and Phg-ON resistance alleles are inherited together and can be monitored with great efficiency using g2303. The close linkage between the Co-10 and Phg-ON genes and prior evidence are consistent with the existence of a resistance gene cluster at one end of chromosome Pv04, which also contains the Co-3 locus and ANT resistance quantitative trait loci. These results will be very useful for breeding programs aimed at developing bean cultivars with ANT and ALS resistance using marker-assisted selection.

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References

  • Adam-Blondon AF, Sevignac M, Dron M, Bannerot H (1994) A genetic map of common bean to localize specific resistance genes against anthracnose. Genome 37:915–924

    Article  PubMed  CAS  Google Scholar 

  • Afanador LK, Haley SD, Kelly JD (1993) Adoption of a ‘mini-prep’ DNA extraction protocol for RAPD marker analysis in common bean (Phaseolus vulgaris L.). Ann Rep Bean Improv Coop 36:10–11

    Google Scholar 

  • Alzate-Marin AL, Costa MR, Arruda KM, 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 

  • Alzate-Marin AL, Souza TLPO, Ragagnin VA, Moreira MA, Barros EG (2004) Allelism tests between the rust resistance genes present in common bean cultivar Ouro Negro and genes Ur-5 and Ur-11. J Phytopathol 152:60–64

    Article  CAS  Google Scholar 

  • Ashfield T, Egan AN, Pfeil BE, Chen NWG, Podicheti R, Ratnaparkhe MB, Ameline-Torregrosa C, Denny R, Cannon S, Doyle JJ, Geffroy V, Roe BA, Saghai Maroof MA, Young ND, Innes RW (2012) Evolution of a complex disease resistance gene cluster in diploid Phaseolus and tetraploid Glycine. Plant Physiol 159:336–354

    Article  PubMed  CAS  Google Scholar 

  • Blair MW, Pedraza F, Buendia HF, Gaitán-Solís 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 

  • Caixeta ET, Borém A, Niestche S, Moreira MA, Barros EG (2003) Inheritance of angular leaf spot resistance in common bean line BAT 332 and identification of RAPD markers linked to the resistance gene. Euphytica 134:297–303

    Article  CAS  Google Scholar 

  • Caixeta ET, Borém A, Alzate-Marin AL, Fagundes S, Morais SMG, Barros EG, Moreira MA (2005) Allelic relationships for genes that confer resistance to angular leaf spot in common bean. Euphytica 145:237–245

    Article  CAS  Google Scholar 

  • Campa A, Giraldez R, Ferreira JJ (2011) Genetic analysis of the resistance to eight anthracnose races in the common bean differential cultivar Kaboon. Phytopathology 101:757–764

    Article  PubMed  Google Scholar 

  • Corrêa RX, Costa MR, Good-God PI, Ragagnin VA, Faleiro FG, Moreira MA, Barros EG (2000) Sequence characterized amplified regions linked to rust resistance genes in the common bean. Crop Sci 40:804–807

    Article  Google Scholar 

  • Corrêa RX, Good-God PI, Oliveira MLP, Nietsche S, Moreira MA, Barros EG (2001) Herança da resistência à mancha-angular do feijoeiro e identificação de marcadores moleculares flanqueando o loco de resistência. Fitopatol Bras 26:27–32

    Article  Google Scholar 

  • Correa-Victoria FJ, Pastor-Corrales MA, Saettler AW (1989) Angular leaf spot. In: Schwartz HF, Pastor-Corrales MA (eds) Bean production problems in the tropics, 2nd edn. CIAT, Colombia, pp 59–76

    Google Scholar 

  • Crous PW, Liebenberg MM, Braun U, Groenewald JZ (2006) Re-evaluating the taxonomic status of Phaeoisariopsis griseola, the causal agent of angular leaf spot of bean. Stud Mycol 55:163–173

    Article  PubMed  Google Scholar 

  • David P, Sévignac M, Thareau V, Catillon Y, Kami J, Gepts P, Langin T, Geffroy V (2008) BAC end sequences corresponding to the B4 resistance gene cluster in common bean: a resource for markers and synteny analyses. Mol Genet Genomics 280:521–533

    Article  PubMed  CAS  Google Scholar 

  • Faleiro FG, Nietsche S, Ragagnin VA, Borém A, Moreira MA, Barros EG (2001) Resistance of common bean rust and angular leaf spot under greenhouse conditions. Fitopatol Bras 26:86–89

    Google Scholar 

  • Freyre R, Skrock PW, Geffroy V, Adam-Blondon AF, Shirmohamadali A, Johnson WC, Llaca V, Nodari RO, Pereira PA, Tsai SM, Tohme J, Dron M, Nienhuis J, Vallejo 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 

  • Gaitán-Solís E, Duque MC, Edwards KJ, Tohme J (2002) Microsatellite repeats in common bean (Phaseolus vulgaris): isolation, characterization and cross-species amplification in Phaseolus ssp. Crop Sci 42:2128–2136

    Article  Google Scholar 

  • Geffroy V, Sicard D, 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, Sévignac M, De Oliveira JCF, Fouilloux G, Skroch P (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 

  • Geffroy V, Sévignac M, Billant P, Dron M, Langin T (2008) Resistance to Colletotrichum lindemuthianum in Phaseolus vulgaris: a case study for mapping two independent genes. Theor Appl Genet 116:407–415

    Article  PubMed  CAS  Google Scholar 

  • Geffroy V, Macadre C, David P, Pedrosa-Harand A, Sévignac M, Dauga C, Langin T (2009) Molecular analysis of a large subtelomeric nucleotide-binding-site-leucine-rich-repeat family in two representative genotypes of the major gene pools of Phaseolus vulgaris. Genetics 181:405–419

    Article  PubMed  CAS  Google Scholar 

  • Gepts P (1987) Characterizing plant phenology. In: Wisiol K, Hesketh J (eds) Plant growth modeling for resource management. CRC Press, Boca Raton, pp 3–24

    Google Scholar 

  • Gepts P (1999) Development of an integrated genetic linkage map in common bean (Phaseolus vulgaris L.) and its use. In: Singh S (ed) Bean breeding for the 21st century. Kluwer, Dordrecht, The Netherlands, pp 53–91 (389–400)

    Google Scholar 

  • Gepts P, Aragão F, de Barros E, Blair MW, Brondani R, Broughton W, Galasso I, Hernández G, Kami J, Lariguet P, McClean P, Melotto M, Miklas P, Pauls P, Pedrosa-Harand A, Porch T, Sánchez F, Sparvoli F, Yu K (2008) Genomics of Phaseolus beans, a major source of dietary protein and micronutrients in the tropics. In: Moore PH, Ming R (eds) Genomics of tropical crop plants. Springer, Berlin, pp 113–143

    Chapter  Google Scholar 

  • Gonçalves AMO, Gonçalves-Vidigal MC, Vidigal Filho PS, Poletine JP, Lacanallo GF, Coimbra GK (2010) Characterization of the anthracnose resistance gene in Andean common bean Corinthiano cultivar. Ann Rep Bean Improv Coop 53:220–221

    Google Scholar 

  • Gonçalves-Vidigal MC, Kelly JD (2006) Inheritance of anthracnose resistance in the common bean cultivar Widusa. Euphytica 151:411–419

    Article  Google Scholar 

  • Gonçalves-Vidigal MC, Sakiyama NS, Vidigal Filho PS, Amaral JRAT, Poletine JP, Oliveira VR (2001) Resistance of common bean cultivar AB 136 races 31 and 69 of Colletotrichum lindemuthianum: the Co-6 locus. Crop Breed Appl Biotech 1:99–104

    Article  Google Scholar 

  • Gonçalves-Vidigal MC, Lacanallo GF, Vidigal Filho PS (2008) A new gene conferring resistance to anthracnose in Andean common bean (Phaseolus vulgaris L.) cultivar ‘Jalo Vermelho’. Plant Breed 127:592–596

    Article  Google Scholar 

  • Gonçalves-Vidigal MC, Vidigal Filho PS, Medeiros AF, Pastor-Corrales MA (2009) Common bean landrace Jalo Listras Pretas is the source of a new Andean anthracnose resistance gene. Crop Sci 49:133–138

    Article  Google Scholar 

  • Gonçalves-Vidigal MC, Cruz AS, Garcia A, Kami J, Vidigal Filho PS, Sousa LL, McClean P, Gepts P, Pastor-Corrales MA (2011) Linkage mapping of the Phg-1 and Co-1 4 genes for resistance to angular leaf spot and anthracnose in the common bean cultivar AND 277. Theor Appl Genet 122:893–903

    Article  PubMed  Google Scholar 

  • Gonçalves-Vidigal MC, Meirelles AC, Poletine JP, Sousa LL, Cruz AS, Nunes MP, Lacanallo GF, Vidigal Filho PS (2012a) Genetic analysis of anthracnose resistance in ‘Pitanga’ dry bean cultivar. Plant Breed 131:423–429

    Article  Google Scholar 

  • Gonçalves-Vidigal MC, Vidigal Filho PS, Nogueira LM, Reck SAC, Oliveira MB, Motomiya WR, Lacanallo GF, Cruz AS, Grunvald AK, Nunes MPBP, Sousa LL, Pastor-Corrales MA (2012b) Reaction of common bean cultivars inoculated simultaneously with Colletotrichum lindemuthianum and Pseudocercospora griseola. Ann Rep Bean Improv Coop 55:97–98

    Google Scholar 

  • Inglis DA, Hagedorn J, Rand RE (1988) Use of dry inoculum to evaluate beans for resistance to anthracnose and angular leaf spot. Plant Dis 72:771–774

    Article  Google Scholar 

  • Kang Y, Kim K, Shim S, Yoon M, Sun S, Kim M, Van K, Lee S-H (2012) Genome-wide mapping of NBS-LRR genes and their association with disease resistance in soybean. BMC Plant Biol 12:139

    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, Gepts P, Miklas PN, Coyne DP (2003) Tagging and mapping of genes and QTL and molecular marker-assisted selection for traits of economic importance in bean and cowpea. Field Crops Res 82:135–154

    Article  Google Scholar 

  • Lincoln SE, Lander SL (1993) Mapmaker/exp 3.0 and Mapmaker/QTL 1.1. Whitehead Institute of Medical Research. Technical Report, Cambridge

  • Lopez CE, Acosta IF, Jara C, Pedraza P, Gaitan-Solis E, Gallego G, Beebe S, Thome J (2003) Identifying resistance gene analogs associated with resistances to different pathogens in common bean. Phytopathology 93:88–95

    Article  PubMed  CAS  Google Scholar 

  • Mahuku GS, Iglesias AM, Jara C (2009) Genetics of angular leaf spot resistance in the Andean common bean accession G5686 and identification of markers linked to the resistance genes. Euphytica 167:381–396

    Article  CAS  Google Scholar 

  • Mahuku GS, Henriquez MA, Montoya C, Jara C, Teran H, Beebe S (2011) Inheritance and development of molecular markers linked to angular leaf spot resistance genes in the common bean accession G10909. Mol Breed 28:57–71

    Article  Google Scholar 

  • Martin T, Biruma M, Fridborg I, Okori P, Dixelius C (2011) A highly conserved NB-LRR encoding gene cluster effective against Setosphaeria turcica in sorghum. BMC Plant Biol 11:151

    Article  PubMed  CAS  Google Scholar 

  • McClean P, Mamidi S, McConnell M, Chikara S, Lee R (2010) Synteny mapping between common bean and soybean reveals extensive blocks of shared loci. BMC Genomics 11:184

    Article  PubMed  Google Scholar 

  • McConnell M, Mamidi S, Lee R, Chikara S, Rossi M, Papa R, McClean P (2010) Syntenic relationships among legumes revealed using a gene-based genetic linkage map of common bean (Phaseolus vulgaris L.). Theor Appl Genet 121:1103–1116

    Article  PubMed  Google Scholar 

  • McDowell JM, Simon SA (2006) Recent insights into R gene evolution. Mol Plant Pathol 5:437–448

    Article  Google Scholar 

  • McHale LK, Haun WJ, Xu WW, Bhaskar PB, Anderson JE, Hyten DL, Gerhardt DJ, Jeddeloh JA, Stupar RM (2012) Structural variants in the soybean genome localize to clusters of biotic stress-response genes. Plant Physiol 159:1295–1308

    Article  PubMed  CAS  Google Scholar 

  • Meksem K, Doubler TW, Chancharoenchai K, Nijti N, Chang SJ, Arelli APR, Cregan PE, Gray LE, Gibson PT, Lightfoot DA (1999) Clustering among loci underlying soybean resistance to Fusarium solani, SDS and SCN in near-isogenic lines. Theor Appl Genet 99:1131–1142

    Article  CAS  Google Scholar 

  • Méndez-Vigo B, Rodríguez-Suárez C, Pañeda A, Ferreira JJ, Giraldez R (2005) Molecular markers and allelic relationships of anthracnose resistance gene cluster B4 in common bean. Euphytica 141:237–245

    Article  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 using segregating populations. Proc Natl Acad Sci USA 88:9828–9832

    Article  PubMed  CAS  Google Scholar 

  • Miklas PN, Pastor-Corrales MA, Jung G, Coyne DP, Kelly JD, McClean PE, Gepts P (2002) Comprehensive linkage map of bean rust resistance genes. Ann Rep Bean Improv Coop 45:125–129

    Google Scholar 

  • Miklas PN, Hu J, Grunwald NJ, Larsen KM (2006) Potential application of TRAP (targeted region amplified polymorphism) markers of mapping and tagging disease resistance traits in common bean. Crop Sci 46:910–916

    Article  CAS  Google Scholar 

  • Nodari RO, Tsai SM, Guzmán P, Gilbertson RL, Gepts P (1993) Toward an integrated linkage map of common bean. III. Mapping genetic factors controlling host–bacteria interactions. Genetics 134:341–350

    PubMed  CAS  Google Scholar 

  • Oblessuc PR, Borges A, Chowdhury B, Caldas DGG, Tsai SM, Camargo LEA, Melotto M (2012) Dissecting Phaseolus vulgaris innate immune system against Colletotrichum lindemuthianum infection. PLoS One 7:e43161

    Article  PubMed  CAS  Google Scholar 

  • Pastor-Corrales MA (1991) Estandarización de variedades diferenciales y de designación de razas de Colletotrichum lindemuthianum. Phytopathology 81:694

    Google Scholar 

  • Pastor-Corrales MA, Tu JC (1989) Anthracnose. In: Schwartz HF, Pastor-Corrales MA (eds) Bean production problems in the tropics. CIAT, Colombia, pp 77–104

    Google Scholar 

  • Pastor-Corrales MA, Otoya MM, Molina A, Singh SP (1995) Resistance to Colletotrichum lindemuthianum isolates from Middle America and Andean South America in different common bean races. Plant Dis 79:63–67

    Article  Google Scholar 

  • Pedrosa-Harand A, Porch T, Gepts P (2008) Standard nomenclature for common bean chromosomes and linkage groups. Ann Rep Bean Improv Coop 51:106–107

    Google Scholar 

  • Queiroz VT, Sousa CS, Costa MR, Sanglard DA, Arruda KMA, Souza TLPO, Ragagnin VA, Barros EG, Moreira MA (2004) Development of SCAR markers linked to common bean angular leaf spot resistance genes. Ann Rep Bean Improv Coop 47:237–238

    Google Scholar 

  • Ragagnin VA, Souza TLPO, Sanglard DA, Arruda KMA, Costa MR, Alzate-Marin AL, Carneiro JES, Moreira MA, Barros G (2009) Development and agronomic performance of common bean lines simultaneously resistant to anthracnose, angular leaf spot and rust. Plant Breed 128:156–163

    Article  Google Scholar 

  • Rodríguez-Suárez C, Mendéz-Vigo B, Pañeda A, Ferreira JJ, Giraldez R (2007) A genetic linkage map of Phaseolus vulgaris L. and localization of genes for specific resistance to six races of anthracnose (Colletotrichum lindemuthianum). Theor Appl Genet 114:713–722

    Article  PubMed  Google Scholar 

  • Sanglard DA, Balbi BP, de Barros EG (2009) An efficient protocol for isolation, sporulation and maintenance of Pseudocercospora griseola. Ann Rep Bean Improv Coop 52:62–63

    Google Scholar 

  • Schwartz HF, Pastor-Corrales MA (1989) Bean production problems in the tropics. CIAT, Cali, pp 105–157

    Google Scholar 

  • Singh SP, Schwartz F (2010) Breeding common bean for resistance to diseases: a review. Crop Sci 50:2199–2223

    Article  Google Scholar 

  • Sousa LL, Gonçalves-Vidigal MC, Gonçalves AO, Vidigal Filho PS, Awale H, Kelly JD (2013) Molecular mapping of the anthracnose resistance gene Co-15 in the common bean cultivars Corinthiano. Ann Rep Bean Improv Coop 56:45–46

    Google Scholar 

  • Souza TLPO, Dessaune SN, Sanglard DA, Moreira MA, Barros EG (2011) Characterization of the rust resistance gene present in the common bean cultivar Ouro Negro, the main rust resistance source used in Brazil. Plant Pathol 60:839–845

    Article  Google Scholar 

  • Voorrips RE (2002) Mapchart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was financially supported by the National Council for Scientific and Technological Development (CNPq). Anelise S. Cruz was supported by a scholarship from Capes. We would like to thank Andressa Gonçalves Vidigal for additional review of the manuscript. M.C. Gonçalves-Vidigal and P.S. Vidigal Filho are grateful for grants from CNPq.

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Communicated by D. Lightfoot.

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Gonçalves-Vidigal, M.C., Cruz, A.S., Lacanallo, G.F. et al. Co-segregation analysis and mapping of the anthracnose Co-10 and angular leaf spot Phg-ON disease-resistance genes in the common bean cultivar Ouro Negro. Theor Appl Genet 126, 2245–2255 (2013). https://doi.org/10.1007/s00122-013-2131-8

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