Fine-mapping of a major QTL controlling angular leaf spot resistance in common bean (Phaseolus vulgaris L.)

Theoretical and Applied Genetics

Volumn 128, Issue 5, 2015, Pages 813-826

  Keller, Beat ^a   Manzanares, Chloe ^a   Jara, Carlos ^b   Lobaton, Juan David ^b   Studer, Bruno ^a   Raatz, Bodo ^b  

^a ETH ZURICH   (Switzerland)

^b INTERNATIONAL CENTER FOR TROPICAL AGRICULTURE CIAT   (Colombia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; DEVELOPING COUNTRIES; GENES; PLANTS (BOTANY); PROTEINS;

ESSENTIAL PROTEINS; LOW INPUT AGRICULTURE; MAPPING POPULATIONS; MARKER-ASSISTED SELECTION; PHASEOLUS VULGARIS; QUANTITATIVE TRAIT LOCUS; RESISTANT CULTIVARS; SINGLE-NUCLEOTIDE POLYMORPHISM MARKERS;

MAPPING;

GENETIC MARKER; MICROSATELLITE DNA;

ASCOMYCETES; CHROMOSOME MAP; DISEASE RESISTANCE; GENETIC LINKAGE; GENETIC MARKER; GENETICS; GENOTYPE; MICROBIOLOGY; PHASEOLUS; PHENOTYPE; PLANT DISEASE; PLANT GENE; QUANTITATIVE TRAIT LOCUS;

ASCOMYCOTA; CHROMOSOME MAPPING; DISEASE RESISTANCE; GENES, PLANT; GENETIC LINKAGE; GENETIC MARKERS; GENOTYPE; MICROSATELLITE REPEATS; PHASEOLUS; PHENOTYPE; PLANT DISEASES; QUANTITATIVE TRAIT LOCI;

EID: 84934297800     PISSN: 00405752     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00122-015-2472-6     Document Type: Article

References (97)

1. Abadio AKR, Lima SS, Santana MF, Salomao TMF, Sartorato A, Mizubuti ESG, Araujo EF, de Queiroz MV (2012) Genetic diversity analysis of isolates of the fungal bean pathogen Pseudocercospora griseola from central and southern Brazil. Genet Mol Res 11(2):1272–1279. doi:10.4238/2012.May.14.1
2. Allorent D, Savary S (2005) Epidemiological characteristics of angular leaf spot of bean: a systems analysis. Eur J Plant Pathol 113(4):329–341
3. Bassanezi RB, Amorim L, Filho AB, Berger RD (2002) Gas exchange and emission of chlorophyll fluorescence during the monocycle of rust, angular leaf spot and anthracnose on bean leaves as a function of their trophic characteristics. J Phytopathol 150(1):37–47
4. Blair MW, Cortes AJ, Penmetsa RV, Farmer A, Carrasquilla-Garcia N, Cook DR (2013) A high-throughput SNP marker system for parental polymorphism screening, and diversity analysis in common bean (Phaseolus vulgaris L.). Theor Appl Genet 126(2):535–548. doi:10.1007/s00122-012-1999-z
5. Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19(7):889–890. doi:10.1093/bioinformatics/btg112
6. Broughton WJ, Hernandez G, Blair M, Beebe S, Gepts P, Vanderleyden J (2003) Beans (Phaseolus spp.)—model food legumes. Plant Soil 252(1):55–128. doi:10.1023/a:1024146710611
7. Caixeta ET, Borem A, Fagundes SD, Niestche S, de Barros EG, Moreira MA (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(3):297–303
8. Caixeta ET, Borem A, Alzate-Marin AL, Fagundes SD, Silva M, de Barros EG, Moreira MA (2005) Allelic relationships for genes that confer resistance to angular leaf spot in common bean. Euphytica 145(3):237–245. doi:10.1007/s10681-005-1258-3
9. 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. Proc Natl Acad Sci. doi:10.1073/pnas.1016981108
10. Carvalho GA, Paula Junior TJ, Alzate-Marin AL, Nietsche S, Barros EG, Moreira MA (1998) Inheritance of resistance of the Andean bean line AND-277 to race 63-23 of Phaeoisariopsis griseola and identification of a RAPD marker linked to the resistance gene. Fitopatol Bras 23(4):482–485
11. Castellanos G, Jara C, Mosquera G (2011) Manejo del hongo en el laboratorio. Phaeoisariopsis griseola, vol 6. Centro Internacional de Agricultura Tropical (CIAT), Cali-Palmira
12. Cook DE, Lee TG, Guo X, Melito S, Wang K, Bayless AM, Wang J, Hughes TJ, Willis DK, Clemente TE, Diers BW, Jiang J, Hudson ME, Bent AF (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338(6111):1206–1209. doi:10.1126/science.1228746
13. Corrêa R, Good-God P, Oliveira M, Niestche S, Moreira M, de Barros E (2001) Herança da resistência á manchaangular do feijoeiro e identificaçao de marcadores moleculares flanqueando o loco de resistência. Fitopatol Bras 26:7–32
14. 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
15. Cunha C, Hintz T, Griffiths P (2004) Genetic diversity of snap bean cultivars determined using randomly amplified polymorphic DNA (RAPD) markers. HortScience 39(3):481–484
16. David P, Chen NWG, Pedrosa-Harand A, Thareau V, Sevignac M, Cannon SB, Debouck D, Langin T, Geffroy V (2009) A nomadic subtelomeric disease resistance gene cluster in common bean. Plant Physiol 151(3):1048–1065. doi:10.1104/pp.109.142109
17. Debouck DG, Toro O, Paredes OM, Johnson WC, Gepts P (1993) Genetic diversity and ecological distribution of Phaseolus vulgaris (Fabaceae) in northwestern South America. Econ Bot 47(4):408–423. doi:10.1007/bf02907356
18. de Jesus WC, do Vale FX, Coelho RR, Hau B, Zambolim L, Costa LC, Filho AB (2001) Effects of angular leaf spot and rust on yield loss of phaseolus vulgaris. Phytopathology 91(11):1045–1053
19. Dong J, Xiao F, Fan F, Gu L, Cang H, Martin GB, Chai J (2009) Crystal structure of the complex between pseudomonas effector AvrPtoB and the tomato Pto kinase reveals both a shared and a unique interface compared with AvrPto-Pto. Plant Cell 21(6):1846–1859. doi:10.1105/tpc.109.066878
20. Faleiro F, Ragagnin V, Schuster I, Corrêa R, Good-God P, Brommonshenkel S, Moreira M, Barros E (2003) Mapeamento de genes de resistência do feijoeiro à ferrugem, antracnose e mancha-angular usando marcadores RAPD. Fitopatol Bras 28:59–66
21. FAOSTAT (2011) FAO statistic. Food and agriculture organization of the united nations (FAO). http://faostat.fao.org/. Accessed 16 May 2013
22. Ferreira da Silva G, Bosco dos Santos J, Patto Ramalho MA (2003) Identification of SSR and RAPD markers linked to a resistance allele for angular leaf spot in the common bean (Phaseolus vulgaris) line ESAL 550. Genetics and Molecular Biology 26(4):459–463
23. Ferreira CF, Borem A, Carvalho GA, Nietsche S, Paula TJ, Barros EG, Moreira MA (2000) Inheritance of angular leaf spot resistance in common bean and identification of a RAPD marker linked to a resistance gene. Crop Sci 40(4):1130–1133
24. Gepts P (1998) Origin and evolution of common bean: past events and recent trends. HortScience 33(7):1124–1130
25. Gepts P, Bliss FA (1985) F1 hybrid weakness in the common bean; differential geographic origin suggests two gene pools in cultivated bean germplasm. J Hered 76:447–450
26. Gepts P, Aragao FJL, de Barros E, Blair MW, Brondani R, Broughton W, Galasso I, Hernandez G, Kami J, Lariguet P, McClean P, Melotto M, Miklas P, Pauls P, Pedrosa-Harand A, Porch T, Sanchez 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, vol 1. Plant Genetics and Genomics-Crops and Models, Springer, New York, pp 113–143
27. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227. doi:10.1146/annurev.phyto.43.040204.135923
28. Goncalves-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(5):893–903. doi:10.1007/s00122-010-1496-1
29. Goodstein DM, Shu 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. doi:10.1093/nar/gkr944
30. Gundry CN, Vandersteen JG, Reed GH, Pryor RJ, Chen J, Wittwer CT (2003) Amplicon melting analysis with labeled primers: A closed-tube method for differentiating homozygotes and heterozygotes. Clin Chem 49(3):396–406. doi:10.1373/49.3.396
31. Guzman P, Gilbertson RL, Nodari R, Johnson WC, Temple SR, Mandala D, Mkandawire ABC, Gepts P (1995) Characterization of variability in the fungus Phaeoisariopsis griseola suggests coevolution with the common bean (Phaseolus vulgaris). Phytopathology 85(5):600–607. doi:10.1094/Phyto-85-600
32. Hemalatha S, Platel K, Srinivasan K (2007) Zinc and iron contents and their bioaccessibility in cereals and pulses consumed in India. Food Chem 102(4):1328–1336. doi:10.1016/j.foodchem.2006.07.015
33. Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23(10):1289–1291. doi:10.1093/bioinformatics/btm091
34. Lee B, Shin G (2009) CleanEST: a database of cleansed EST libraries. Nucleic Acids Res 37:D686–D689. doi:10.1093/nar/gkn648
35. Lehmensiek A, Sutherland MW, McNamara RB (2008) The use of high resolution melting (HRM) to map single nucleotide polymorphism markers linked to a covered smut resistance gene in barley. Theor Appl Genet 117(5):721–728. doi:10.1007/s00122-008-0813-4
36. Loh YT, Zhou JM, Martin GB (1998) The myristylation motif of Pto is not required for disease resistance. Mol Plant Microbe Interact 11(6):572–576. doi:10.1094/mpmi.1998.11.6.572
37. 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(1):88–95. doi:10.1094/phyto.2003.93.1.88
38. Mahuku GS, Henriquez MA, Munoz J, Buruchara RA (2002) Molecular markers dispute the existence of the Afro-Andean group of the bean angular leaf spot pathogen, Phaeoisariopsis griseola. Phytopathology 92(6):580–589. doi:10.1094/phyto.2002.92.6.580
39. Mahuku GS, Jara C, Cajiao E, Beebe S (2003) Sources of resistance to angular leaf spot (Phaeoisariopsis griseola) in common bean core collection, wild Phaseolus vulgaris and secondary gene pool. Euphytica 130(3):303–313. doi:10.1023/a:1023095531683
40. Mahuku G, Montoya C, Henriquez MA, Jara C, Teran H, Beebe S (2004) Inheritance and characterization of angular leaf spot resistance gene present in common bean accession G 10474 and identification of an AFLP marker linked to the resistance gene. Crop Sci 44(5):1817–1824
41. 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. doi:10.1007/s10681-009-9897-4
42. Mahuku GS, Antonia Henriquez M, 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(1):57–71. doi:10.1007/s11032-010-9461-x
43. Mamidi S, Rossi M, Moghaddam SM, Annam D, Lee R, Papa R, McClean PE (2013) Demographic factors shaped diversity in the two gene pools of wild common bean Phaseolus vulgaris L. Heredity 110(3):267–276. doi:10.1038/hdy.2012.82
44. Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu TY, Earle ED, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262(5138):1432–1436. doi:10.1126/science.7902614
45. Martinez Meyer MR, Rojas A, Santanen A, Stoddard FL (2013) Content of zinc, iron and their absorption inhibitors in Nicaraguan common beans (Phaseolus vulgaris L.). Food Chem 136 (1):87–93
46. 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(1–2):105–131. doi:10.1007/s10681-006-4600-5
47. Mok DWS, Mok MC (1976) A modified Giemsa technique for identifying bean chromosomes. J Hered 67(3):187–188
48. Monda EO, Sanders FE, Hick A (2001) Infection and colonization of bean leaf by Phaeoisariopsis griseola. Plant Pathol 50(1):103–110. doi:10.1046/j.1365-3059.2001.00537.x
49. Montgomery J, Wittwer CT, Palais R, Zhou LM (2007) Simultaneous mutation scanning and genotyping by high-resolution DNA melting analysis. Nat Protoc 2(1):59–66. doi:10.1038/nprot.2007.10
50. Myers J, Davis J (2002) Molecular polygenetics of snap bean. Department of Horticulture, Oregon State University, Corvallis
51. Namayanja A, Buruchara R, Mahuku G, Rubaihayo P, Kimani P, Mayanja S, Eyedu H (2006) Inheritance of resistance to angular leaf spot in common bean and validation of the utility of resistance linked markers for marker assisted selection out side the mapping population. Euphytica 151(3):361–369. doi:10.1007/s10681-006-9158-8
52. NCBI (2013) GenBank. National Center for Biotechnology Information (NCBI). http://www.ncbi.nlm.nih.gov/genbank. Accessed 11 July 2013
53. Nietsche S, Borem A, Carvalho GA, Rocha RC, Paula TJ, de Barros EG, Moreira MA (2000) RAPD and SCAR markers linked to a gene conferring resistance to angular leaf spot in common bean. J Phytopathol-Phytopathol Z 148(2):117–121
54. Oblessuc PR, Baroni RM, Garcia AAF, Chioratto AF, Carbonell SAM, Camargo LEA, Benchimol LL (2012) Mapping of angular leaf spot resistance QTL in common bean (Phaseolus vulgaris L.) under different environments. BMC Genet 13(50):9. doi:10.1186/1471-2156-13-50
55. Oblessuc PR, Perseguini J, Baroni RM, Chiorato AF, Carbonell SAM, Mondego JMC, Vidal RO, Camargo LEA, Benchimol-Reis LL (2013) Increasing the density of markers around a major QTL controlling resistance to angular leaf spot in common bean. Theor Appl Genet 126(10):2451–2465. doi:10.1007/s00122-013-2146-1
56. Oh CS, Martin GB (2011) Effector-triggered immunity mediated by the Pto kinase. Trends Plant Sci 16(3):132–140. doi:10.1016/j.tplants.2010.11.001
57. Park SO, Coyne DP, Bokosi JM, Steadman JR (1999) Molecular markers linked to genes for specific rust resistance and indeterminate growth habit in common bean. Euphytica 105(2):133–141. doi:10.1023/a:1003477714349
58. Park G, Servin JA, Turner GE, Altamirano L, Colot HV, Collopy P, Litvinkova L, Li LD, Jones CA, Diala FG, Dunlap JC, Borkovich KA (2011) Global analysis of serine-threonine protein kinase genes in Neurospora crassa. Eukaryot Cell 10(11):1553–1564. doi:10.1128/ec.05140-11
59. Pastor-Corrales MA, Jara C, Singh SP (1998) Pathogenic variation in, sources of, and breeding for resistance to Phaeoisariopsis griseola causing angular leaf spot in common bean. Euphytica 103(2):161–171. doi:10.1023/a:1018350826591
60. Peleman JD, Wye C, Zethof J, Sorensen AP, Verbakel H, van Oeveren J, Gerats T, van der Voort JR (2005) Quantitative trait locus (QTL) isogenic recombinant analysis: a method for high-resolution mapping of QTL within a single population. Genetics 171(3):1341–1352. doi:10.1534/genetics.105.045963
61. PhaseolusGenes (2013) Bean Breeder’s molecular marker toolbox. UC Davis Bioinformatics Core at University of California, Davis. http://phaseolusgenes.bioinformatics.ucdavis.edu. Accessed 23 May 2013
62. Phytozome.net (2014) Phaseolus vulgaris v1.0. DOE-JGI and USDA-NIFA. http://www.phytozome.net/. Accessed 20 May 2014
63. Queiroz VT, Sousa CS, Costa MR, Sanglad 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. Annu Rep Bean Improv Coop 47:237–238
64. Ramirez M, Graham MA, Blanco-Lopez L, Silvente S, Medrano-Soto A, Blair MW, Hernandez G, Vance CP, Lara M (2005) Sequencing and analysis of common bean ESTs. Building a foundation for functional genomics. Plant Physiol 137(4):1211–1227. doi:10.1104/pp.104.054999
65. Reed GH, Wittwer CT (2004) Sensitivity and specificity of single-nucleotide polymorphism scanning by high-resolution melting analysis. Clin Chem 50(10):1748–1754. doi:10.1373/clinchem.2003.029751
66. Rodriguez-Suarez C, Mendez-Vigo B, Paneda 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(4):713–722. doi:10.1007/s00122-006-0471-3
67. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology, Humana Press, Totowa
68. Salmeron JM, Oldroyd GED, Rommens CMT, Scofield SR, Kim HS, Lavelle DT, Dahlbeck D, Staskawicz BJ (1996) Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86(1):123–133. doi:10.1016/s0092-8674(00)80083-5
69. Sanglard DA, Gomes Ribeiro CA, Pereira Balbi B, Antunes Arruda KM, Gonçalves de Barros E, Alves Moreira M (2013) Characterization of the angular leaf spot resistance gene present in common bean cultivar Ouro Negro. J Agric Sci 5(2):19–23
70. Sartorato A, Nietsche S, Barros EG, Moreira MA (2000) RAPD and SCAR markers linked to resistance gene to angular leaf spot in common beans. Fitopatol Bras 25:637–642
71. Sathe SK (2002) Dry bean protein functionality. Crit Rev Biotechnol 22(2):175–223
72. 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 DL, 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 PB, Rokhsar DS, Jackson SA (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46:707–713
73. Schoonhoven AV, Pastor-Corrales MA (1987) Standard system for the evaluation of bean germplasm. Centro Internacional de Agricultura Tropical, Cali
74. Schwartz HF, Correa VF, Pineda DPA, Otoya MM, Katherman MJ (1981) Dry bean yield losses caused by Ascochyta, angular, and white leaf spots in Colombia. Plant Dis 65:494–496
75. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soeding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7(539):6. doi:10.1038/msb.2011.75
76. Singh SP (2005) Common bean (Phaseolus vulgaris L.). In: Singh RJ, Jauhar PP (eds) Genetic resources, chromosome engineering, and crop improvement: grain legumes, vol 1. CRC Press, USA
77. Singh SP, Terán H, Muñoz CG, Osorno JM (2002) Selection for seed yield in Andean intra-gene pool and Andean×Middle American inter-gene pool populations of common bean. Euphytica 127(3):437–444. doi:10.1023/A:1020317608553
78. Smith SM, Pryor AJ, Hulbert SH (2004) Allelic and haplotypic diversity at the Rp1 rust resistance locus of maize. Genetics 167(4):1939–1947. doi:10.1534/genetics.104.029371
79. Studer B, Jensen LB, Fiil A, Asp T (2009) “Blind” mapping of genic DNA sequence polymorphisms in Lolium perenne L. by high resolution melting curve analysis. Mol Breed 24(2):191–199. doi:10.1007/s11032-009-9291-x
80. Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, Li D, Meyer T, Muller R, Ploetz L, Radenbaugh A, Singh S, Swing V, Tissier C, Zhang P, Huala E (2008) The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Res 36:D1009–D1014. doi:10.1093/nar/gkm965
81. Swiderski MR, Innes RW (2001) The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. Plant J Cell Mol Biol 26(1):101–112
82. TAIR (2013) The Arabidopsis information resource (TAIR). http://arabidopsis.org. Accessed 11 July 2013
83. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. doi:10.1093/molbev/msr121
84. Teixeira FF, Bosco dos Santos J, Patto Ramalho MA, Barbosa Abreu ÂdF, Teixeira Guimarães C, Carlos de Oliveira A (2005) QTL mapping for angular leaf spot in common bean using microsatellite markers. Crop Breed Appl Biotechnol 5:272–278
85. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3–new capabilities and interfaces. Nucl Acids Res 40(15):e115. doi:10.1093/nar/gks596
86. Vallejos EC, 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(2):1229–1242
87. Wang J, Chuang K, Ahluwalia M, Patel S, Umblas N, Mirel D, Higuchi R, Germer S (2005) High-throughput SNP genotyping by single-tube PCR with T-m-shift primers. Biotechniques 39(6):885–893. doi:10.2144/000112028
88. Warren RF, Merritt PM, Holub E, Innes RW (1999) Identification of three putative signal transduction genes involved in R gene-specified disease resistance in Arabidopsis. Genetics 152(1):401–412
89. Wei FS, Wong RA, Wise RP (2002) Genome dynamics and evolution of the Mla (powdery mildew) resistance locus in barley. Plant Cell 14(8):1903–1917. doi:10.1105/tpc.002238
90. Wheeler B (2010) lmPerm: permutation tests for linear models, R package. http://www.icesi.edu.co/CRAN/src/contrib/Archive/lmPerm/lmPerm_1.1-0.tar.gz
91. Willocquet L, Allorent D, Savary S (2004) Quantitative analysis of two important epidemiological features of the common bean: Phaeoisariopsis griseola pathosystem. Fitopatol Bras 29(6):676–679
92. Wittwer CT, Reed GH, Gundry CN, Vandersteen JG, Pryor RJ (2003) High-resolution genotyping by amplicon melting analysis using LCGreen. Clin Chem 49(6):853–860. doi:10.1373/49.6.853
93. Xin ZG, Velten JP, Oliver MJ, Burke JJ (2003) High-throughput DNA extraction method suitable for PCR. Biotechniques 34(4):820–826
94. Yu K, Park SJ, Poysa V, Gepts P (2000) Integration of simple sequence repeat (SSR) markers into a molecular linkage map of common bean (Phaseolus vulgaris L.). J Hered 91(6):429–434. doi:10.1093/jhered/91.6.429
95. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7(1–2):203–214. doi:10.1089/10665270050081478
96. Zhang Y, Lubberstedt T, Xu ML (2013) The genetic and molecular basis of plant resistance to pathogens. J Genet Genom 40(1):23–35. doi:10.1016/j.jgg.2012.11.003
97. Zhou J, Loh Y-T, Bressan RA, Martin GB (1995) The tomato gene Pti1 encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell 83(6):925–935. doi:10.1016/0092-8674(95)90208-2