Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Identification of resistance sources in common bean (Phaseolus vulgaris) genotypes from Turkey and the reactions of some promising genotypes to bean anthracnose (Colletotrichum lindemuthianum)

Gülsüm Palacıoğlu https://orcid.org/0000-0002-3603-2413 A , Mehmet Zahit Yeken https://orcid.org/0000-0003-0490-371X B , Faik Kantar C , Hüseyin Çancı D , Vahdettin Çiftçi B , Harun Bayraktar E * and Göksel Özer https://orcid.org/0000-0002-3385-2520 F
+ Author Affiliations
- Author Affiliations

A Department of Plant Protection, Faculty of Agriculture, Şırnak University, Şırnak, 73000, Turkey.

B Department of Field Crops, Faculty of Agriculture, Bolu Abant Izzet Baysal University, Bolu, 14030, Turkey.

C Department of Agricultural Biotechnology, Faculty of Agriculture, Akdeniz University, Antalya, 07000, Turkey.

D Department of Field Crops, Faculty of Agriculture, Akdeniz University, Antalya, 07000, Turkey.

E Department of Plant Protection, Faculty of Agriculture, Ankara University, Ankara, 06010, Turkey.

F Department of Plant Protection, Faculty of Agriculture, Bolu Abant Izzet Baysal University, Bolu, 14030, Turkey.

* Correspondence to: bayrakta@agri.ankara.edu.tr

Handling Editor: Marta Santalla

Crop & Pasture Science 73(10) 1168-1179 https://doi.org/10.1071/CP21704
Submitted: 21 October 2021  Accepted: 11 March 2022   Published: 19 April 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context: Among biotic factors, bean anthracnose caused by Colletotrichum lindemuthianum (Sacc. & Magnus) Briosi & Cavara is one of the most destructive diseases of common bean (Phaseolus vulgaris L.). Resistance in common bean genotypes is controlled by anthracnose resistance loci (designated Co).

Aims: The objective of this study was to evaluate the presence of Co resistance genes in common bean genotypes from Turkey and to examine promising genotypes as candidates for parent plants in breeding studies.

Methods: The presence of Co resistance genes in 693 common bean genotypes from 35 provinces of Turkey was determined by 12 SCAR (sequence characterised amplified region), RAPD (random amplified polymorphic DNA), STS (sequence-tagged site) and CAPS (cleaved amplified polymorphic sequence) markers. The disease reaction of 40 agronomically promising genotypes to different pathogen isolates was evaluated in a pot study.

Key results: The results indicated the presence of Co-1, Co-14, Co-15, Co-2, Co-33, Co-4, Co-42, Co-6, Co-10, Co-11 and Co-13 resistance genes, alone or in combination; Co-5 was not detected in any of the genotypes. Among the genotypes, Co-15 was the most frequent resistance source, followed by Co-4, Co-6 and Co-11, respectively. Common bean genotypes carrying Co-14, Co-2, Co-33, Co-11 and Co-13 have been identified for the first time in Turkish germplasm. Five genotypes carrying the various combinations of Co-1, Co-15, Co-4, Co-6, Co-10, Co-11 and Co-13 were resistant to all isolates in pathogenicity tests.

Conclusions: This study is the most comprehensive to date on Co genes linked to the resistance of common bean genotypes throughout Turkey and provides an important gene pool for breeding studies into bean anthracnose. Resistant genotypes identified will be useful as parent plants in resistance breeding studies.

Implications: Resistance genotypes carrying different Co genes to bean anthracnose will contribute significantly to the disease management strategy.

Keywords: bean anthracnose, Co genes, Co resistance genes, Colletotrichum lindemuthianum, common bean, disease reaction, gene pool, genitor plant, molecular marker, morphological screening.


References

Awale H, Falconi E, Villatoro JC, Kelly JD (2007) Variability in Colletotrichum lindemuthianum from Ecuador and Guatemala. Annual Report Bean Improvement Cooperatıve 50, 85

Balardin RS, Jarosz AM, Kelly JD (1997) Virulence and molecular diversity in Colletotrichum lindemuthianum from South, Central, and North America. Phytopathology 87, 1184–1191.
Virulence and molecular diversity in Colletotrichum lindemuthianum from South, Central, and North America.Crossref | GoogleScholarGoogle Scholar | 18945016PubMed |

Boersma JG, Conner RL, Balasubramanian PM, Yu K, Hou A (2013) Marker-assisted dissection of anthracnose resistance in the dry bean cultivar Morden003. Canadian Journal of Plant Science 93, 1115–1123.
Marker-assisted dissection of anthracnose resistance in the dry bean cultivar Morden003.Crossref | GoogleScholarGoogle Scholar |

Campa A, Rodríguez-Suárez C, Giraldez R, Ferreira JJ (2014) Genetic analysis of the response to eleven Colletotrichum lindemuthianum races in a RIL population of common bean (Phaseolus vulgaris L.). BMC Plant Biology 14, 115
Genetic analysis of the response to eleven Colletotrichum lindemuthianum races in a RIL population of common bean (Phaseolus vulgaris L.).Crossref | GoogleScholarGoogle Scholar | 24779442PubMed |

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, e0169954
Mapping and genetic structure analysis of the anthracnose resistance locus Co-1HY in the common bean (Phaseolus vulgaris L.).Crossref | GoogleScholarGoogle Scholar | 28076395PubMed |

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 gene in Mesoamerican common bean cultivar Crioulo 159. Crop Science 56, 2904–2915.
Characterization and mapping of anthracnose resistance gene in Mesoamerican common bean cultivar Crioulo 159.Crossref | GoogleScholarGoogle Scholar |

Corrêa RX, Costa MR, Good-God PI, Ragagnin VA, Faleiro FG, Moreira MA, de Barros EG (2000) Sequence characterized amplified regions linked to rust resistance genes in the common bean. Crop Science 40, 804–807.
Sequence characterized amplified regions linked to rust resistance genes in the common bean.Crossref | GoogleScholarGoogle Scholar |

Costa LC, Nalin RS, Dias MA, Ferreira ME, Song Q, Pastor-Corrales MA, Hurtado-Gonzales OP, de Souza EA (2021) Different loci control resistance to different isolates of the same race of Colletotrichum lindemuthianum in common bean. Theoretical and Applied Genetics 134, 543–556.
Different loci control resistance to different isolates of the same race of Colletotrichum lindemuthianum in common bean.Crossref | GoogleScholarGoogle Scholar | 33130954PubMed |

Darben LM, Gonela A, Elias HT, da Silva CR, Pastre HH, Gonçalves-Vidigal MC (2017) Common bean germplasm resistant to races 73 and 2047 of Colletotrichum lindemuthianum. African Journal of Biotechnology 16, 1142–1149.
Common bean germplasm resistant to races 73 and 2047 of Colletotrichum lindemuthianum.Crossref | GoogleScholarGoogle Scholar |

de Lima Castro SA, Gonçalves-Vidigal MC, Gilio TAS, Lacanallo GF, Valentini G, Martins VSR, Song Q, Galván MZ, Hurtado-Gonzales OP, Pastor-Corrales MA (2017) Genetics and mapping of a new anthracnose resistance locus in Andean common bean Paloma. BMC Genomics 18, 306
Genetics and mapping of a new anthracnose resistance locus in Andean common bean Paloma.Crossref | GoogleScholarGoogle Scholar | 28420340PubMed |

De Ron AM, Álvarez-García S, Casquero PA, Carro-Huelga G, Gutiérrez S, Lorenzana A, Mayo-Prieto S, Rodríguez-González A, Suárez-Villanueva V, Rodiño AP, Beaver JS (2019) Common bean genetics, breeding, and genomics for adaptation to changing to new agri-environmental conditions. In ‘Genomic designing of climate-smart pulse crops’. (Ed. C Kole) pp. 1–106. (Springer Nature: Cham, Switzerland)

Ekincialp A, Şensoy S (2018) Phenotypic and molecular determination of anthracnose disease resistance in Lake Van Basin’s bean genotypes (Phaseolus vulgaris L.). Legume Research 41, 135–142.
Phenotypic and molecular determination of anthracnose disease resistance in Lake Van Basin’s bean genotypes (Phaseolus vulgaris L.).Crossref | GoogleScholarGoogle Scholar |

Erdinç Ç, Turkmen O, Demir S, Şensoy S (2017) Determination of the anthracnose (Colletotrichum lindemuthianum (Sacc. And Magn.) Lambs. Scrıb.) resistance in some Turkish bean genotypes by artificial inoculation and molecular methods. Journal of Animal and Plant Sciences 27, 175–185.

FAOSTAT (2021) Food and agriculture data. Food and Agriculture Organization of the United Nations, Rome, Italy. Available at http://faostat.fao.org/site/567/default.aspx. [Accessed 20 June 2021]

Geetha SB, Subbareddy S, Satishchandra P, Moses R, Chandra S (2013) Morphological and molecular screening of French bean (Phaseolus vulgaris L.) germplasm using SCAR markers for Colletotrichum lindemuthianum (Sacc. and Magn.) Scrib. causing anthracnose resistance. Archives of Phytopathology and Plant Protection 46, 84–97.
Morphological and molecular screening of French bean (Phaseolus vulgaris L.) germplasm using SCAR markers for Colletotrichum lindemuthianum (Sacc. and Magn.) Scrib. causing anthracnose resistance.Crossref | GoogleScholarGoogle Scholar |

Geffroy V, Creusot F, Falquet J, Sévignac M, Adam-Blondon A-F, Bannerot H, Gepts P, Dron M (1998) A family of LRR sequences in the vicinity of the Co-2 locus for anthracnose resistance in Phaseolus vulgaris and its potential use in marker-assisted selection. Theoretical and Applied Genetics 96, 494–502.
A family of LRR sequences in the vicinity of the Co-2 locus for anthracnose resistance in Phaseolus vulgaris and its potential use in marker-assisted selection.Crossref | GoogleScholarGoogle Scholar | 24710889PubMed |

Genchev D, Christova P, Kiryakov I, Beleva M, Batchvarova R (2010) Breeding of common bean for resistance to the physiological races of anthracnose identified in Bulgaria. Biotechnology & Biotechnological Equipment 24, 1814–1823.
Breeding of common bean for resistance to the physiological races of anthracnose identified in Bulgaria.Crossref | GoogleScholarGoogle Scholar |

Gepts P, Debouck D (1991) Origin, domestication, and evolution of the common bean. In ‘Common beans: research for crop improvement’. (Eds A van Schoonhoven, O Voysest) pp. 7–53. (AB International: Cali, Colombia)

Gilio TAS, Hurtado-Gonzales OP, Valentini G, Castro SAL, Elias HT, Song Q, Gonçalves-Vidigal M, Pastor-Corrales MA (2017) Fine mapping the broad spectrum anthracnose resistance gene in Amendoim Cavalo. Annual Report of the Bean Improvement Cooperative 60, 3–4.

Gonçalves AMO, Gonçalves-Vidigal MC, Vidigal Filho PS, Poletine JP, Lacanallo GF, Coimbra GK (2010) Characterization of the anthracnose resistance gene in Andean common bean Corinthiano cultivar. Annual Report Bean Improvement Cooperative 53, 220–221.

Gonçalves-Vidigal MC, Kelly JD (2006) Inheritance of anthracnose resistance in the common bean cultivar Widusa. Euphytica 151, 411–419.
Inheritance of anthracnose resistance in the common bean cultivar Widusa.Crossref | GoogleScholarGoogle Scholar |

Gonçalves-Vidigal MC, da Silva CR, Vidigal Filho PS, Gonela A, Kvitschal MV (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. Genetics and Molecular Biology 30, 589–593.
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.Crossref | GoogleScholarGoogle Scholar |

Gonçalves-Vidigal MC, Thomazella C, Vidigal Filho PS, Kvitschal MV, Elias HT (2008) Characterization of Colletotrichum lindemuthianum isolates using differential cultivars of common bean in Santa Catarina State, Brazil. Brazilian Archives of Biology and Technology 51, 883–888.
Characterization of Colletotrichum lindemuthianum isolates using differential cultivars of common bean in Santa Catarina State, Brazil.Crossref | GoogleScholarGoogle Scholar |

Gonçalves-Vidigal MC, Vidigal Filho PS, Medeiros AF, Pastor-Corrales MA (2009) Common bean landrace Jalo Listras Pretas is the source of new Andean anthracnose resistance gene. Crop Science 49, 133–138.
Common bean landrace Jalo Listras Pretas is the source of new Andean anthracnose resistance gene.Crossref | GoogleScholarGoogle Scholar |

Gonçalves-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-14 genes for resistance to angular leaf spot and anthracnose in the common bean cultivar AND 277. Theoretical and Applied Genetics 122, 893–903.
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.Crossref | GoogleScholarGoogle Scholar | 21113774PubMed |

Gonçalves-Vidigal MC, Meirelles AC, Poletine JP, De Sousa LL, Cruz AS, Nunes MP, Lacanallo GF, Vidigal Filho PS (2012) Genetic analysis of anthracnose resistance in ‘Pitanga’ dry bean cultivar. Plant Breeding 131, 423–429.
Genetic analysis of anthracnose resistance in ‘Pitanga’ dry bean cultivar.Crossref | GoogleScholarGoogle Scholar |

Gonçalves-Vidigal MC, Cruz AS, Lacanallo GF, Vidigal Filho PS, Sousa LL, Pacheco CMNA, McClean P, Gepts P, 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.
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.Crossref | GoogleScholarGoogle Scholar | 23760652PubMed |

Gonçalves-Vidigal MC, Gilio TAS, Valentini G, Vaz-Bisneta M, Vidigal Filho PS, Song Q, Oblessuc PR, Melotto M (2020) New Andean source of resistance to anthracnose and angular leaf spot: fine-mapping of disease-resistance genes in California Dark Red Kidney common bean cultivar. PLoS ONE 15, e0235215
New Andean source of resistance to anthracnose and angular leaf spot: fine-mapping of disease-resistance genes in California Dark Red Kidney common bean cultivar.Crossref | GoogleScholarGoogle Scholar | 32598372PubMed |

Hegay S, Geleta M, Bryngelsson T, Asanaliev A, Garkava-Gustavsson L, Persson Hovmalm H, Ortiz R (2014) Introducing host–plant resistance to anthracnose in Kyrgyz common bean through inoculation-based and marker-aided selection. Plant Breeding 133, 86–91.
Introducing host–plant resistance to anthracnose in Kyrgyz common bean through inoculation-based and marker-aided selection.Crossref | GoogleScholarGoogle Scholar |

Kelly JD, Bornowski N (2018) Marker-assisted breeding for economic traits in common bean. In ‘Biotechnologies of crop improvement. Vol. 3’. (Eds SS Gosal, SH Wani) pp. 211–238. (Springer Nature: Cham, Switzerland)
| Crossref |

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

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 Crops Research 82, 135–154.
Tagging and mapping of genes and QTL and molecular marker-assisted selection for traits of economic importance in bean and cowpea.Crossref | GoogleScholarGoogle Scholar |

Lacanallo GF, Goncalves-Vidigal MC, Vidigal-Filho PS, Kami J, Gonela A (2010) Mapping of an Andean gene for resistance to anthracnose in the landrace Lallo Listras Pretas. Annual Report Bean Improvement Cooperative 53, 96–97.

Madakbaş SY, Ergin M, Bekar NK (2013) Identification and characterization of anthracnose (Colletotrichum lindemuthianum (Sacc. & Magnus) Lambs. Scrib.) isolates from Turkey using differential set cultivars. Journal of Food, Agriculture & Environment 11, 385–392.

Maldonado-Mota CR, Moghaddam SM, Schröder S, Hurtado-Gonzales OP, McClean PE, Pasche J, Lamppa R, Pastor-Corrales MA, Tobar-Piñón MG, Osorno JM (2021) Genomic regions associated with resistance to anthracnose in the Guatemalan climbing bean (Phaseolus vulgaris L.) germplasm collection. Genetic Resources and Crop Evolution 68, 1073–1083.
Genomic regions associated with resistance to anthracnose in the Guatemalan climbing bean (Phaseolus vulgaris L.) germplasm collection.Crossref | GoogleScholarGoogle Scholar |

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, 237–245.
Molecular markers and allelic relationships of anthracnose resistance gene cluster B4 in common bean.Crossref | GoogleScholarGoogle Scholar |

Meziadi C, Richard MMS, Derquennes A, Thareau V, Blanchet S, Gratias A, Pflieger S, Geffroy V (2016) Development of molecular markers linked to disease resistance genes in common bean based on whole genome sequence. Plant Science 242, 351–357.
Development of molecular markers linked to disease resistance genes in common bean based on whole genome sequence.Crossref | GoogleScholarGoogle Scholar | 26566851PubMed |

Mungalu H, Sansala M, Hamabwe S, Mukuma C, Gepts P, Kelly JD, Kamfwa K (2020) Identification of race-specific quantitative trait loci for resistance to Colletotrichum lindemuthianum in an Andean population of common bean. Crop Science 60, 2843–2856.
Identification of race-specific quantitative trait loci for resistance to Colletotrichum lindemuthianum in an Andean population of common bean.Crossref | GoogleScholarGoogle Scholar |

Nunes MPBA, Gonçalves-Vidigal MC, Martins VSR, Xavier LFS, Valentini G, Vaz Bisneta M, Vidigal Filho PS (2021) Relationship of Colletotrichum lindemuthianum races and resistance loci in the Phaseolus vulgaris L. genome. Crop Science 61, 3877–3893.
Relationship of Colletotrichum lindemuthianum races and resistance loci in the Phaseolus vulgaris L. genome.Crossref | GoogleScholarGoogle Scholar |

Padder BA, Sharma PN, Awale HE, Kelly JD (2017) Colletotrichum lindemuthianum, the causal agent of bean anthracnose. Journal of Plant Pathology 99, 317–330.
Colletotrichum lindemuthianum, the causal agent of bean anthracnose.Crossref | GoogleScholarGoogle Scholar |

Palacıoğlu G, Bayraktar H, Özer G (2018) Genetic diversity of Colletotrichum lindemuthianum, as assessed by iPBS retrotransposon markers. In ‘Proceedings of international agriculture congress’. 3–6 May 2018, Komrat, Moldova. p. 124.

Palacıoğlu G, Bayraktar H, Özer G (2020) Genetic variability of Colletotrichum lindemuthianum isolates from Turkey and resistance of Turkish bean cultivars. Spanish Journal of Agricultural Research 18, e1005
Genetic variability of Colletotrichum lindemuthianum isolates from Turkey and resistance of Turkish bean cultivars.Crossref | GoogleScholarGoogle Scholar |

Palacıoğlu G, Özer G, Yeken MZ, Çiftçi V, Bayraktar H (2021) Resistance sources and reactions of common bean (Phaseolus vulgaris L.) cultivars in Turkey to anthracnose disease. Genetic Resources and Crop Evolution 68, 3373–3381.
Resistance sources and reactions of common bean (Phaseolus vulgaris L.) cultivars in Turkey to anthracnose disease.Crossref | GoogleScholarGoogle Scholar |

Pastor-Corrales MA, Otoya MM, Molina A, Singh SP (1995) Resistance to Colletotrichum lindemuthianum isolates from Middle America and Andean South America in different common bean races. Plant Disease 79, 63–67.
Resistance to Colletotrichum lindemuthianum isolates from Middle America and Andean South America in different common bean races.Crossref | GoogleScholarGoogle Scholar |

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. Annual Report Bean Improvement Cooperative 47, 249–250.

Richard MMS, Pflieger S, Sévignac M, Thareau V, Blanchet S, Li Y, Jackson SA, Geffroy V (2014) Fine mapping of Co-x, an anthracnose resistance gene to a highly virulent strain of Colletotrichum lindemuthianum in common bean. Theoretical and Applied Genetics 127, 1653–1666.
Fine mapping of Co-x, an anthracnose resistance gene to a highly virulent strain of Colletotrichum lindemuthianum in common bean.Crossref | GoogleScholarGoogle Scholar |

Saettler AW (1991) Anthracnose. ‘In Compendium of bean diseases’. (Ed. R Hall) pp. 16–17. (APS Press: St. Paul, MN, USA)

Schoonhoven AV, Pastor-Corrales MA (1987) ‘Standard system for the evaluation of bean germplasm’, p. 56. (CIAT (Centro Intemacional de Agricultura Tropical): Cali, Colombia)

Silva CR, Goncalves-Vidigal MC, Garcia A, Vidigal Filho PS, Gonela A (2009) Identification of a molecular marker linked to the Co-11 anthracnose resistance gene in common bean. Annual Report Bean Improvement Cooperative 52, 46–47.

Singh SP (1991) Bean genetics. In ‘Common beans research for crop improvement’. (Eds A van Schoonhoven, O Voysest). (CAB International, in association with CIAT (Centro Intemacional de Agricultura Tropical): Cali, Colombia)

Souza TLPO, Wendland A, Rodrigues MS, Almeida LCS, Correia FR, Rodrigues LA, Pereira HS, Faria LC, Melo LC (2014) Anthracnose resistance sources to be explored by the common bean breeding programs in Brazil. Annual Report Bean Improvement Cooperative 57, 217–218.

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. The Plant Genome 8, eplantgenome2014.10.0079
Identification of a new chromosomal region involved in the genetic control of resistance to anthracnose in common bean.Crossref | GoogleScholarGoogle Scholar | 33228300PubMed |

Tryphone MT, Chilagane LA, Protas D, Kusolwa PM, Nchimbi-Msolla S (2013) Marker assisted selection for common bean diseases improvements in Tanzania: prospects and future needs. In ‘Plant breeding from laboratories to fields’. (Ed. SB Andersen) pp. 121–147. (IntechOpen: Rijeka, Croatia)
| Crossref |

Vallejo V, Kelly JD (2001) Development of a SCAR marker linked to Co-5 gene in common bean. Annual Report Bean Improvement Cooperative 44, 121–122.

Vidigal Filho PS, Gonçalves-Vidigal MC, Kelly JD, Kirk WW (2007) Sources of resistance to anthracnose in traditional common bean cultivars from Paraná, Brazil. Journal of Phytopathology 155, 108–113.
Sources of resistance to anthracnose in traditional common bean cultivars from Paraná, Brazil.Crossref | GoogleScholarGoogle Scholar |

Vieira AF, Almeida LCS, Rodrigues LA, Costa JGC, Melo LC, Pereira HS, Sanglard DA, Souza TLPO (2018) Selection of resistance sources to common bean anthracnose by field phenotyping and DNA marker-assisted screening. Genetics and Molecular Research 17,
Selection of resistance sources to common bean anthracnose by field phenotyping and DNA marker-assisted screening.Crossref | GoogleScholarGoogle Scholar |

Yeken MZ, Çiftçi V, Çancı H, Özer G, Kantar F (2019) Morphological characterization of common bean genotypes collected from the Western Anatolia region of Turkey. International Journal of Agriculture and Wildlife Science 5, 124–139.
Morphological characterization of common bean genotypes collected from the Western Anatolia region of Turkey.Crossref | GoogleScholarGoogle Scholar |

Young RA, Kelly JD (1997) RAPD markers linked to three major anthracnose resistance genes in common beans. Crop Science 37, 940–946.
RAPD markers linked to three major anthracnose resistance genes in common beans.Crossref | GoogleScholarGoogle Scholar |

Zuiderveen GH, Padder BA, Kamfwa K, Song Q, Kelly JD (2016) Genome-wide association study of anthracnose resistance in Andean beans (Phaseolus vulgaris). PLoS ONE 11, e0156391
Genome-wide association study of anthracnose resistance in Andean beans (Phaseolus vulgaris).Crossref | GoogleScholarGoogle Scholar | 27270627PubMed |