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Genetic diversity of Pseudocercospora griseola resistance loci in common beans

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Abstract

Common bean (Phaseolus vulgaris L.) is one of the most widely grown legumes in the world. Although the crop has high yield potential, average yields in Brazil are low due to several diseases. Angular leaf spot (ALS), caused by Pseudocercospora griseola, is among the most important diseases. A set of 81 accessions from the Instituto Agronômico (IAC, Campinas, SP) germplasm bank were evaluated for ALS resistance and genotyped by 12 microsatellites previously associated with ALS QTL resistance. Allele frequencies, number of alleles per locus, expected heterozygosity (He), and Shannon’s Information Index (I) were calculated. The average Ho was 0.12, and the He was 0.54. The STRUCTURE analysis and UPGMA clustering based on Nei’s genetic distance indicated a moderate degree of genetic diversity, with 4 and 5 main groups, respectively. Evaluation of the severity of ALS showed that 17% of the accessions had resistance. Cultivars were recommended for breeding crosses aimed at gaining in genetic diversity and resistance to ALS.

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References

  • Aggarwal VD, Pastor-Corrales MA, Chirwa RM, Buruchara RA (2004) Andean beans (Phaseolus vulgaris L.) with resistance to the angular leaf spot pathogen (Phaeoisariopsis griseola) in southern and eastern Africa. Euphytica 136:201–210

    Google Scholar 

  • Amaro GB, Abreu AFB, Ramalho MAP, Silva FB (2007) Phenotypic recurrent selection in the common bean (Phaseolus vulgaris L) with carioca-type grains for resistance to the fungi Phaeoisariopsis griseola and identification of RAPD markers linked to the resistance gene. Euphytica 134:297–303

    Google Scholar 

  • Azevedo CBG, Ribeiro T, Silva DA, Carbonell SAM, Chiorato AF (2015) Adaptabilidade, estabilidade e resistência a patógenos em genótipos de feijoeiro. Pesquisa Agropecuária Brasileira 50:912–922

    Google Scholar 

  • Bassi D, Briñez B, Rosa JS, Oblessuc PR, Almeida CP, Nucci SM, Silva LCD, Chiorato AF, Vianello RP, Camargo LEA, Blair MW, Benchimol-Reis LL (2017) Linkage and mapping quantitative loci associated with angular leaf spot and powdery mildew resistance in common beans. Genetics and Molecular Biology 40:109–122

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

  • Bhering LL (2017) Rbio: a tool for biometric and statistical analysis using the R platform. Crop Breeding and Applied Biotechnology 17:187–190

    Google Scholar 

  • Briñez B, Perseguini JMKC, Rosa JS, Bassi D, Gonçalves JGR, Almeida C, Paulino JFC, Blair MW, Chioratto AF, Carbonell SAM, Valdisser PAMR, Vianello RP, Benchimol-Reis LL (2017) Mapping QTLs for drought tolerance in a SEA 5 x AND 277 common bean cross with SSRs and SNP markers. Genetics and Molecular Biology 40:813–823

    PubMed  PubMed Central  Google Scholar 

  • Broughton WJ, Hernández G, Blair M, Beebe SE, Gepts P, Vanderleyden J (2003) Beans (Phaseolus spp.) - model food legumes. Plant and Soil 252:55–128

    CAS  Google Scholar 

  • Campa A, Murube E, Ferreira JJ (2018) Genetic diversity, population structure, and linkage disequilibrium in a Spanish common bean diversity panel revealed through genotyping-by-sequencing. Genes 9:518–518

    PubMed Central  Google Scholar 

  • Carvalho GA, Paula-Júnior TJ, Alzate-Marin AL, Nietsche S, Barros EG, Moreira MA (1998) Herança da resistência da linhagem AND-277 de feijoeiro-comum à raça 63-23 de Phaeoisariopsis griseola e identificação de marcador RAPD ligado ao gene de resistência. Fitopatologia Brasileira 23:482–485

    CAS  Google Scholar 

  • Chataika BYE, Bokosi JM, Kwapata MB, Chirwa RM, Mwale VM, Mnyenyembe P, Myers JR (2010) Performance of parental genotypes and inheritance of Angular Leaf Spot (Phaeosariopsis griseola) resistance in the common bean (Phaseolus vulgaris). African Journal of Biotechnology 9:4398–4406

    Google Scholar 

  • Chiorato AF, Carbonell SAM (2014) O Melhoramento Genético do Feijoeiro no Instituto Agronômico IAC (1932 a 2014) O Agronômico (Campinas) 64/66:6-13

  • CIMMYT (2005) Laboratory protocols: CIMMYT applied molecular genetics laboratory. 3rd edition. CIMMYT, Mexico City, 102 p

  • Colombari Filho JM, Geraldi IO, Barona MAA (2010) Heterose e distâncias genéticas moleculares para a produção de grãos em soja. Ciência e Agrotecnol 34:940–945

    Google Scholar 

  • CONAB - Companhia Nacional de Abastecimento (2019) Acompanhamento da safra brasileira de grãos: Safra 2018/19 - Décimo segundo levantamento. https://www.conab.gov.br/info-agro/safras/graos/boletim-da-safra-de-graos/. Accessed on june, 2020

  • Cooper HD, Spillane C, Hodgkin T (2001) Broadening the genetic base of crops: an overview. In: Cooper HD, Spil-lane C, Hodgkin T (eds) Broadening the genetic base of crop production. CAB International, Wallingford, pp 1–23

    Google Scholar 

  • Corrêa RX, Good-God PIV, Oliveira MLP, Nietsche S, Moreira MA, Barros EG (2001) Herança da resistência à mancha-angular do feijoeiro e identificação de marcadores moleculares flanqueando o loco de resistência. Fitopatologia Brasileira 26:27–32

    Google Scholar 

  • Correa-Victoria FJ, Pastor-Corrales MA, Saettler AW (1989) Angular leaf spot. In: Schwartz HF, Pastor-Corrales MA (eds) Bean production problems in the tropics. CIAT, Cali, pp 59–75

    Google Scholar 

  • Crous PW, Liebenberg MM, Braun U, Johannes Z, Groenewald JZ (2006) Re-evaluating the taxonomic status of Phaeoisariopsis griseola, the causal agent of angular leaf spot of bean. Studies in Mycology 55:163–173

    PubMed  PubMed Central  Google Scholar 

  • da Silva LC, de Souza TLPO, Cruz CD, Carneiro PCS, Silva FF, de Barros EG, de Souza Carneiro JE (2018) Linkage fine-mapping and QTLs affecting morpho-agronomic traits of a Mesoamerican × Andean RIL common bean population. Euphytica 214:221

    Google Scholar 

  • Delfini J, Moda-Cirino V, Ruas CF, dos Santos NJ, Ruas PM, Buratto JS (2017) Distinctness of Brazilian common bean cultivars with carioca and black grain by means of morphoagronomic and molecular descriptors. PLoS ONE 12:e0188798

    PubMed  PubMed Central  Google Scholar 

  • Dray S, Dufour A, Chessel D (2007) The ade4 package - II: two-table and K-table methods. R News 7:47–52

    Google Scholar 

  • Earl DA, Vonholdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 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. Molecular Ecology 14:2611–2620

    CAS  PubMed  Google Scholar 

  • Ferreira E, Cavalcanti P, Nogueira D (2014) ExpDes: a R package for ANOVA and experimentais designs. Applications of Mathematics 5:2952–2958

    Google Scholar 

  • Francis RM (2017) POPHELPER: an R package and web app to analyze and visualize population structure. Molecular Ecology Resources 17:27–32

    CAS  PubMed  Google Scholar 

  • Gioia T, Logozzo G, Marzario S, Spagnoletti Zeuli P, Gepts P (2019) Evolution of SSR diversity from wild types to U.S. advanced cultivars in the Andean and Mesoamerican domestications of common bean (Phaseolus vulgaris). PLoS ONE 14:e0211342

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gonçalves-Vidigal MC, Cruz AS, Garcia A, Kami J, Vidigal Filho PS, Sousa L, Mc Clean P, Gepts P, Pastor-Corrales MA (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. Theoretical and Applied Genetics 122:893–903

    PubMed  Google Scholar 

  • Gonçalves-Vidigal MC, Cruz AS, Lacanallo GF, Vidigal Filho PS, Sousa LL, Pacheco CM, Pastor-Corrales MA (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. Theoretical and Applied Genetics 126:2245–2255

    PubMed  Google Scholar 

  • Guzmán P, Gilbertson R, Nodari R, Jonhson 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 85:600–607

    Google Scholar 

  • Hefni M, Ohrvik V, Mohamed T, Witthoft C (2010) Folate content in foods commonly consumed in Egypt. Food Chemistry 121:540–545

    CAS  Google Scholar 

  • Jesus-Junior WC, Vale FX, Coelho RH, Hau B, Zambolim L, Costa LC, Filho AB (2001) Effects of angular leaf spot and rust on yield loss of Phaseolus vulgaris. Phytopathology 91:1045–1053

    Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology 16:1099–1106

    PubMed  Google Scholar 

  • Kamvar ZN, Brooks JC, Grünwald NJ (2015) Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Frontiers in Genetics 6:208

    PubMed  PubMed Central  Google Scholar 

  • Knapp SJ, Stoup WW, Ross WM (1985) Exact confidence intervals for heritability on a progeny mean basis. Crop Science 25:192–194

    Google Scholar 

  • Keller B, Manzanares C, Jara C, Lobaton JD, Studer B, Raatz B (2015) Fine-mapping of a major QTL controlling angular leaf spot resistance in common bean (Phaseolus vulgaris L.). Theoretical and Applied Genetics 128:813–826

    CAS  PubMed  Google Scholar 

  • Liebenberg MM, Pretorius ZA (1997) A review of angular leaf spot of common bean (Phaseolus vulgaris L). African Plant Protection 3:81–10

    Google Scholar 

  • 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. Molecular Breeding 28:57–71

    Google Scholar 

  • Mendonça HA, dos Santos JB, Ramalho MAP (2003) Genetic control of common bean reaction to angular leaf spot. Crop Breeding and Applied Biotechnology 68:661–664

    Google Scholar 

  • 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 147:105–131

    CAS  Google Scholar 

  • Miller T, Gepts P, Kimno S, Arunga E, Chilagane LA, Nchimbi-Msolla S, Namusoke A, Namayanja A, Tedla YR (2018) Alternative markers linked to the Phg-2 angular leaf spot resistance locus in common bean using the Phaseolus genes marker database. African Journal of Biotechnology 17:818–828

    CAS  Google Scholar 

  • Nay MM, Souza TLPO, Raatz B, Mukankusi CM, Gonçalves-Vidigal MC, Abreu AFB, Melo LC, Pastor-Corrales MA (2019a) A review of angular leaf spot resistance in common bean. Crop Science 59:1376–1391

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nay MM, Mukankusi CM, Studer B, Raatz B (2019b) Haplotypes at the Phg-2 Locus are determining pathotype-specificity of angular leaf spot resistance in common bean. Frontiers in Plant Science 10:1126–1126

    PubMed  PubMed Central  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oblessuc PR, Baroni RM, Garcia AAF, Chioratto AF, Carbonell SAM, Camargo LEA, Benchimol-Reis LL (2012) Mapping of angular leaf spot resistance QTL in common bean (Phaseolus vulgaris L.) under different environments. BMC Genetics 13:50

    PubMed  PubMed Central  Google Scholar 

  • Oblessuc PR, Perseguini JMKC, Baroni RM, Chiorato AF, Carbonel SAM, Mondengo 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. Theoretical and Applied Genetics 26:2451–2465

    Google Scholar 

  • 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 103:161–171

    Google Scholar 

  • Pastor-Corrales MA, Jara C (1995) La evolución de Phaeoisariopsis griseola com el frijol comum en America Latina. Fitopatología Colombiana 19:15–24

    Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research - an update. Bioinformatics 28:2537–2539

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira HS, Mota APS, Rodrigues LA, de Souza TLPO, Melo LC (2019a) Genetic diversity among common bean cultivars based on agronomic traits and molecular markers and application to recommendation of parent lines. Euphytica 215:38

    Google Scholar 

  • Pereira R, Abreu ABF, Nalin RS, Souza EA (2019b) Phenotyping for angular leaf spot severity and its implication in breeding common bean for resistance. Science in Agriculture 76:415–423

    CAS  Google Scholar 

  • Perseguini JMKC, Chioratto AF, Zucchi MI, Colombo CA, Carbonell SAM, Mondego JMC, Gazaffi R, Garcia AAF, Campos T, Souza AP (2011) Genetic diversity in cultivated carioca common beans based on molecular marker analysis. Genetics and Molecular Biology 34:88–102

    CAS  Google Scholar 

  • Perseguini JMKC, Oblessuc PR, Rosa JRBF, Gomes KA, Chiorato AF, Carbonell SAM (2016) Genome-wide association studies of anthracnose and angular leaf spot resistance in common bean (Phaseolus vulgaris L.). PLoS ONE 11:e0150506

    PubMed  PubMed Central  Google Scholar 

  • Perseguini JMKC, Silva GMB, Rosa JRBF, Gazaffi R, Marçal FJ, Carbonell SAM, Chiorato AF, Zucchi MI, Garcia AAF, Benchimol-Reis LL (2015) Developing a common bean core collection suitable for association mapping studies. Genetics and Molecular Biology 38:67–78

    PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raatz B, Mukankusi C, Lobaton JD, Male A, Chisale V, Amsalu B, Fourie D, Mukamuhirwa F, Muimui K, Mutari B, Nchimbi-Msolla S, Nkalubo S, Tumsa K, Chirwa R, Maredia KM, He C (2019) Analyses of African common bean (Phaseolus vulgaris L.) germplasm using a SNP fingerprinting platform: diversity, quality control and molecular breeding. Genetic Resources and Crop Evolution 66:707–722

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rava SCA, Sartorato A, Porto de Carvalho JR (1985) Yield losses in dry bean (Phaseolus vulgaris L.) caused by angular leaf spot (Isariopsis griseola Sacc.). Annual Report Bean Improvement Cooperative 28:5–6

    Google Scholar 

  • Reis-Prado FG, Sartorato A, Costa JGC, Rava CA, Sibov ST, Pinheiro JB, Carneiro MS (2006) Reação de cultivares de feijoeiro comum à mancha angular em casa de vegetação. Fitopatologia Brasileira 31:306–309

    Google Scholar 

  • Sanglard DA, Mafra VS, Ribeiro CAG, Silva LC, Barros EG, Moreira MA, Carneiro JES, Mota APS, Vianello RP, Souza TLPO (2013) Rudá x AND 277 RILs: a potential new core mapping population for common bean. Annual Report Bean Improvement Cooperative 56:23–24

    Google Scholar 

  • Sannazzaro AM, Wutke EB, Oliveira SHF, Castro JL, Gallo PB, Martins ALM, Bortoleto N, Sabino JC, Kanthack RAD, Ishimura I, Silveira LCP, Dornelles CR, Pereira JCVNA, Sakai M, Saes LA, Bacchi GS (2003) Severidade da mancha angular (Phaeiosariopsis griseola) em cultivares de feijoeiro no estado de São Paulo. Unidade de Pesquisa e Desenvolvimento de Sorocaba 70:315–321

    Google Scholar 

  • Sartorato A, Nietsche S, Barros E, Moreira MA, Sartorato A, Nietsche S, Moreira MA (2000) RAPD and SCAR markers linked for resistance gene to angular leaf spot in common beans. Fitopatologia Brasileira 25:637–642

    CAS  Google Scholar 

  • Sartorato A (2004) Pathogenic variability and genetic diversity of Phaeoisariopsis griseola isolates from two counties in the state of Goias, Brazil. Journal of Phytopathology 152:385–390

    Google Scholar 

  • 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 genomewide analysis of dual domestications. Nat Genet 46:707–713.

  • Schwartz HF, Correa F, Pineda P, Otoya MM, Katherman MJ (1981) Dry bean yield losses caused by Ascochyta, angular, and white leaf spots in Colombia. Plant Disease 65:494–496

    Google Scholar 

  • Schwartz HF, Pastor-Corrales MA (1989) Bean production problems in the tropics. CIAT, Cali

    Google Scholar 

  • Schwartz HF, Steadman JR, Hall R, Forster RL (2005) Compendium of bean diseases, 2nd edn. APS Press, St. Paul

    Google Scholar 

  • Scott AJ, Knott M (1974) A cluster analysis method for grouping means in the analysis of variance. Biometrics 30:507–512

    Google Scholar 

  • Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611

    Google Scholar 

  • Singh SP, Schwartz HF (2010) Breeding common bean for resistance to diseases: a review. Crop Science 50:2199–2223

    Google Scholar 

  • Souza TLPO, Gonçalves-Vidigal MC, Raatz B, Mukankusi CM, Abreu ÂFB, Melo LC, Pastor-Corrales MA (2016) Major loci controlling resistance to the angular leaf spot of common bean. Annual Report Bean Improvement Cooperative 59: 15–18

  • Stenglein S, Ploper LD, Vizgarra O, Balleti P (2003) Angular leaf spot: a disease caused by the fungus Phaeoisariopsis griseola (Sacc.) Ferraris on Phaseolus vulgaris L. Advances in Applied Microbiology 52:209–243

    CAS  PubMed  Google Scholar 

  • Tryphone GM, Chilagane LA, Nchimbi-msolla S (2016) Genetic characterization of angular leaf spot resistance in selected common bean landraces from Tanzania. African Journal of Biotechnology 8:14–56

    Google Scholar 

  • Valentini G, Gonçalves-Vidigal MC, Elias JCF, Moiana LD, Mindo NNA (2018) Population structure and genetic diversity of common bean accessions from Brazil. Plant Molecular Biology Reporter 36:897–906

    Google Scholar 

  • Van-Schoonhoven A, Pastor-Corrales MA (1991) Sistema estándar para La evaluación de germoplasma de Frijol. CIAT, Cali, pp 20–46

    Google Scholar 

  • Wagara IN, Mwang’ombe AW, Kimenju JW, Buruchara RA, Jamnadass R, Majiwa PAO (2004) Genetic diversity of Phaeoisariopsis griseola in Kenya as revealed by AFLP and group-specific primers. Journal of Phytopathology 152:235–224

    CAS  Google Scholar 

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Acknowledgments

We are very thankful to Dr. Elaine Aparecida de Souza from the Genetics and Plant Breeding Department (UFLA, MG, Brazil) who gently provided the P. griseola isolate for the development of this study.

Funding

We are grateful to the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for granting funding for the research project (FAPESP Number 2014/11145-2) and scholarships (FAPESP Numbers 2017/01753-3, 2014/19967-1), which enabled this study to be carried out.

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C.P.A.; N.A.; J.F.C.P.; G.F.J.B.; and B.C.D. conducted the experiments. C.P.A and M.M.B. analyzed the data. C.P.A. wrote the draft. G.M.F. conducted the manuscript edition. F.R.A.P; A.F.C.; S.A.M.; and L.L.B-R supported data curation and conducted review of the manuscript. L.L.B-R idealized the study and was responsible for the project’s funding. All the authors read and approved the final version.

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Correspondence to Caléo Panhoca de Almeida.

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de Almeida, C.P., Arruda, N., de Carvalho Paulino, J.F. et al. Genetic diversity of Pseudocercospora griseola resistance loci in common beans. Trop. plant pathol. 46, 129–138 (2021). https://doi.org/10.1007/s40858-020-00395-0

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