Abstract
Halo blight, caused by Pseudomonas syringae pv. phaseolicola (Burkn.) Downs (Psp), is an important disease in common bean (Phaseolus vulgaris L.). This study investigated the genetic control of the resistance to two local isolates of Psp (ITA-812 and ITA-684) in a recombinant inbred line (RIL) population derived from the cross between the bean genotypes Xana and Cornell 49242. The cultivar Cornell 49242 exhibited moderate resistance to these isolates, whereas cultivar Xana was susceptible. The RIL population showed a continuous variation in response to the two isolates. Analysis revealed four significant quantitative trait loci (QTLs): Psp4812XC and Psp6.1812XC located on linkage groups Pv04 and Pv06 (for the response to isolate ITA-812), and Psp6.1684XC and Psp6.2684XC located on Pv06 (for the response to isolate ITA-684). The QTLs Psp6.1812XC and Psp6.1684XC were located in the same genetic region (Psp6.1), close to the Psp6.2 region in which the QTL Psp6.2684XC was mapped. A genetic dissection was undertaken to verify the consistency of these three QTLs located on the end of Pv06. Four sets of RILs were established according to the genotypes (Xana and Cornell 49242) of the underlying markers for the regions Psp6.1 and Psp6.2. Re-evaluation of these sets of lines revealed significant differences relative only to isolate ITA-684. The set of lines with the Cornell genotype in both regions was significantly more resistant than the other three sets of lines. This suggested that both regions were necessary to detect a significant effect in the response to isolate ITA-684. In the physical positions corresponding to these two genetic regions, in silico analysis revealed 16 candidate genes (putative orthologous genes) that carried sequences homologous to the resistance genes RPM1, FLS2, RPG1/RPG1-B, and Pto—all of which confer resistance to P. syringae in different species. The results confirm that, apart from the major genes implicated in resistance to Psp, specific bean genotypes exhibit a quantitative mode of inheritance of resistance to Psp.
Similar content being viewed by others
References
Aggour AR, Coyne DP, Vidaver AK (1989) Comparison of leaf and pod disease reactions of beans (Phaseolus vulgaris L.) inoculated by different methods with strains of Xanthomonas campestris pv. phaseoli (Smith) dye. Euphytica 43:143–152
Ariyarathne HM, Coyne DP, Jung G, Skroch PW, Vidaver AK, Steadman JR, Miklas PN, Bassett MJ (1999) Molecular mapping of disease resistance genes for halo blight, common bacterial blight, and bean common mosaic virus in a segregating population of common bean. J Am Soc Hortic Sci 124:654–662
Arnold DL, Lovell HC, Jackson RW, Mansfield JW (2011) Pseudomonas syringae pv. phaseolicola: from ‘has bean’ to supermodel. Mol Plant Pathol 12:617–627
Ashfield T, Keen NT, Buzzell RI, Innes RW (1995) Soybean resistance genes specific for different Pseudomonas syringae avirulence genes are allelic, or closely linked, at the RPG1 locus. Genetics 141:1597–1604
Axtell MJ, Staskawicz BJ (2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112:369–377
Bernardo R (2008) Molecular markers and selection for complex traits in plants: learning from the last 20 years. Crop Sci 48:1649–1664
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
Blair MW, Muñoz C, Buendía HF, Flower J, Bueno JM, Cardona C (2010) Genetic mapping of microsatellite markers around the arcelin bruchid resistance locus in common bean. Theor Appl Genet 121:393–402
Bozkurt IA, Soylu S (2011) Determination of responses of different bean cultivars against races of Pseudomonas syringae pv phaseolicola, causal agent of halo blight of bean. Euphytica 179:417–425
Bradbury JF (1986) Guide to plant pathogenic bacteria. CAB International, Farnham Royal, Great Britain
Campa A, Pérez-Vega E, Pascual A, Ferreira JJ (2010) Genetic analysis and molecular mapping of quantitative trait loci in common bean against Pythium ultimum. Phytopathology 100:1315–1320
Chandra S, Martin GB, Low PS (1996) The Pto kinase mediates a signaling pathway leading to the oxidative burst in tomato. Plant Biol 93:13393–13397
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
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971
Collard BCY, Jahufer MZZ, Brouwer JB, Pang ECK (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: the basic concepts. Euphytica 142:169–196
Córdoba JM, Chavarro C, Rojas F, Muñoz C, Blair MW (2010a) Identification and mapping of simple sequence repeat markers from common bean (Phaseolus vulgaris L.) bacterial artificial chromosome end sequences for genome characterization and genetic-physical map integration. Plant Genome 3:154–165
Córdoba JM, Chavarro C, Schlueter JA, Jackson SA, Blair MW (2010b) Integration of physical and genetic maps of common bean through BAC-derived microsatellite markers. BMC Genomics 11:436
Croft KPC, Voisey CR, Slusarenko AJ (1990) Mechanism of hypersensitive cell collapse: correlation of increased lipoxygenase activity with membrane damage in leaves of Phaseolus vulgaris (L) inoculated with an avirulent race of Pseudomonas syringae pv. phaseolicola. Physiol Mol Plant Pathol 36:49–62
Day B, Dahlbeck D, Staskawicz BJ (2006) NDR1 interaction with RIN4 mediates the differential activation of multiple disease resistance pathways in Arabidopsis. Plant Cell 18:2782–2791
Flor HH (1955) Host parasite interaction in flax rust—its genetics and other implications. Phytopathology 45:680–685
Forsyth A, Mansfield JW, Grabov N, Torres M, Sinapidou E, Grant MR (2010) Genetic dissection of basal resistance to Pseudomonas syringae pv. phaseolicola in accessions of Arabidopsis. Mol Plant Microbe Interact 23:1545–1552
Fourie D, Miklas PN, Ariyaranthe H (2004) Genes conditioning halo blight resistance to races 1, 7 and 9 occur in a tight cluster. Annu Rep Bean Improv Coop 47:103–104
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
Gaitán-Solís E, Duque MC, Edwards KJ, Tohme J (2002) Microsatellite in common bean (Phaseolus vulgaris): isolation, characterization, and cross-species amplification in Phaseolus ssp. Crop Sci 42:2128–2136
García-Ponce B, Rocha-Sosa M (2000) The octadecanoid pathway is required for pathogen-induced multi-functional acetyl-CoA carboxylase accumulation in common bean (Phaseolus vulgaris L.). Plant Sci 157:181–190
Goodstein DM, Shengqiang S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40(D1):D1178–D1186
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 × Jalo EEP558. Genet Mol Res 6:691–706
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 Breed 25:25–45
Joehanes R, Nelson JC (2008) QGene 4.0, an extensible Java QTL-analysis platform. Bioinformatics 24:2788–2789
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
Mackey D, Holt BF, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743–754
Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–1436
McConnell M, Mamidi S, Lee R, Chikara S, Rossi M, Papa R, McClean P (2010) Syntenic relationships among legumes revealed using a gene-based linkage map of common bean (Phaseolus vulgaris L.). Theor Appl Genet 121:1103–1116
Miklas PN, Porch TG (2010) Guidelines for common bean QTL nomenclature. Annu Rep Bean Improv Coop 53:202–204
Miklas PN, Fourie D, Wagner J, Larsen RC, Mienie CMS (2009) Tagging and mapping Pse-1 gene for resistance to halo blight in common bean host differential cultivar UI-3. Crop Sci 49:41–48
Miklas PN, Fourie D, Trapp J, Larsen RC, Chavarro C, Blair MW, Gepts P (2011) Genetic characterization and molecular mapping Pse-2 gene for resistance to halo blight in common bean. Crop Sci 51:2439–2448
Moghaddam SM, Song Q, Mamidi S, Schmutz J, Lee R, Cregan P, Osorno JM, McClean PE (2013) Developing market class specific InDel markers from next generation sequence data in Phaseolus vulgaris L. Front Plant Sci 4:251
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
Pérez-Vega E, Trabanco N, Campa A, Ferreira JJ (2013) Genetic mapping of two genes conferring resistance to powdery mildew in common bean (Phaseolus vulgaris L.). Theor Appl Genet 126:1503–1512
Rico A, Lopez R, Asenio C, Aizpún MT, Asensio-S.-Manzanera MC, Murillo J (2003) Nontoxigenic strains of Pseudomonas syringae pv. phaseolicola are a main cause of halo blight of beans in Spain and escape current detection methods. Phytopathology 93:1553–1559
Saettler AW, Ishimuru C, Mohan SK, Franc GD (2005) Halo blight. In: Schwartz HF, Steadman JR, Hall R, Forster RL (eds) Compendium of bean diseases, 2nd edn. APS Press, St Paul, pp 36–37
Selote D, Kachroo A (2010) RPG1-B-derived resistance to AvrB-expressing Pseudomonas syringae requires RIN4-like proteins in soybean. Plant Physiol 153:1199–1211
Shi C, Yu K, Xie W, Perry G, Navabi A, Pauls KP, Miklas PN, Fourie D (2012) Development of candidate gene markers associated to common bacterial blight resistance in common bean. Theor Appl Genet 125(7):1525–1537
Taylor JD, Teverson DM, Allen DJ, Pastor-Corrales MA (1996a) Identification and origin of races of Pseudomonas syringae pv. phaseolicola from Africa and other bean growing areas. Plant Pathol 45:469–478
Taylor JD, Teverson DM, Davis JHC (1996b) Sources of resistance to Pseudomonas syringae pv. phaseolicola races in Phaseolus vulgaris. Plant Pathol 45:479–485
Voisey CR, Slusarenko AJ (1989) Chitinase mRNA and enzyme activity in Phaseolus vulgaris (L.) increase more rapidly in response to avirulent than to virulent cells of Pseudomonas syringae pv. phaseolicola. Physiol Mol Plant Pathol 35:403–412
Walker JC, Patel PN (1964) Inheritance of resistance to halo blight in bean. Phytopathology 54:952–954
Yaish MWF, Sosa D, Vences FJ, Vaquero F (2006) Genetic mapping of quantitative resistance to race 5 of Pseudomonas syringae pv. phaseolicola in common bean. Euphytica 179:417–425
Acknowledgments
This work was supported by grant RTA2011-0076-CO2-01 from INIA-Ministerio de Economía y Competitividad, Spain and European Regional Development Fund. Noemí Trabanco was the recipient of a salary fellowship from Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA, Spain). We thank Marcos Bueno for technical assistance in the molecular marker analysis.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Trabanco, N., Asensio-Manzanera, M.C., Pérez-Vega, E. et al. Identification of quantitative trait loci involved in the response of common bean to Pseudomonas syringae pv. phaseolicola . Mol Breeding 33, 577–588 (2014). https://doi.org/10.1007/s11032-013-9974-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11032-013-9974-1