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Different loci control resistance to different isolates of the same race of Colletotrichum lindemuthianum in common bean

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Linkage and genome-wide association analyses using high-throughput SNP genotyping revealed different loci controlling resistance to different isolates of race 65 of Colletotrichum lindemuthianum in common bean.

Abstract

Development of varieties with durable resistance to anthracnose is a major challenge in common bean breeding programs because of the extensive virulence diversity of Colletotrichum lindemuthianum fungus. We used linkage and genome-wide association analyses to tap the genomic regions associated with resistance to different isolates of race 65. Linkage mapping was done using an F2 population derived from the cross between the Mesoamerican common beans BRS Estilo x Ouro Vermelho, inoculated with two different isolates of race 65. Association genetics relied on a diversity common bean panel containing 189 common bean accessions inoculated with five different isolates of race 65 as an attempt to validate the linkage analysis findings and, eventually, identify other genomic regions associated with resistance to race 65. The F2 population and diversity panel were genotyped with the BARCBean6K_3 Illumina BeadChip containing 5398 SNP markers. Both linkage and genome-wide association analyses identified different loci controlling resistance to different isolates of race 65 on linkage group Pv04. Genome-wide association analysis also detected loci on Pv05, Pv10 and Pv11 associated with resistance to race 65. These findings indicate that resistance to race 65 can be overcome by the virulence diversity among different isolates of the same race and could lead to the loss of resistance after cultivar release. We identified 25 resistant common bean cultivars to all five isolates of race 65 in the diversity panel. The accessions should be useful to develop cultivars combining different resistance genes that favor durable resistance to anthracnose in common bean.

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References

  • 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

    CAS  Google Scholar 

  • Alzate-Marin AL, Souza KA, Morais Silva MG et al (2007) Genetic characterization of anthracnose resistance genes Co-4 3 and Co-9 in common bean cultivar tlalnepantla 64 (PI 207262). Euphytica 154:18

    Google Scholar 

  • Balardin RS, Jarosz AM, Kelly JD (1997) Virulence and Molecular Diversity in Colletotrichum lindemuthianum from South, Central, and North America. Phytopathology 87(12):1184–1191. https://doi.org/10.1094/PHYTO.1997.87.12.1184

    Article  CAS  PubMed  Google Scholar 

  • Bannerot H (1965) Résults de I’ infection d’une collection de haricots par six races physiologiques d’anthracnose. Annual de Amélioré des Plantes 15:201–222

    Google Scholar 

  • Barcelos L, Pinto JMA, Vaillancourt LJ, Souza EA (2014) Characterization of Glomerella strains recovered from anthracnose lesions on common bean plants in Brazil. PLoS One 9(3):e90910

    PubMed  PubMed Central  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE et al (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    CAS  PubMed  Google Scholar 

  • Broman KW, Wu H, Sen Ś, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890

    CAS  PubMed  Google Scholar 

  • Broughton W, Hernandez G, Blair M et al (2003) Beans (Phaseolus spp.)—model food legumes. Plant Soil 252:55–128

    CAS  Google Scholar 

  • Brown JKM (2015) Durable resistance of crops to disease: a darwinian perspective. Annu Rev Phytopathol 53:513–539

    CAS  PubMed  Google Scholar 

  • Burt AJ, Manilal William H, Perry G et al (2015) Candidate gene identification with snp marker-based fine mapping of anthracnose resistance gene co-4 in common bean. PLoS One 10(10):e0139450

    PubMed  PubMed Central  Google Scholar 

  • Campa A, Ferreira JJ (2017) Gene coding for an elongation factor is involved in resistance against powdery mildew in common bean. Theor Appl Genet 130:849–860

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Carvalho PRC, Pereira RP, Falleiros MO, Mota SF, Souza EA (2015) Chromosomal characterization of Colletotrichum lindemuthianum and Glomerella spp. strains isolated from common bean. 28th Fungal genetics conference. Pacific Grove, California

  • Castro SAL, Gonçalves-Vidigal MC, Gilio TAS et al (2017) Genetics and mapping of a new anthracnose resistance locus in Andean common bean Paloma. BMC Genom 18:306

    Google Scholar 

  • Chen M, Wu J, Wang L, Mantri N, Zhang X, Zhu Z, Wang S (2017) Mapping and Genetic Structure Analysis of the Anthracnose Resistance Locus Co-1HY in the Common Bean (Phaseolus vulgaris L.). PLoS One 12(1):e0169954

    PubMed  PubMed Central  Google Scholar 

  • Choudhary N, Bawa V, Paliwal R et al (2018) Gene/QTL discovery for Anthracnose in common bean (Phaseolus vulgaris L.) from North-western Himalayas. PLoS One 13(2):e0191700

    PubMed  PubMed Central  Google Scholar 

  • Costa LC, Nalin RS, Ramalho MAP, De Souza EA (2017) Are duplicated genes responsible for anthracnose resistance in common bean? PLoS One 12(3):e0173789

    PubMed  PubMed Central  Google Scholar 

  • Davide LMC, De SEA (2009) Pathogenic variability within race 65 of Colletotrichum lindemuthianum and its implications for common bean breeding. Crop Breed Appl Biotechnol 9:23–30

    Google Scholar 

  • De Ron AM, Papa R, Bitocchi E et al (2013) Common Bean. In: De Ron AM (ed) Grain Legumes. Springer, New York, pp 5–36

    Google Scholar 

  • De Souza TLPO, Alzate-Marin AL, Dessaune SN et al (2007) Inheritance study and validation of SCAR molecular marker for rust resistance in common bean. Crop Breed Appl Biotechnol 7:11–15

    Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19:11–15

    Google Scholar 

  • Earl DA, vonHoldt BM (2012) Structure harvester: a website and program for visualizing structure output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620

    CAS  PubMed  Google Scholar 

  • 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 biotic stress. Wiley-Blackwell, Chichester, pp 151–181

    Google Scholar 

  • Fouilloux G (1976) Bean anthracnose: new genes of resistance. Ann Rep Bean Improv Coop 19:36–37

    Google Scholar 

  • Fouilloux G (1979) New races of bean anthracnose and consequences on our breeding programs. In: International symposium on diseases of tropical food crops. Louvain-la-Neuve, pp 221–235

  • Geffroy V, Sicard D, de Oliveira JCF et al (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 Interact 12:774–784

    CAS  PubMed  Google Scholar 

  • Geffroy V, Sévignac M, Billant P et al (2008) Resistance to Colletotrichum lindemuthianum in Phaseolus vulgaris: a case study for mapping two independent genes. Theor Appl Genet 116:407–415

    CAS  PubMed  Google Scholar 

  • Gilio TAS, Hurtado-Gonzales OP, Valentini G et al (2017) Fine mapping the broad spectrum anthracnose resistance gene in Amendoim Cavalo. Ann Rep Bean Improv Coop 60:3–4

    Google Scholar 

  • Gonçalves-Vidigal MC, Lacanallo GF, Vidigal Filho PS (2008a) A new gene conferring resistance to anthracnose in Andean common bean (Phaseolus vulgaris L.) cultivar ‘Jalo Vermelho.’ Plant Breed 127:592–596

    Google Scholar 

  • Gonçalves-Vidigal MC, Thomazella C, Vidigal Filho PS et al (2008b) Characterization of Colletotrichum lindemuthianum isolates using differential cultivars of common bean in Santa Catarina state, Brazil. Braz Arch Biol Technol 51:883–888

    Google Scholar 

  • 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

    Google Scholar 

  • González AM, Yuste-Lisbona FJ, Rodiño AP et al (2015) Uncovering the genetic architecture of Colletotrichum lindemuthianum resistance through QTL mapping and epistatic interaction analysis in common bean. Front Plant Sci 6:141

    PubMed  PubMed Central  Google Scholar 

  • Ishikawa FH, Souza EA, Davide LMC (2008) Genetic variability within isolates of Colletotrichum lindemuthianum belonging to race 65 from the state of Minas Gerais, Brazil. Biologia (Bratisl) 63:156–161

    CAS  Google Scholar 

  • Ishikawa FH, Ramalho MAP, Souza EA (2011) Common bean lines as potential diffetential cultivars for race 65 of Colletotrichum lindemuthianum. J Plant Pathol 93:461–464

    Google Scholar 

  • Ishikawa FH, Souza EA, Shoji J-Y et al (2012) Heterokaryon incompatibility is suppressed following conidial anastomosis tube fusion in a fungal plant pathogen. PLoS One 7(2):e31175

    CAS  PubMed  PubMed Central  Google Scholar 

  • Keller B, Manzanares C, Jara C et al (2015) Fine-mapping of a major QTL controlling angular leaf spot resistance in common bean (Phaseolus vulgaris L.). Theor Appl Genet 128:813–826

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kelly JD, Bornowski N (2018) Marker-assisted breeding for economic traits in common bean. In: Gosal SS, Wani SH (eds) Biotechnologies of crop improvement genomic approaches, vol 3. Springer, Cham, pp 211–238

    Google Scholar 

  • Kelly JD, Vallejo VA (2004) A comprehensive review of the major genes conditioning resistance to anthracnose in common bean. HortScience 39:1196–1207

    CAS  Google Scholar 

  • Kloth KJ, Thoen MPM, Bouwmeester HJ et al (2012) Association mapping of plant resistance to insects. Trends Plant Sci 17:311–319

    CAS  PubMed  Google Scholar 

  • Kopelman NM, Mayzel J, Jakobsson M et al (2015) CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across k. Mol Ecol Resour 20:1179–1191

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Li X, Zhou Z, Ding J, Wu Y, Zhou B, Wang R, Ma J, Wang S, Zhang X, Xia Z, Chen J, Wu J (2016) Combined linkage and association mapping reveals QTL and candidate genes for plant and ear height in maize. Front Plant Sci 7:833. https://doi.org/10.3389/fpls.2016.00833

    Article  PubMed  PubMed Central  Google Scholar 

  • Margarido GRA, Souza AP, Garcia AAF (2007) OneMap: software for genetic mapping in outcrossing species. Hereditas 144:78–79

    CAS  PubMed  Google Scholar 

  • Martins ACF, Dias MA, Pereira FAC, Souza EA (2019) Productions in vitro and in vivo of sexual structures of Glomerella spp. strains from common bean. Ann Rep Bean Improv Coop 62:15–16

    Google Scholar 

  • Méndez-Vigo B, Rodríguez-Suárez C, Pañeda A et al (2005) Molecular markers and allelic relationships of anthracnose resistance gene cluster B4 in common bean. Euphytica 141:237–245

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Miklas PN, Fourie D, Trapp J et al (2014) New loci including Pse-6 conferring resistance to halo bacterial blight on chromosome Pv04 in common bean. Crop Sci 54:2099–2108

    Google Scholar 

  • Murube E, Campa A, Ferreira J (2019) Integrating genetic and physical positions of the anthracnose resistance genes described in bean chromosomes Pv01 and Pv04. PLoS One 14(2):e0212298

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oblessuc PR, Baroni RM, da Silva PG et al (2014) Quantitative analysis of race-specific resistance to Colletotrichum lindemuthianum in common bean. Mol Breed 34:1313–1329

    CAS  Google Scholar 

  • Padder BA, Sharma PN, Awale HE, Kelly JD (2017) Colletotrichum lindemuthianum, the causal agent of bean Anthracnose. J Plant Pathol 99:317–330

    Google Scholar 

  • Pastor-Corrales MA (1991) Estandarizacion de variedades diferenciales y de designacion de razas de Colletotrichum lindemuthianum. Phytopathology 81:694

    Google Scholar 

  • Perseguini JMKC, Oblessuc PR, Rosa JRBF et al (2016) Genome-wide association studies of anthracnose and angular leaf spot resistance in common bean (Phaseolus vulgaris L.). PLoS One 11(3):e0150506

    PubMed  PubMed Central  Google Scholar 

  • Pinto JMA, Pereira R, Mota SF et al (2012) Investigating Phenotypic Variability in Colletotrichum lindemuthianum Populations. Phytopathology 102:490–497

    CAS  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • RCore Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Ribeiro T, de Esteves JAF, Silva DA et al (2016) Classification of Colletotrichum lindemuthianum races in differential cultivars of common bean. Acta Sci Agron 38:179–184

    Google Scholar 

  • Richard MMS, 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 127:1653–1666

    CAS  PubMed  Google Scholar 

  • Rodríguez-Suárez C, Pañeda A, Campa A et al (2005) Anthracnose resistance spectra of breeding lines derived from the dry bean landrace Andecha. Ann Rep Bean Improv Coop 48:48–49

    Google Scholar 

  • Rohlf FJ (2009) NTSYS-pc: numerical taxonomy and multivariate analysis system. Exeter Publishing Ltd, Setauket, New York

    Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schwartz HF, Pastor-Corrales MA (2005) Anthracnose. In: Schwartz HF, Steadman JR, Hall R, Forster R (eds.) Compendium of bean diseases, 1st ed. APS Press, pp 25–27

  • Silva KJD, Souza EA, Ishikawa FH (2007) Characterization of Colletotrichum lindemuthianum Isolates from the State of Minas Gerais, Brazil. Phytopathology 155:241–247

    Google Scholar 

  • Song Q, Jia G, Hyten DL et al (2015) SNP Assay Development for Linkage Map Construction, Anchoring Whole-Genome Sequence, and Other Genetic and Genomic Applications in Common Bean. G3 Genes Gonomes Genet 5:2285–2290

    Google Scholar 

  • Song Q, Yan L, Quigley C et al (2017) Genetic characterization of the soybean nested association mapping population. Plant Genome 10(2):1–14

    Google Scholar 

  • Souza TLPO (2016) Major angular leaf spot resistance loci in common bean (Phaseolus vulgaris). Ann Rep Bean Improv Coop 59:15–16

    Google Scholar 

  • Souza EA, Camargo Júnior OA, Pinto JMA (2010) Sexual recombination in Colletotrichum lindemuthianum occurs on a fine scale. Genet Mol Res 9:1759–1769

    CAS  PubMed  Google Scholar 

  • Sousa LL, Cruz AS, Filho PSV et al (2014) Genetic mapping of the resistance allele Co-5 2 to Colletotrichum lindemuthianum in the common bean MSU 7–1 line. Aust J Crop Sci 8:317–323

    Google Scholar 

  • 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 55:1900

    CAS  Google Scholar 

  • Turner SD (2014) qqman: an R package for visualizing GWAS results using Q–Q and manhattan plots. Preprint at bioRxiv. https://doi.org/10.1101/005165

    Article  Google Scholar 

  • Valentini G, Gonçalves-Vidigal MC, Gonzales OPH 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

    CAS  PubMed  Google Scholar 

  • van Schoonhoven A, Pastor-Corrales MA (1987) Standard system for the evaluation of bean germplasm. Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia

    Google Scholar 

  • Vlasova A, Capella-Gutiérrez S, Rendón-Anaya M et al (2016) Genome and transcriptome analysis of the Mesoamerican common bean and the role of gene duplications in establishing tissue and temporal specialization of genes. Genome Biol 17:3

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Yu J, Pressoir G, Briggs WH et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208

    CAS  PubMed  Google Scholar 

  • Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. Plant Genome 1:5–20

    CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors are grateful to the following Brazilian funding agencies: Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Fundação de Apoio à Pesquisa do Estado de Minas Gerais (FAPEMIG). This research was also supported by the US Department of Agriculture, Agriculture Research Service, USA, and by EMBRAPA–Brazilian Corporation for Agricultural Research.

Funding

This study was funded by Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (grant number: 88881.131945/2016–01) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (grant number: 140589/2015–5).

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Conceived and designed the experiments: LCC RSN MAD MEF QS MAPC OPHG EAS. Performed the experiments: LCC RSN MAD. Analyzed the data: LCC RSN MEF QS EAS. Contributed reagents/materials/analysis tools: LCC RSN MEF QS EAS. Wrote the paper: LCC RSN MAD MEF QS MAPC OPHG EAS.

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Correspondence to Elaine Aparecida de Souza.

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Communicated by Janila Pasupuleti.

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Costa, L.C., Nalin, R.S., Dias, M.A. et al. Different loci control resistance to different isolates of the same race of Colletotrichum lindemuthianum in common bean. Theor Appl Genet 134, 543–556 (2021). https://doi.org/10.1007/s00122-020-03713-x

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