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Interaction of quantitative trait loci for resistance to common bacterial blight and pathogen isolates in Phaseolus vulgaris L.

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Abstract

Common bacterial blight (CBB) is a major disease of common bean (Phaseolus vulgaris L.) worldwide. Genetic resistance is the most effective and environmentally safe approach for controlling CBB, and identification of resistance quantitative trait loci (QTL) can improve response to selection when breeding for CBB resistance. Interactions of CBB resistance QTL and pathogen isolates with different levels of aggressiveness were studied using an F 4:5 recombinant inbreed line (RIL) population, derived from a cross between the susceptible cultivar “Sanilac” and the resistant breeding line “OAC 09-3.” Disease phenotyping was performed under field and growth room conditions using multiple bacterial isolates with differential levels of aggressiveness. QTL analysis was performed with 237 molecular markers. The effect of pathogen isolate on the average phenotypic value in the RIL population and the interaction of RILs and the pathogen isolates were highly significant. Two QTL underlying CBB resistance were detected on Pv08 and Pv03. A major QTL (R 2 p between 15 and 56%) was identified in a 5-cM (380 kbp) interval in the distal end of the long arm of Pv08. This genomic region was significantly associated with multiple disease evaluation traits in field and growth room assays and against different isolates of the pathogen, which included the previously known CBB marker SU91. A new QTL on Pv03 (Xa3.3SO), associated with the PvSNP85p745405 allele from the susceptible parent, Sanilac, appeared to be an isolate-specific QTL against the aggressive fuscans isolate ISO118. Interaction between the SU91 and Xa3.3SO QTL resulted in a significant reduction in mean disease severity for almost all disease evaluation traits after plants were challenged with the isolate ISO118. The 7.92 and 7.79% diseased areas in RILs with both QTL, compared with 14.92 and 13.81% in RILs without either in test1 and in test2 quantified by image analysis, showed a 44 and 47% reduction of percent diseased areas, indicating that the two QTL interact to limit the expansion of CBB symptoms after infection by ISO118. The information obtained in this study indicates that while the broad-spectrum SU91 QTL is useful in breeding programs, isolate-specific QTL, such as Xa3.3SO, will aid in breeding bean varieties with enhanced resistance against aggressive regional isolates.

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References

  • Anderson J, Down E, Whitford G (1960) The Sanilac pea bean-its history, development and characteristics. Q Bull Mich State Univ Agric Exp Stn 43:214–236

    Google Scholar 

  • Anderson J, Smith B, Washnock C (1999) Cardiovascular and renal benefits of dry bean and soybean intake. Am J Clin Nutr 70:464s–474s

    CAS  PubMed  Google Scholar 

  • Bai Y, Michaels T, Pauls K (1998) Determination of genetic relationships among Phaseolus vulgaris populations in a conical cross from RAPD marker analyses. Mol Breed 4:395–406. doi:10.1023/A:1009601910980

    Article  CAS  Google Scholar 

  • Bett KE, Banniza S (2014) Population study of Xanthomonas spp. from bean growing regions of Canada and response of bean cultivars to pathogen inoculation. Can J Plant Pathol 36:341–353. doi:10.1080/07060661.2014.925000

    Article  Google Scholar 

  • Bett KE, Vandenberg A, Banniza S, Lu Q, Barlow B, Ife S (2013) CDC WM-2 common bean. Can J Plant Sci 94:469–471. doi:10.4141/cjps2013-313

    Article  Google Scholar 

  • Blair MW, Astudillo C, Grusak MA, Graham R, Beebe SE (2009) Inheritance of seed iron and zinc concentrations in common bean (Phaseolus vulgaris L.) Mol Breed 23:197–207. doi:10.1007/s11032-008-9225-z

    Article  CAS  Google Scholar 

  • Darrasse A, Carrère S, Barbe V, Boureau T, Arrieta-Ortiz ML, Bonneau S, Briand M, Brin C, Cociancich S, Durand K, Fouteau S, Gagnevin L, Guérin F, Guy E, Indiana A, Koebnik R, Lauber E, Munoz A, Noël LD, Pieretti I, Poussier S, Pruvost O, Robène-Soustrade I, Rott P, Royer M, Serres-Giardi L, Szurek B, Van Sluys MA, Verdier V, Vernière C, Arlat M, Manceau C, Jacques M-A (2013) Genome sequence of Xanthomonas fuscans subsp. fuscans strain 4834-R reveals that flagellar motility is not a general feature of xanthomonads. BMC Genomics 14:761. doi:10.1186/1471-2164-14-761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Darsonval A, Darrasse A, Durand K, Bureau C, Cesbron S, Jacques M-A (2009) Adhesion and fitness in the bean phyllosphere and transmission to seed of Xanthomonas fuscans subsp. fuscans. Mol Plant-Microbe Interact 22:747–757. doi:10.1094/MPMI-22-6-0747

    Article  CAS  PubMed  Google Scholar 

  • Das MK, Rajaram S, Mundt CC, Kronstad WE (1992) Inheritance of slow-rusting resistance to leaf rust in wheat. Crop Sci 32:1452–1456

    Article  Google Scholar 

  • Duncan RW, Singh SP, Gilbertson RL (2011) Interaction of common bacterial blight bacteria with disease resistance quantitative trait loci in common bean. Phytopathology 101:425–435. doi:10.1094/PHYTO-03-10-0095

    Article  PubMed  Google Scholar 

  • Durham KM, Xie W, Yu K, Pauls KP, Lee E, Navabi A (2013) Interaction of common bacterial blight quantitative trait loci in a resistant inter-cross population of common bean. Plant Breed 132:658–666. doi:10.1111/pbr.12103

    Article  CAS  Google Scholar 

  • Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296. doi:10.1146/annurev.py.09.090171.001423

    Article  Google Scholar 

  • Fourie D, Herselman L (2002) Breeding for common blight resistance in dry beans in South Africa. Annu Rep Bean Improv Coop 45:50–51

    Google Scholar 

  • Freyre R, Skroch PW, Geffroy V, Adam-Blondon AF, Shirmohamadali A, Johnson WC, Llaca V, Nodari RO, Periera 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. doi:10.1007/s001220050964

    Article  CAS  Google Scholar 

  • Gaitán-Solís E, Duque MC, Edwards KJ, Tohme J (2002) Microsatellite repeats in common bean (Phaseolus vulgaris). Crop Sci 42:2128–2136. doi:10.2135/cropsci2002.2128

    Article  Google Scholar 

  • Gillard CL, Conner RL, Howard RJ, Pauls KP, Shaw L, Taran B (2009) The performance of dry bean cultivars with and without common bacterial blight resistance in field studies across Canada. Can J Plant Sci 89:405–410. doi:10.4141/CJPS08045

    Article  Google Scholar 

  • Grisi M, Blair M, Gepts P, Brondani C, Pereira P, Brondani R (2007) Genetic mapping of a new set of microsatellite markers in a reference common bean (Phaseolus vulgaris) population BAT93 x Jalo EEP558. Genet Mol Res GMR 6:691–706

    CAS  PubMed  Google Scholar 

  • Gujaria-Verma N, Ramsay L, Sharpe AG, Sanderson LA, Debouck DG, Tar’an B, Bett KE (2016) Gene-based SNP discovery in tepary bean (Phaseolus acutifolius) and common bean (P. vulgaris) for diversity analysis and comparative mapping. BMC Genomics 17:239. doi:10.1186/s12864-016-2499-3

    Article  PubMed  PubMed Central  Google Scholar 

  • Hajri A, Brin C, Hunault G, Lardeux F, Lemaire C, Manceau C, Boureau T, Poussier S (2009) A «repertoire for repertoire» hypothesis: repertoires of type three effectors are candidate determinants of host specificity in Xanthomonas. PLoS One 4:e6632. doi:10.1371/journal.pone.0006632

    Article  PubMed  PubMed Central  Google Scholar 

  • Holland JB, Nyquist WE, Cervantes-Martinez CT (2003) Estimating and interpreting heritability for plant breeding: an update. Plant breeding reviews 22:9–112

    Google Scholar 

  • Jung G, Coyne DP, Skroch PW, Nienhuis J, Arnaud-Santana E, Bokosi J, Ariyarathne HM, Steadman JR, Beaver JS, Kaeppler SM (1996) Molecular markers associated with plant architecture and resistance to common blight, web blight, and rust in common beans. J Am Soc Hortic Sci 121:794–803

    CAS  Google Scholar 

  • Kosambi DD (1943) The estimation of map distances from recombination values. Ann Eugenics 12:172–175. doi:10.1111/j.1469-1809.1943.tb02321.x

    Article  Google Scholar 

  • Kuć J (1982) Induced immunity to plant disease. Bioscience 32:854–860. doi:10.2307/1309008

    Article  Google Scholar 

  • Leips J, Gilligan P, Mackay TFC (2006) Quantitative trait loci with age-specific effects on fecundity in Drosophila melanogaster. Genetics 172:1595–1605. doi:10.1534/genetics.105.048520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marquez ML, Terán H, Singh SP (2007) Selecting common bean with genes of different evolutionary origins for resistance to Xanthomonas campestris pv. phaseoli. Crop Sci 47:1367–1374. doi:10.2135/cropsci2006.12.0769

    Article  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. doi:10.1007/s00122-010-1375-9

    Article  PubMed  Google Scholar 

  • McElroy JB (1985) Breeding for dry beans, Phaseolus vulgaris L., for common bacterial blight resistance derived from Phaseolus acutifolius. A. Gray. Ph.D. Thesis. Cornell Univ., Ithaca

  • Mhedbi-Hajri N, Darrasse A, Pigne S, Durand K, Fouteau S, Barbe V, Manceau C, Lemaire C, Jacques M-A (2011) Sensing and adhesion are adaptive functions in the plant pathogenic xanthomonads. BMC Evol Biol 11:67. doi:10.1186/1471-2148-11-67

    Article  PubMed  PubMed Central  Google Scholar 

  • Michaels TE, Smith TH, Larsen J, Beattie AD, Pauls KP (2006) OAC Rex common bean. Can J Plant Sci 86:733–736. doi:10.4141/P05-128

    Article  CAS  Google Scholar 

  • Miklas PN, Porch T (2010) Guidelines for common bean QTL nomenclature. Annu Rep Bean Improv Coop 53:202204

    Google Scholar 

  • Miklas PN, Zapata M, Beaver JS, Grafton KF (1999) Registration of four dry bean germplasms resistant to common bacterial blight: ICB-3, ICB-6, ICB-8, and ICB-10. Crop Sci 39:594. doi:10.2135/cropsci1999.0011183X003900020065x

    Article  Google Scholar 

  • Miklas PN, Hu J, Grünwald NJ, Larsen KM (2006) Potential application of TRAP (targeted region amplified polymorphism) markers for mapping and tagging disease resistance traits in common bean. Crop Sci 46:910–916. doi:10.2135/cropsci2005.08-0242

    Article  CAS  Google Scholar 

  • Miklas PN, Fourie D, Trapp J, Larsen RC, Chavarro C, Blair MW, Gepts P (2011) Genetic characterization and molecular mapping gene for resistance to halo blight in common bean. Crop Sci 51:2439–2448. doi:10.2135/cropsci2011.01.0046

    Article  CAS  Google Scholar 

  • Mkandawire ABC, Mabagala RB, Guzmán P, Gepts P, Gilbertson RL (2004) Genetic diversity and pathogenic variation of common blight bacteria (Xanthomonas campestris pv. phaseoli and X. campestris pv. phaseoli var. fuscans) suggests pathogen coevolution with the common bean. Phytopathology 94:593–603. doi:10.1094/PHYTO.2004.94.6.593

    Article  CAS  PubMed  Google Scholar 

  • Mutlu N, Miklas P, Reiser J, Coyne D (2005) Backcross breeding for improved resistance to common bacterial blight in pinto bean (Phaseolus vulgaris L.) Plant Breed 124:282–287. doi:10.1111/j.1439-0523.2005.01078.x

    Article  Google Scholar 

  • Navabi A, Rupert T, Park SJ, Yu K, Smith TH, Pauls KP (2013) Apex common bean. Can J Plant Sci 93:131–135. doi:10.4141/cjps2012-139

    Article  Google Scholar 

  • Nodari R, Tsai S, Guzman P, Gilbertson R, Gepts P (1993) Towards an integrated linkage map of common bean. III. Mapping genetic factors controlling host-bacteria interactions. Genetics 134:341–350

    CAS  PubMed  PubMed Central  Google Scholar 

  • O’Boyle PD, Kelly JD, Kirk WW (2007) Use of marker-assisted selection to breed for resistance to common bacterial blight in common bean. J Am Soc Hortic Sci 132:381–386

    Google Scholar 

  • Pariaud B, Ravigné V, Halkett F, Goyeau H, Carlier J, Lannou C (2009) Aggressiveness and its role in the adaptation of plant pathogens. Plant Pathol 58:409–424. doi:10.1111/j.1365-3059.2009.02039.x

    Article  Google Scholar 

  • Park SJ, Dhanvantari BN (1987) Transfer of common blight (Xanthomonas campestris pv phaseoli) resistance from Phaseolus coccineus Lam. to P. vulgaris L. through interspecific hybridization. Can J Plant Sci 67:685–695. doi:10.4141/cjps87-096

    Article  Google Scholar 

  • Park SO, Coyne DP, Mutlu N, Jung G, Steadman JR (1999) Confirmation of molecular markers and flower color associated with QTL for resistance to common bacterial blight in common beans. J Am Soc Hortic Sci 124:519–526

    CAS  Google Scholar 

  • Pedraza FG, Gallego G, Beebe SE, Tohme J (1997) Marcadores SCAR y RAPD para la resistancia a la bacteriosis comun (CBB). CIAT, Cali

    Google Scholar 

  • Perry G, DiNatale C, Xie W, Navabi A, Reinprecht Y, Crosby W, Yu K, Shi C, Pauls KP (2013) A comparison of the molecular organization of genomic regions associated with resistance to common bacterial blight in two Phaseolus vulgaris genotypes. Front Plant Sci 4:318. doi:10.3389/fpls.2013.00318

    Article  PubMed  PubMed Central  Google Scholar 

  • Saettler AW (1991) Common bacterial blight. In: Hall R (ed) Compendium of bean diseases. APS Press, St. Paul

    Google Scholar 

  • SAS Institute Inc. (2008) SAS/STAT® 9.2. User’s Guide. SAS Institute Inc, Cary, NC

  • 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 M, 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 C, 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. doi:10.1038/ng.3008

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotec 18:233–234. doi:10.1038/72708

    Article  CAS  Google Scholar 

  • Shi C, Yu K, Xie W, Perry G, Navabi A, Peter Pauls K, Miklas P, Fourie D (2012) Development of candidate gene markers associated to common bacterial blight resistance in common bean. Theor Appl Genet 125:1525–1537. doi:10.1007/s00122-012-1931-6

    Article  CAS  PubMed  Google Scholar 

  • Silva LO, Singh SP, Pastor-Corrales MA (1989) Inheritance of resistance to bacterial blight in common bean. Theor Appl Genet 78:619–624. doi:10.1007/BF00262555

    Article  Google Scholar 

  • Singh SP, Miklas PN (2015) Breeding common bean for resistance to common blight: a review. Crop Sci 55:971–984. doi:10.2135/cropsci2014.07.0502

    Article  Google Scholar 

  • Singh SP, Muñoz CG (1999) Resistance to common bacterial blight among Phaseolus species and common bean improvement. Crop Sci 39:80–89. doi:10.2135/cropsci1999.0011183X003900010013x

    Article  Google Scholar 

  • Singh SP, Schwartz HF (2010) Breeding common bean for resistance to diseases: a review. Crop Sci 50:2199–2223. doi:10.2135/cropsci2009.03.0163

    Article  Google Scholar 

  • Singh SP, Muñoz CG, Terán H (2001) Registration of common bacterial blight resistant dry bean germplasm VAX1, VAX 3, and VAX 4. Crop Sci 41:275–276. doi:10.2135/cropsci2001.411275x

    Article  Google Scholar 

  • Smith TH, Michaels TE, Navabi A, Pauls KP (2012) Rexeter common bean. Can J Plant Sci 92:351–353. doi:10.4141/cjps2011-184

    Article  Google Scholar 

  • Tar’an B, Michaels TE, Pauls KP (2001) Mapping genetic factors affecting the reaction to Xanthomonas axonopodis pv. phaseoli in Phaseolus vulgaris L. under field conditions. Genome 44:1046–1056. doi:10.1139/g01-099

    Article  Google Scholar 

  • Thomas CV, Waines JG (1984) Fertile backcross and allotetraploid plants from crosses between tepary beans and common beans. J Hered 75:93–98

    Article  Google Scholar 

  • Vallejos CE, Sakiyama NS, Chase CD (1992) A molecular marker-based linkage map of Phaseolus vulgaris L. Genetics 131:733–740

    CAS  PubMed  PubMed Central  Google Scholar 

  • Van Ooijen J (2006) Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wagenningen

    Google Scholar 

  • Vandemark GJ, Fourie D, Miklas PN (2008) Genotyping with real-time PCR reveals recessive epistasis between independent QTL conferring resistance to common bacterial blight in dry bean. Theor Appl Genet 117:513–522. doi:10.1007/s00122-008-0795-2

    Article  CAS  PubMed  Google Scholar 

  • Viteri DM, Cregan PB, Trapp JJ, Miklas PN, Singh SP (2014) A new common bacterial blight resistance QTL in VAX 1 common bean and interaction of the new QTL, SAP6, and SU91 with bacterial strains. Crop Sci 54:1598–1608. doi:10.2135/cropsci2014.01.0008

    Article  CAS  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78. doi:10.1093/jhered/93.1.77

    Article  CAS  PubMed  Google Scholar 

  • Walters DR (2009) Are plants in the field already induced? Implications for practical disease control. Crop Prot 28:459–465. doi:10.1016/j.cropro.2009.01.009

    Article  Google Scholar 

  • Wang S, Basten C, Zeng Z (2007) Windows QTL cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh

    Google Scholar 

  • Whankaew S, Poopear S, Kanjanawattanawong S, Tangphatsornruang S, Boonseng O, Lightfoot D, Triwitayakorn K (2011) A genome scan for quantitative trait loci affecting cyanogenic potential of cassava root in an outbred population. BMC Genomics 12:266. doi:10.1186/1471-2164-12-266

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie W, Yu K, Pauls KP, Navabi A (2012) Application of image analysis in studies of quantitative disease resistance, exemplified using common bacterial blight–common bean pathosystem. Phytopathology 102:434–442. doi:10.1094/PHYTO-06-11-0175

    Article  PubMed  Google Scholar 

  • Yu K, Park SJ, Poysa V (2000) Marker-assisted selection of common beans for resistance to common bacterial blight: efficacy and economics. Plant Breed 119:411–415. doi:10.1046/j.1439-0523.2000.00514.x

    Article  CAS  Google Scholar 

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Acknowledgements

The authors acknowledge Terry Rupert, Tom Smith, Jan Brazolot, Chris Grainger, Chun Shi, Gregory Perry, Bin Zeng, Larissa Ramsay, and Anastasia Chechulina for their assistance with various aspects of the project. Financial support provided by the Ontario Bean Growers (OBG), the Ontario Ministry of Research and Innovation, the Saskatchewan Pulse Growers, and the Agriculture and Agri-Food Canada is gratefully acknowledged.

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  1. Alireza Navabi

    Present address: Department of Plant Agriculture, University of Guelph, Crop Science Building, 50 Stone Road East, Guelph, ON, N1G 2W1, Canada

Authors and Affiliations

  1. Department of Plant Agriculture, University of Guelph, Crop Science Building, 50 Stone Road East, Guelph, ON, N1G 2W1, Canada

    Weilong Xie, Raja Khanal, Sarah McClymont & K. Peter Pauls

  2. Harrow Research and Development Centre, Agriculture and Agri-Food Canada, 2585 County Road 20, Harrow, ON, N0R 1G0, Canada

    Raja Khanal, Kangfu Yu & Alireza Navabi

  3. Department of Plant Sciences, University of Saskatchewan, 51 Campus Drive, Saskatoon, SK, S7N 5A8, Canada

    Robert Stonehouse & Kirstin Bett

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  1. Weilong Xie
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Correspondence to Alireza Navabi.

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Electronic supplementary material Table S2.

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Electronic supplementary material Figure S1.

Alignment of common bean genetic and physical map. For each linkage group except Pv10, the map on the left is physical map (in megabase pairs, Mbp) based on a BLAST search of molecular markers against the P. vulgaris reference genome JGI v1.0 (http://www.phytozome.net/), the map on the right is the genetic map (in centimorgans, cM) constructed using a F4:5 recombinant inbred population derived from a cross between Sanilac and OAC 09-3. Solid lines connect same markers on both maps with endpoints indicating positions of markers on linkage bars. (PDF 69 kb)

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Xie, W., Khanal, R., McClymont, S. et al. Interaction of quantitative trait loci for resistance to common bacterial blight and pathogen isolates in Phaseolus vulgaris L.. Mol Breeding 37, 55 (2017). https://doi.org/10.1007/s11032-017-0657-1

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