Abstract
Powdery mildew (PM) is a serious disease in many legume species, including the common bean (Phaseolus vulgaris L.). This study investigated the genetic control behind resistance reaction to PM in the bean genotype, Cornell 49242. The results revealed evidence supporting a qualitative mode of inheritance for resistance and the involvement of two independent genes in the resistance reaction. The location of these resistance genes was investigated in a linkage genetic map developed for the XC RIL population. Contingency tests revealed significant associations for 28 loci out of a total of 329 mapped loci. Fifteen were isolated or formed groups with less than two loci. The thirteen remaining loci were located at three regions in linkage groups Pv04, Pv09, and Pv11. The involvement of Pv09 was discarded due to the observed segregation in the subpopulation obtained from the Xana genotype for the loci located in this region. In contrast, the two subpopulations obtained from the Xana genotype for the BM161 locus, linked to the Co-3/9 anthracnose resistance gene (Pv04), and from the Xana genotype for the SCAReoli locus, linked to the Co-2 anthracnose resistance gene (Pv11), exhibited monogenic segregations, suggesting that both regions were involved in the genetic control of resistance. A genetic dissection was carried out to verify the involvement of both regions in the reaction to PM. Two resistant recombinant lines were selected, according to their genotypes, for the block of loci included in the Co-2 and Co-3/9 regions, and they were crossed with the susceptible parent, Xana. Linkage analysis in the respective F2 populations supported the hypothesis that a dominant gene (Pm1) was located in the linkage group Pv11 and another gene (Pm2) was located in the linkage group Pv04. This is the first report showing the localization of resistance genes against powdery mildew in Phaseolus vulgaris and the results offer the opportunity to increase the efficiency of breeding programs by means of marker-assisted selection.

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References
Ameline-Torregrosa C, Cazaux M, Danesh D, Chardon F, Cannon SB, Esquerré-Tugayé M-T, Dumas B, Young ND, Samac DA, Huguet T, Jacquet C (2008a) Genetic dissection of resistance to anthracnose and powdery mildew in Medicago truncatula. MPMI 21:61–68
Ameline-Torregrosa C, Wang BB, O’Bleness MS, Deshpande S, Zhu H, Roe B, Young ND, Cannon SB (2008b) Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula. Plant Physiol 146:5–21
Awale HE, Ismail SM, Vallejo VA, Kelly JD (2008) SQ4 SCAR marker linked to the Co-2 gene on B11 appears to be linked to the Ur-11 gene. Ann Rep Bean Improv Coop 51:172–173
Bett KE, Michaels TE (1995) A two-gene model for powdery mildew resistance in common bean. Ann Rep Bean Improv Coop 38:145–146
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
Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, Van Daelen R, Van der Lee T, Diergaarde P, Groenendijk J, Töpsch S, Vos P, Salamini F, Schulze-Lefert P (1997) The barley Mlo Gene: a novel control element of plant pathogen resistance. Cell 88:695–705
Campa A, Giraldez R, Ferreira JJ (2009) Genetic dissection of the resistance to nine different anthracnose races in the common bean differential cultivars MDRK and TU. Theor Appl Genet 119:1–11
Chen NWG, Sévignac M, Thareau V, Magdelenat G, David P, Ashfield T, Innes RW, Geffroy V (2010) Specific resistances against Pseudomonas syringae effectors AvrB and AvrRpm1 have evolved differently in common bean (Phaseolus vulgaris), soybean (Glycine max), and Arabidopsis thaliana. New Phytol 187:941–956
Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-Microbe Interactions: shaping the evolution of the plant immune response. Cell 124:803–814
Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411(41):826–833
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
David P, Chen NWG, Pedrosa-Harand A, Thareau V, Sévignac M, Cannon SB, Debouck D, Langin T, Geffroy V (2009) A nomadic subtelomeric disease resistance gene cluster in common bean. Plant Physiol 151:1048–1065
DeYoung B, Innes RW (2006) Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol 7:1243–1249
Dundas B (1936) Inheritance of resistance to powdery mildew in beans. Hilgardia 10:241–253
Ferreira V, Patto MA, Corte HR (1999) Genetic control of common bean (Phaseolus vulgaris) resistance to powdery mildew (Erysiphe polygoni). Genet Mol Biol 22:233–236
Ferreira JJ, Campa A, Kelly JD (2012) Organization of genes conferring resistance to anthracnose in common bean. In: genomics applications in plant breeding, R Tuberosa and R Varshney (eds) Wiley-Blackwell Pubs (in press)
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
Gaitán-Solis 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
Geffroy V, Creusot F, Falquet J, Sévignac M, Adam-Blondon A-FH, Bannerot H, Gepts P, 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
Geffroy V, Macadre C, David P, Pedrosa-Harand A, Sevignac 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
Grisi MCM, Blair MW, Gepts P, Brondani C, Pereira PAA, Brondani RPV (2007) Genetic mapping of a new set of microsatellite markers in a reference common bean (Phaseolus vulgaris L.) population BAT93 x Jalo EEP558. Genet Mol Res 6(3):691–706
Hanai LR, Santini L, Camargo LEA, Pelegrinelli MH, Gepts P, Mui S, Carneiro ML (2010) Extension of the core map of common bean with EST-SSR, RGA, AFLP and putative functional markers. Mol Breeding 25:25–45
Jun T-H, Rouf Mian MA, Kang S-T, Michel AP (2012) Genetic mapping of the powdery mildew resistance gene in soybean PI 567301B. Theor Appl Genet 125(6):1159–1168
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
López CE, Acosta IF, Jara C, Pedraza F, Gaitán-Solís 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
Martins WS, Soares DC, de Souza Fabricio, Neves K, Bertioli DJ (2009) WebSat: a web software for microsatellite marker development. Bioinformation 3(6):282–283
McDowell JM, Woffenden BJ (2003) Plant disease resistance genes: recent insights and potential applications. Trend in Biotech 21:178–183
Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-Wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834
Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8:1113–1130
Miklas PN, Pastor-Corrales MA, Jung G, Coyne DP, Kelly JD, McClean PE, Gepts P (2002) Comprehensive linkage map of bean rust resistance genes. Annu Rep Bean Improv Coop 45:125–129
Mutlu N, Miklas PN, Coyne DP (2006) Resistance gene analog polymorphism (RGAP) markers co-localize with disease resistance genes and QTL in common bean. Mol Breeding 17:127–135
Pedrosa-Harand A, Porch T, Gepts P (2008) Standard nomenclature for common bean chromosomes and linkage groups. Annu Rep Bean Improv Coop 51:106–107
Pérez-Vega E, Pañeda A, Rodríguez-Suárez C, Campa A, Giraldez R, Ferreira JJ (2010) Mapping of QTLs for morpho-agronomic and seed quality traits in a RIL population of common bean (Phaseolus vulgaris L.). Theor Appl Genet 120:1367–1380
Rodríguez-Suárez C, Méndez-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
Rodríguez-Suárez C, Ferreira JJ, Campa, Pañeda A, Giraldez R (2008) Molecular mapping and intra-cluster recombination between anthracnose race-specific resistance genes in the common bean differential cultivars Mexico 222 and Widusa. Theor Appl Genet 116:807–814
Singh VK, Singh AK, Chand R, Singh BD (2012) Genome wide analysis of disease resistance mlo gene family in sorghum [Sorghum bicolor (l.) moench]. J Plant Genomic 2(1):18–27
Trabanco N, Pérez-Vega E, Campa A, Rubiales D, Ferreira JJ (2012) Genetic resistance to powdery mildew in common bean. Euphytica 186:875–882
Acknowledgments
This work was supported by grants RTA2009-093 and RTA2011-0076-CO2-01 from INIA-Ministerio de Economía y Competitividad, Spain. Noemí Trabanco was the recipient of a salary fellowship from Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA, Spain).
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Communicated by H. T. Nguyen.
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Table 1 ESM. Results of contingency tests carried out among the loci included in the genetic map and the response to powdery mildew in the XC RIL population. Loci are listed in the same order as in the genetic linkage map. Significant contingency tests are indicated with green colour. Added loci in the present study are identified with blue words.
Table 2 ESM. List of microsatellite markers designed from the accessions EU931620.1, FJ817289, FJ817291.1 and FJ817290 deposited in the Genebank data base (David et al. 2009). Markers indicated using red word were analyzed for polymorphism between the two parents. Mapped microsatellites markers are indicated with yellow colour.
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Pérez-Vega, E., Trabanco, N., Campa, A. et al. Genetic mapping of two genes conferring resistance to powdery mildew in common bean (Phaseolus vulgaris L.). Theor Appl Genet 126, 1503–1512 (2013). https://doi.org/10.1007/s00122-013-2068-y
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DOI: https://doi.org/10.1007/s00122-013-2068-y


