Abstract
The anthracnose disease caused by the fungal pathogen Colletotrichum lindemuthianum (Sacc & Magnus) Briosi & Cavara, is a disease that causes significant seed yield losses in common bean (Phaseolus vulgaris L.) worldwide. A germplasm collection of climbing beans from Guatemala was evaluated in the greenhouse for their reaction to race 73 of C. lindemuthianum that occurs in many growing areas worldwide. This germplasm mostly represents the so-called race Guatemala. Approximately 10% of 369 climbing bean accessions showed no symptoms (score of 1 on a 1–9 anthracnose severity visual score scale). Genome wide association study (GWAS) results using 78,754 SNP markers indicated that genomic regions with resistance to race 73 of C. lindemuthianum exist in Pv04 and Pv07, which have been previously reported. We also report four candidate genes located on Pv04 and Pv07 suspected to be responsible for anthracnose resistance, based on their proximity to significantly associated SNP markers.
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References
Adam-Blondon AF, Sevignac M, Dron M, Bannerot H (1994) A genetic map of common bean to localize specific resistance genes against anthracnose. Genome 37:915–924
Awale H, Falconí-Castillo E, Villatoro-Mérida JC, Kelly J (2008) Caracterización de aislamientos de Colletotrichum lindemuthianum de Ecuador y Guatemala para identificar genes de resistencia. Agronomía Mesoamericana 1–6
Alzate-Marin AL, Menarim H, Chagas JM, de Barros EG, Moreira MA (2000) Identification of RAPD marker linked to Co-6 anthracnose resistance gene in common bean cultivar AB136. Genet Mol Biol 23:633–637
Alzate-Marin AL, Costa MR, Arruda KM et al (2003) Characterization of the anthracnose resistance gene present in Ouro Negro (Honduras 35) common bean cultivar. Euphytica 133:165–169
Alzate-Marin AL, Souza KA, Silva MGM et al (2007) Genetic characterization of anthracnose resistance genes genes Co-43 and Co-9 in common bean cultivar Tlalnepantla 64 (PI207262). Euphytica 154:1–8
Balardin RS, Jarosz AM, Kelly JD (1997) Virulence and molecular diversity in Colletotrichum lindemuthianum from South, Central, and North America. Phytopathol 87:1184–1191
Beebe SE, Pastor-Corrales MA (1991) Breeding for disease resistance. In: van Schoonhoven A, Voyest O (eds) Common beans: research for crop improvement. Wallingford, pp 561–617
Beebe S, Skroch PW, Tohme J et al (2000) Structure of genetic diversity among common bean landaces of Middle American origin based on correspondence analysis of RAPD. Crop Sci 40:264–273
Bellincampi D, Cervone F, Lionetti V (2014) Plant cell wall dynamics and wall-related susceptibility in plant–pathogen interactions. Front Plant Sci 5:228. https://doi.org/10.3389/fpls.2014.00228
Bellucci E, Bitocchi E, Rau D, Rodriguez M, Biagetti E, Giardini A, Attene G, Nanni L, Papa R (2014) Genomics of origin, domestication and evolution of Phaseolus vulgaris. In: Tuberosa R, Graner A, Frison E (eds) Genomics of plant genetic resources. Springer, Dordrecht, pp 483–507
Blair MW, Giraldo MC, Buendia HF et al (2006) Microsatellite marker diversity in common bean (Phaseolus vulgaris L.). Theor Appl Genet 113:100–109
Broughton WJ, Hernández G, Blair M et al (2003) Beans (Phaseolus spp.) – model food legumes. Plant Soil 252:55–128
Burlakoti RR (2008) Gibberella Zeae: population structure, mycotoxin profiles, real-time PCR quantification, and host resistance. Dissertation, North Dakota State University
Campa A, Rodríguez-Suárez C, Pañeda A et al (2005) The bean anthracnose resistance gene Co-5 is located in linkage group B7. Annu Rept Bean Improv Coop 48:68–69
Campa A, Vega EP, Giraldez R et al (2007) Inheritance of race-specific resistance to anthracnose in the differential cultivar AB136. Annu Rept Bean Improv Coop 50:87–88
Campa A, Giraldez R, Ferreira JJ (2009) Genetic dissection of the resistance to nine anthracnose races in the common bean differential cultivars MDRK and TU. Theor Appl Genet 119:1–11
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
Campa A, Trabanco N, Ferreira JJ (2017) Identification of clusters that condition resistance to Anthracnose in the common bean differential cultivars AB136 and MDRK. Phytopathology 107:1515–1521
Castellanos G, Jara C, Mosquera G (2015) Bean pathogens: practical guide for lab and greenhouse work. Centro Internacional de Agricultura Tropical (CIAT). Cali, Colombia. 244p
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. https://doi.org/10.2135/cropsci2015.10.0651
Chacón MI, Pickersgill B, Debouck DG (2005) Domestication patterns in common bean (Phaseolus vulgaris L.) and the origin of the Mesoamerican and Andean cultivated races. Theor Appl Genet 110:432–444
Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833
de Lima Castro SA, Gonçalves-Vidigal MC, Gilio TAS et al (2017) Genetics and mapping of a new anthracnose resistance locus in Andean common bean Paloma. BMC Genomics 18(1)
Del Rio L, Bradley C (2002) Anthracnose of dry beans. NDSU Extension Service, pp 1233
Fernández O, Fernando O, Gepts PL, López GM, Arregocés O (1986) Stages of development of the common bean plant. Centro Internacional de Agricultura Tropical (CIAT), Cali, CO, pp32
Ferreira JJ, Campa A, Kelly JD (2013) Organization of genes conferring resistance to Anthracnose in common bean. In: Varshney RK, Tuberosa R (eds) Translational genomics for crop breeding. Wiley, New York, pp 151–181
Flor HH (1955) Host-parasite interaction in flax rust -its genetics and other implications. Phytopathology 45:680–685
Fouilloux G (1976) Bean anthracnose: new genes of resistance. Ann Rep Bean Improv Coop 19:36–37
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
Geffroy V, Macadre C, David P et al (2009) Molecular analysis of a large subtelomeric nucleotide-binding-siteleucine-rich-repeat family in two representative genotypes of the major gene pools of Phaseolus vulgaris. Genetics 181:405–419. https://doi.org/10.1534/genetics.108.093583
Gonçalves-Vidigal MC, Kelly JD (2006) Inheritance of anthracnose resistance in the common bean cultivar Widusa. Euphytica 151:411–419. https://doi.org/10.1007/s10681-006-9164-x
Gonçalves-Vidigal MC, Silva CR, Vidigal Filho PS (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
Gonçalves-Vidigal MC, Lacanallo GF, Vidigal PS (2008) A new Andean gene conferring resistance to anthracnos in common bean (Phaseolus vulgaris L.) cultivar Jalo Vermelho. Plant Breed 127:592–596
Gonçalves-Vidigal MC, Vidigal Filho PS, Medeiros AF et al (2009) Common bean landrace Jalo Listras Pretas is the source of a new Andean anthracnose resistance gene. Crop Sci 49:133–138
Gonçalves-Vidigal MC, Cruz AS, Garcia A et al (2011) Linkage mapping of the Phg-1 and Co-14 genes for resistance to angular leaf spot and anthracnose in the common bean cultivar AND 277. Theor Appl Genet 122:893–903. https://doi.org/10.1007/s00122-010-1496-1
Gonçalves-Vidigal MC, Meirelles AC, Poletine JP et al (2012) Genetic analysis of anthracnose resistance in ‘Pitanga’ dry bean cultivar. Plant Breed 131:423–429
Gonçalves-Vidigal MC, Cruz AS, Lacanallo GF et al (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(9):2245–2255. https://doi.org/10.1007/s00122-013-2131-8
Gonçalves-Vidigal MC, Pacheco CMNA, Vidigal Filho PS et al (2016) Genetic mapping of the anthracnose resistance gene Co-14 in the common bean cultivar Pitanga. Ann Rep Bean Improv Coop 59:55–56
Goodstein DM, Shu S, Howson R et al (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:1178–1186
Halvorson JM, Lamppa RS, Markell SG, Pasche JS (2016) Characterization of Colletotrichum lindemuthianum races infecting dry edible bean in North Dakota. Can J Plant Pathol 38:64–69
He J, Zhao X, Laroche A et al (2014) Genotyping-by-sequencing (GBS), an ultimate marker-assisted selection (MAS) tool to accelerate plant breeding. Front Plant Sci 5:484. https://doi.org/10.3389/fpls.2014.00484
Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329. https://doi.org/10.1038/nature05286
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 Crop Res 82:135–154
Kelly JD, Vallejo VA (2004) A Comprehensive review of the major genes conditioning resistance to anthracnose in common bean. HortSci 39:1196–1207
Lacanallo GF, Gonçalves-Vidigal MC (2015) Mapping of an Andean gene for anthracnose resistance (Co-13) in common bean (Phaseolus vulgaris L.) Jalo Listras Pretas landrace. Aust J Crop Sci 9:394–400
Lipka AE, Tian F, Wang Q et al (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics 28:2397–2399
Mahuku GS, Riascos JJ (2004) Virulence and molecular diversity within Colletotrichum lindemuthianum isolates from Andean and Mesoamerican bean varieties and regions. Eur J Plant Path 110:253–263
Maldonado-Mota CR (2017) Identification of new sources of resistance to anthracnose in climbing bean germplasm from Guatemala. Dissertation, North Dakota State University
Mamidi S, Chikara S, Goos RJ et al (2011) Genome-wide association analysis identifies candidate genes associated with iron deficiency chlorosis in soybean. Plant Genome 4:154–164
Mamidi S, Lee RK, Goos JR et al (2014) Genome-wide association studies identifies seven major regions responsible for iron deficiency chlorosis in soybean (Glycine max). PLoS One 9(9):e107469. https://doi.org/10.1371/journal.pone.0107469
Mayer AM, Staples RC (2002) Laccase: new functions for an old enzyme. Phytochemistry 60:551–565
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
McKenna A, Hanna M, Banks E et al (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303
Méndez-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(3):237–245
Meziadi C, Richard MMS, Derquennes A et al (2016) Development of molecular markers linked to disease resistance genes in common bean based on whole genome sequence. Plant Sci 242:351–357
Miklas PN, Kelly JD, Beebe SE et al (2006) Common bean breeding for resistance against biotic and abiotic stresses: From classical to MAS breeding. Euphytica 147:105–131
Moghaddam SM, Mamidi S, Osorno JM et al (2016) Genome-wide association study identifies candidate loci underlying agronomic traits in a Middle American diversity panel of common bean. Plant Genome 9:1–21
Mohammed A (2013) An overview of distribution, biology and the management of common bean anthracnose. J Plant Pathol Microbiol 4:1–6
Murube E, Campa A, Ferreira JJ (2019) Integrating genetic and physical positions of the anthracnose resistance genes described in bean chromosomes Pv01 and Pv04. PLoS One 14(2):e0212298. https://doi.org/10.1371/journal.pone.0212298
Orellana A, Villatoro J, Mérida M (2006) Caracterización morfoagronómica y evaluación preliminar de la colección de germoplasma de frijol voluble (Phaseolus vulgaris L.) en Chimaltenango. In: Instituto de Ciencia y Tecnología Agrícolas (ICTA) final report, Guatemala, pp 1–17
Padder BA, Sharma PN, Awale HE, Kelly JD (2017) Colletotrichum lindemuthianum, the causal agent of bean anthracnose. J Plant Pathol 99:317–330
Pastor-Corrales MA (1991) Estandarización de variedades diferenciales y de designación de razas de Colletotrichum lindemuthianum. Phytopathol 81:694
Pastor-Corrales MA, Tu JC (1994) Antracnosis. In: Pastor-Corrales MA y Schwartz HF (eds), Problemas de Producción del Frijol en los Trópicos, 2nd ed. Centro Internacional de Agricultura Tropical (CIAT). Cali, Colombia. 805 p, pages 87–119
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 anthracnose resistance genes Co-4 and Co-6. Annu Rep Bean Improv Coop 47:249–250
Richard MS, Pflieger S, Sévignac M et al (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(7):1653–1666. https://doi.org/10.1007/s00122-014-2328-5
Rodríguez-Suárez C, Ferreira JJ, Campa A et al (2008) Molecular mapping and intra-cluster recombination between anthracnose racespecific resistance genes in the common bean differential cultivars Mexico 222 and Widusa. Theor Appl Genet 116:807–814
Scheet P, Stephens M (2006) A fast and flexible statistical model for large-scale population genotype data: Applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet 78:628–644
Schmutz J, McClean PE, Mamidi S et al (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46:707–713
Schröder S, Mamidi S, Lee R et al (2016) Optimization of genotyping by sequencing (GBS) data in common bean (Phaseolus vulgaris L.). Mol Breed 36:1–9
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
Schwartz HF, Steadman JR, Hall R et al (2005) Anthracnose. In: American Phytopathological Society (ed) Compendium of bean diseases, 2nd edn. St. Paul, pp 109
Singh SP, Schwartz HF (2010) Breeding common bean for resistance to diseases: a review. Crop Sci 50:2199–2223
Sousa LL, Cruz AS, Vidigal-Filho PS et al (2014) Genetic mapping of the resistance allele Co-52 to Colletotrichum lindemuthianum in the common bean MSU 7-1 line. Aust J Crop Sci 8:317–323
Sousa LL, Gonçalves AO, Gonçalves-Vidigal MC et al (2015) Genetic characterization and mapping of anthracnose resistance of common bean landrace cultivar Corinthiano. Crop Sci 55:1–11
Tian M, Huitema E, da Cunha L et al (2004) A Kazal-like extracellular serine protease inhibitor from Phytophthora infestans targets the tomato pathogenesis-related protease P69B. J Biol Chem 279:26370–26377
Tobar-Piñón MG, Moghaddam SM, Lee RK et al (2020) Genetic diversity of Guatemalan climbing bean collections. Gen Resour Crop Evol 1-18
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 https://doi.org/10.3835/plantgenome2014.10.0079
Valentini G, Gonçalves-Vidigal MC, Hurtado-Gonzales OP et al (2017) 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
Vallejo V, Kelly JD (2001) Development of a SCAR marker linked to the Co-5 locus in common bean. Ann Rep Bean Improv Coop 44:121–112
Vallejo V, Kelly JD (2009) New insights into the anthracnose resistance of common bean landrace G 2333. Open Hortic J 2:29–33
Van der Hoorn RA, Kamoun S (2008) From Guard to Decoy: a new model for perception of plant pathogen effectors. Plant Cell 220:2009–2017
Van Schoonhoven A, Pastor-Corrales MA (1987) Standard system for the evaluation of bean germplasm. In: Centro Internacional de Agricultura Tropical (ed) Global and regional trends in production, trade and consumption of food legume crops. Cali, Colombia, pp 29–54
Wang GF, Balint-Kurti PJ (2016) Maize homologs of CCoAOMT and HCT, two key enzymes in lignin biosynthesis, form complexes with the NLR Rp1 protein to modulate the defense response. Plant Physiol 171:2166–2177
Wang J, Feng J, Jia W, Chang S, Li S, Li Y (2015) Lignin engineering through laccase modification: a promising field for energy plant improvement. Biotechnol Biofuels 8:145. https://doi.org/10.1186/s13068-015-0331-y
Young RA, Kelly JD (1996) Characterization of the genetic resistance to Colletotrichum lindemuthianum in common bean differential cultivars. Plant Dis 80:650–654
Young RA, Kelly JD (1997) RAPD markers linked to three major anthracnose resistance genes in common bean. Crop Sci 37:940–946
Young RA, Melotto M, Nodari RO et al (1998) Marker-assisted dissection of the oligogenic anthracnose resistance in the common bean cultivar, “G2333”. Theor Appl Genet 96:87–94
Zhang Z, Ersoz E, Lai CQ et al (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42:355–360
Zizumbo-Villarreal D, Flores-Silva A, Colunga-García MP (2012) The archaic diet in Mesoamerica: incentive for milpa development and species domestication. Econ Bot 66:328–343
Zuiderveen GH, Padder BA, Kamfwa K et al (2016) Genome-wide association study of anthracnose resistance in Andean beans (Phaseolus vulgaris). PLoS One 11(6):e0156391
Acknowledgements
Feed the Future, USAID, Legume Innovation Lab. Genetic Improvement of Middle-American Climbing Beans in Guatemala (SO1.A1); Dry bean breeding program, Dry bean pathology lab and Dry bean genomics lab, NDSU, Fargo, North Dakota; USDA-ARS Soybean Genomics and Improvement Laboratory Beltsville Agricultural Research Center, Maryland; ICTA, Dry bean breeding program, Guatemala. Special thanks to, Robin Lamppa, Rian Lee, Katelynn Walter, Ali Soltani, Luz Montejo, Julio Villatoro, Angela Miranda, Jessica Moscoso, Daniel Coc, Tomás Yancós, Elmer Estrada, Erick William De León, Leonel Esteban Monterroso and Eunice Barrera.
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Maldonado-Mota, C.R., Moghaddam, S.M., Schröder, S. et al. Genomic regions associated with resistance to anthracnose in the Guatemalan climbing bean (Phaseolus vulgaris L.) germplasm collection. Genet Resour Crop Evol 68, 1073–1083 (2021). https://doi.org/10.1007/s10722-020-01050-y
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DOI: https://doi.org/10.1007/s10722-020-01050-y