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High-resolution mapping reveals linkage between genes in common bean cultivar Ouro Negro conferring resistance to the rust, anthracnose, and angular leaf spot diseases

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Abstract

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Co-segregation analysis and high-throughput genotyping using SNP, SSR, and KASP markers demonstrated genetic linkage between Ur-14 and Co-3 4 /Phg-3 loci conferring resistance to the rust, anthracnose and angular leaf spot diseases of common bean.

Abstract

Rust, anthracnose, and angular leaf spot are major diseases of common bean in the Americas and Africa. The cultivar Ouro Negro has the Ur-14 gene that confers broad spectrum resistance to rust and the gene cluster Co-3 4/Phg-3 containing two tightly linked genes conferring resistance to anthracnose and angular leaf spot, respectively. We used co-segregation analysis and high-throughput genotyping of 179 F2:3 families from the Rudá (susceptible) × Ouro Negro (resistant) cross-phenotyped separately with races of the rust and anthracnose pathogens. The results confirmed that Ur-14 and Co-3 4 /Phg-3 cluster in Ouro Negro conferred resistance to rust and anthracnose, respectively, and that Ur-14 and the Co-3 4 /Phg-3 cluster were closely linked. Genotyping the F2:3 families, first with 5398 SNPs on the Illumina BeadChip BARCBEAN6K_3 and with 15 SSR, and eight KASP markers, specifically designed for the candidate region containing Ur-14 and Co-3 4 /Phg-3, permitted the creation of a high-resolution genetic linkage map which revealed that Ur-14 was positioned at 2.2 cM from Co-3 4 /Phg-3 on the short arm of chromosome Pv04 of the common bean genome. Five flanking SSR markers were tightly linked at 0.1 and 0.2 cM from Ur-14, and two flanking KASP markers were tightly linked at 0.1 and 0.3 cM from Co-3 4 /Phg-3. Many other SSR, SNP, and KASP markers were also linked to these genes. These markers will be useful for the development of common bean cultivars combining the important Ur-14 and Co-3 4 /Phg-3 genes conferring resistance to three of the most destructive diseases of common bean.

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References

  • Allen DJ, Dessert M, Trutmann P, Voss J (1989) Common beans in Africa and their constraints. In: Schwartz HF, Pastor-Corrales MA (eds) Bean production problems in the tropics. CIAT, Cali, pp 9–31

    Google Scholar 

  • Alzate-Marin AL, Baia GS, Paula TJ Jr, Carvalho GA, Barros EG, Moreira MA (1997) Inheritance of anthracnose resistance in common bean differential cultivar AB136. Plant Dis 81:996–998

    Article  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 gene present in common bean cultivar Ouro Negro and genes Ur-5 and Ur-11. J Phytopathol 152:60–64

    Article  CAS  Google Scholar 

  • Alzate-Marin AL, Souza KA, Silva MGM, Oliveira EJ, Moreira MA, Barros EG (2007) Genetic characterization of anthracnose resistance genes Co-4 3 and Co-9 in common bean cultivar Tlalnepantla 64 (PI 207262). Euphytica 154:1–8

    Article  CAS  Google Scholar 

  • Augustin E, Coyne DP, Schuster ML (1972) Inheritance of resistance in Phaseolus vulgaris to Uromyces phaseoli typical Brazilian rust race B11 and of plant habit. J Am Soc Hortic Sci 97:526–529

    Google Scholar 

  • Ballantyne B (1978) The genetic basis of resistance to rust caused by Uromyces appendiculatus in bean (Phaseolus vulgaris). Thesis, University of Sidney

  • Bannerot H (1965) Résultats de l’infection d’une collection de haricots par six races physiologiques d’anthracnose. Annual de Amélioré des Plantes 15:201–222

    Google Scholar 

  • Bhakta MS, Jones VA, Vallejos EC (2015) Punctuated distribution of recombination hotspots and demarcation of pericentromeric regions in Phaseolus vulgaris L. PLoS One 10(1):e0116822

    Article  PubMed  PubMed Central  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 

  • Burt AJ, William HM, Perry G, Khanal R, Pauls KP, Kelly JD, Navabi A (2015) Candidate gene identification with SNP marker-based fine mapping of anthracnose resistance gene Co-4 in common bean. PLoS One 10:e0139450

    Article  PubMed  PubMed Central  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 

  • Cao A, Xing L, Wang X, Yang X, Wang W, Sun Y, Qian C, Ni J, Chen Y, Liu D, Wang X, Chen P (2011) Serine/threonine kinase gene Stpk-V, a key member of powdery mildew resistance gene Pm21, confers powdery mildew resistance in wheat. PNAS 108(19):7727–7732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chakraborty A, Sen Gupta PK (1995) Factors affecting cross protection of Fusarium wilt of pigeon pea by soilborne nonpathogenic fungi. Phytoparasitica 23:323–334

    Article  Google Scholar 

  • Christ BJ, Groth JV (1982) Inheritance of resistance in three cultivars of beans to the bean rust pathogen and the interaction of virulence and resistance genes. Phytopathology 72:771–773

    Article  Google Scholar 

  • Christie JM (2007) Phototropin blue-light receptors. Ann Rev Plant Biol 58:21–45

    Article  CAS  Google Scholar 

  • Coimbra-Gonçalves GK, Gonçalves-Vidigal MC, Coelho RT, Valentini G, Vidigal Filho PS, Lacanallo GF, Sousa LL, Elias HT (2016) Characterization and mapping of anthracnose resistance genes in mesoamerican common bean cultivar Crioulo 159. Crop Sci 56:2904–2915

    Article  Google Scholar 

  • Collard BC, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos T Roy Soc B 363:557–572

    Article  CAS  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 H, Pastor-Corrales MA (eds) Bean production problems in the tropics. CIAT, Cali, pp 59–75

    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 Gen Genomics 280:521–533

    Article  CAS  Google Scholar 

  • Elliston J, Kuc J, Williams EB (1976) Protection of Phaseolus vulgaris against anthracnose by Colletotrichum species nonpathogenic to bean. Phytopathology 8:117–126

    Article  Google Scholar 

  • Faleiro FG, Vinhadelli WS, Ragagnin VA, Paula TJ Jr, Moreira MA, Barros EG (1999) Resistência do feijoeiro comum a quatro racas de Uromyces Appendiculatus. Fitopatol Bras 46:11–18

    Google Scholar 

  • Faleiro FG, Ragagnin VA, Corrêa RX, Vinhadelli WS, Moreira MA, Barros EG (2000a) Ligação gênica da resistência à ferrugem e à antracnose na variedade de feijão Ouro Negro. Rev Ceres 47:375–382

    Google Scholar 

  • Faleiro FG, Wender S, Vinhadelli WS, Ragagnin VA, Corrêa RX, Moreira MA, Barros EG (2000b) RAPD markers linked to a block of genes conferring rust resistance to the common bean. Genet Mol Biol 23:399–402

    Article  CAS  Google Scholar 

  • Faleiro FG, Ragagnin VA, Schuster I, Corrêa RX, Good-God PI, Brommonshenkel SH, Moreira MA, Barros EG (2003) Mapeamento de genes de resistência do feijoeiro à ferrugem, antracnose e mancha-angular usando marcadores RAPD. Fitopatol Bras 28:59–66

    Article  Google Scholar 

  • Finke ML, Coyne DP, Steadman JR (1986) The inheritance and association of resistance to rust, common bacterial blight, plant habit and foliar normalities in Phaseolus vulgaris L. Euphytica 35:969–982

    Article  Google Scholar 

  • Fouilloux G (1976) Bean anthracnose: new genes of resistance. Ann Rep Bean Improv Coop 19:36–37

    Google Scholar 

  • Fouilloux G (1979) New races of bean anthracnose and consequences on our breeding programs. In: Maraite H, Meyer JA (eds) Diseases of tropical food crops. Université Catholique de Louvain-La-Neuve, Belgium, pp 221–235

    Google Scholar 

  • Freyre R, Skroch PW, Geffroy V, Adam-Blondon 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 

  • Garcia RAV, Carneiro MS, Sartorato A (2006) Phaeoisariopsis griseola virulence pattern and RAPD diversity. Ann Rep Bean Improv Coop 49:209–210

    Google Scholar 

  • Geffroy V (1997) Dissection génétique de la résistance à Colletotrichum lindemuthianum, agente de l’ anthracnose, chez deux génotypes représentatifs des pools géniques de Phaseolus vulgaris. Thesis, Institut National Agronomique

  • Geffroy V, Delphine S, Oliveira JC, Fsevignac 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 Int 12:774–784

    Article  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  CAS  PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Gonçalves-Vidigal MC (1994) Herança da resistência às raças alfa, delta e capa de Colletotrichum lindemuthianum (Sacc. & Magn.) Scrib. no feijoeiro (Phaseolus vulgaris L.). Thesis, Universidade Federal de Viçosa

  • 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, Silva CR, Vidigal Filho PS, Gonela A, Kvitschal MV (2007) Allelic relationships of anthracnose (Colletotrichum lindemuthianum) resistance in the common bean (Phaseolus vulgaris L.) cultivar Michelite and the proposal of a new anthracnose resistance gene, Co-11. Genet Mol Biol 30:589–593

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Gonçalves-Vidigal MC, Cruz AS, Lacanallo GF, Vidigal Filho PS, Sousa LL, Pacheco CMNA, McClean P, Gepts P, Pastor-Corrales MA (2013) 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

    Article  PubMed  Google Scholar 

  • Hurtado-Gonzales OP, Valentini G, Gilio TAS, Martins AM, Song Q, Pastor-Corrales MA (2017) Fine mapping of Ur-3, a historically important rust resistance locus in common bean. G3 7(2):557–569

    Article  PubMed  Google Scholar 

  • Jung G, Coyne DP, Bokosi J, Steadman JR, Nienhuis J (1998) Mapping genes for specific and adult plant resistance to rust and abaxial leaf pubescence and their genetic relationship using random amplified polymorphic DNA (RAPD) markers in common bean. J Am Soc Hortic Sci 123:859–863

    CAS  Google Scholar 

  • Keim P, Olson TC, Shoemaker RC (1988) A rapid protocol for isolating soybean DNA. Soybean Genet Newsl 15:150–152

    Google Scholar 

  • Keller B, Manzanares C, Jara C, Lobaton JD, Raatz BSB (2015) Fine-mapping of a major QTL controlling angular leaf spot resistance in common bean (Phaseolus vulgaris L.). Theor Appl Genet 128:813–826

    Article  CAS  PubMed  PubMed Central  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. Ann Rep Bean Improv Coop 39:20–24

    Google Scholar 

  • Kelly JD, Stavely JR, Miklas PN (1996) Proposed symbols for rust resistance genes. Ann Rep Bean Improv Coop 39:25–31

    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 

  • Liebenberg MM, Pretorius ZA (2004) Proposal for designation of a rust resistance gene in the large-seeded cultivar Kranskop. Annu Rep Bean Improv Coop 47:255–256

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mahuku GS, Maria Iglesias A, 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(3):381–396

    Article  CAS  Google Scholar 

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

    Article  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 

  • Mendéz-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 

  • Meziadi C, Richard MS, Derquennes A, Thareau V, Blanchet S, Gratias A, Pflieger S, Geffroy V (2016) Development of molecular markers linked to disease resistance genes in common bean based on whole genome sequence. Plant Sci 242:351–357

    Article  CAS  PubMed  Google Scholar 

  • Miklas PN, Delorme R, Stone V, Daly MJ, Stavely JR, Steadman JR, Bassett MJ (2000) Bacterial, fungal, and viral disease resistance loci mapped in a recombinant inbred common bean population (‘Dorado’/XAN 176). J Am Soc Hortic Sci 125:476–481

    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, Kelly JD, Beebe SE, Blair MW (2006) Common bean breeding for resistance against biotic and abiotic stresses: from classical to MAS breeding. Euphytica 147:105–131

    Article  CAS  Google Scholar 

  • Morgulis A, Coulouris G, Raytselis Y, Madden TL, Agarwala R, Schaffer AA (2008) Database indexing for production MegaBLAST searches. Bioinformatics 24:1757–1764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pastor-Corrales MA (2005) Inheritance of resistance in PI 260418 an Andean bean resistant to most races of the bean rust pathogen. Ann Rep Bean Improv Coop 48:134–135

    Google Scholar 

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

    Google Scholar 

  • Pastor-Corrales MA, Aime MC (2004) Differential cultivars and molecular markers segregate isolates of Uromyces appendiculatus into two distinct groups that correspond to the gene pools of their common bean hosts. Phytopathology 94(6):82

    Google Scholar 

  • Pastor-Corrales MA, Erazo OA, Estrada EI, Singh SP (1994) Inheritance of anthracnose resistance in common bean accession G 2333. Plant Dis 78:959–962

    Article  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 

  • Pastor-Corrales MA, Shin SH, Wolf J (2012) Exceptional rust resistance in Mesoamerican common bean accession PI 310762. Ann Rep Bean Improv Coop 55:147–148

    Google Scholar 

  • Richard MMS, Pflieger S, Sevignac M, Thareau V, Blanchet S, Li Y, Jackson SA, Geffroy V (2014) Fine mapping of Co-x, an anthracnose resistance gene to a highly virulent strain of Colletotrichum lindemuthianum in common bean. Theor Appl Genet 127:1653–1666

    Article  CAS  PubMed  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 

  • Schmutz J, Mcclean PE, Mamidi S, Wu GA, Cannon SB, Grimwood J, Jenkins J, Shu S, Song Q, Chavarro C, Torres-Torres M, Geffroy V, Moghaddam SM, Gao D, Abernathy B, Barry K, Blair M, Brick MA, Chovatia M, Gepts P, Goodstein DM, Gonzales M, Hellsten U, Hyten DH, Jia G, Kelly JD, Kudrna D, Lee R, Richard MMS, Miklas PN, Osorno JM, Rodrigues J, Thareau V, Urrea CA, Wang M, Yu Y, Zhang M, Wing RA, Cregan PC, Rokhsar DS, Jackson SA (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46:707–713

    Article  CAS  PubMed  Google Scholar 

  • Schoonhoven A, Pastor-Corrales MA (1987) Standard system for the evaluation of bean germplasm. Centro Internacional de Agricultura Tropical (CIAT). Cali, Colombia

    Google Scholar 

  • Schwartz HF, Pastor-Corrales MA (1989) Bean production problems in the tropics. CIAT, Cali, Colombia, p 654

    Google Scholar 

  • Schwartz HF, Pastor-Corrales MA, Singh SP (1982) New sources of resistance to anthracnose and angular leaf spot of beans (Phaseolus vulgaris L.). Euphytica 31:741–754

    Article  Google Scholar 

  • Shin S-H, Song Q, Cregan PB, Pastor-Corrales MA (2014) SSR DNA markers linked with broad-spectrum rust resistance in common bean discovered by Bulk Segregant Analysis using a large set of SNP markers. Ann Rep Bean Improv Coop 57:187–188

    Google Scholar 

  • Singh SP (1999) Production and utilization. In: Singh SP (ed) Common bean improvement in the 21st century. Kluwer Academic Publishers, Dordrecht, pp 133–165

    Chapter  Google Scholar 

  • Song QJ, Jia G, Zhu Y, Grant D, Nelson RT, Hwang E-Y, Hyten DL, Cregan PB (2010) Abundance of SSR motifs and development of candidate polymorphic SSR markers (BARCSOYSSR_1.0) in soybean. Crop Sci 50:1950–1960

    Article  CAS  Google Scholar 

  • Song Q, Jia G, Hyten DL, Jenkins J, Hwang E-Y, Schroeder S, Osorno JM, Schmutz J, Jackson SA, McClean PE, Cregan PB (2015) SNP assay development for linkage map construction, anchoring whole genome sequence and other genetic and genomic applications in common bean. G3 5:2285–2290

    Article  PubMed  PubMed Central  Google Scholar 

  • Sousa LL, Cruz AS, Vidigal Filho PS, Vallejo VA, Kelly JD, Gonçalves-Vidigal MC (2014) Genetic mapping of the resistance allele Co-5 2 to Colletotrichum lindemuthianum in the common bean MSU 7-1 line. Aust J Crop Sci 8:317–323

    Google Scholar 

  • Sousa LL, Gonçalves AO, Gonçalves-Vidigal MC, Lacanallo GF, Fernandez AC, Awale H, Kelly JD (2015) Genetic characterization and mapping of anthracnose resistance of common bean landrace cultivar Corinthiano. Crop Sci 55:1–11

    Article  Google Scholar 

  • Souza TLPO, Alzate-Marin AL, Dessaune SN, Nunes ES, Queiroz VT, Moreira MA, Barros EG (2007) Inheritance study and validation of SCAR molecular marker for rust resistance in common bean. Crop Breed Appl Biotech 7:11–15

    Article  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 

  • Stavely JR (1984) Genetics of resistance to Uromyces phaseoli in a Phaseolus vulgaris line resistant to most races of the pathogen. Phytopathology 74:339–344

    Article  Google Scholar 

  • Stavely JR (1990) Genetics of rust resistance in Phaseolus vulgaris plant introduction PI 181996. Phytopathology 80:1056

    Google Scholar 

  • Stavely JR, Pastor-Corrales MA (1989) Rust. In: Schwartz HF, Pastor-Corrales MA (eds) Bean production problems in the tropics. CIAT, Cali, Colombia, pp 159–194

    Google Scholar 

  • Stavely JR, Freytag GF, Steadman JR, Schwartz HF (1983) The 1983 bean rust workshop. Ann Rep Bean Improv Coop 26:4–6

    Google Scholar 

  • Stavely JR, Kelly JD, Grafton KF (1994) BelMiDak-rust-resistant navy dry beans germplasm families. HortScience 29:709–711

    Google Scholar 

  • Steadman JR, Pastor-Corrales MA, Beaver JS (2002) An overview of the 3rd Bean Rust and 2nd Bean Common Bacterial Blight International Workshops, March 4–8, 2002, Pietermaritzburg, South Africa. Ann. Rep. Bean Improv. Coop. 45: 120–124

    Google Scholar 

  • Thiel T, Michalek W, Varshney RK, Graner A (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet 106:411–422

    Article  CAS  Google Scholar 

  • Trabanco N, Campa A, Ferreira JJ (2015) Identification of a new chromosomal region involved in the genetic control of resistance to anthracnose in common bean. Plant genome 8:1–11

    Article  Google Scholar 

  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40(15):e115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vallejo VD, Kelly JD (2009) New insights into the anthracnose resistance of common bean landrace G 2333. Open Hort J 2:29–33

    Article  CAS  Google Scholar 

  • Van Ooijen JW (2006) JoinMap® 4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen

    Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78

    Article  CAS  PubMed  Google Scholar 

  • Webster DMN, Ainsworth PM (1988) Inheritance and stability of a small pustule reaction of snap beans to Uromyces appendiculatus. J Am Soc Hortic Sci 113:938–940

    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 oligogenic anthracnose resistance in the common bean cultivar, G2333. Theor Appl Genet 96:87–94

    Article  CAS  Google Scholar 

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Acknowledgements

This research was financially supported by the National Council for Scientific and Technological Development (CNPq) and the Coordination for the Improvement of Higher Education Personnel (CAPES). This work was also supported, in part, by funding from the Norman Borlaug Commemorative Research Initiative of the US Agency for International Development, project number 0210-22310-004-96R and by the US Department of Agriculture, Agricultural Research Services Project Number 8042-22000-286-00D (Pastor-Corrales). The contents of this publication do not necessarily reflect the views or policies of the US Department of Agriculture, nor does mention of trade names, commercial products, or organizations imply endorsement by the US Government.

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Authors and Affiliations

  1. Departamento de Agronomia, Universidade Estadual de Maringá, Av. Colombo, 5790, Maringá-PR, 87020-900, Brazil

    Giseli Valentini, Maria Celeste Gonçalves-Vidigal & Sandra Aparecida de Lima Castro

  2. Soybean Genomics Improvement Laboratory, USDA-ARS, BARC-West, Beltsville, MD, 20705, USA

    Oscar P. Hurtado-Gonzales, Perry B. Cregan, Qijian Song & Marcial A. Pastor-Corrales

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  1. Giseli Valentini
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  5. Perry B. Cregan
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  6. Qijian Song
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  7. Marcial A. Pastor-Corrales
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Correspondence to Marcial A. Pastor-Corrales.

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The authors declare that they have no conflict of interest.

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The experiments shown in the manuscripts submitted for publication comply with the current laws of the country in which they were performed.

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Communicated by Heiko C. Becker.

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Valentini, G., Gonçalves-Vidigal, M.C., Hurtado-Gonzales, O.P. et al. High-resolution mapping reveals linkage between genes in common bean cultivar Ouro Negro conferring resistance to the rust, anthracnose, and angular leaf spot diseases. Theor Appl Genet 130, 1705–1722 (2017). https://doi.org/10.1007/s00122-017-2920-6

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  • DOI: https://doi.org/10.1007/s00122-017-2920-6

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