Abstract
Anthracnose is a severe disease of common bean that, under favorable conditions, can cause a 100% yield loss. For effective resistance breeding, the virulence and genetic variability of the causal pathogen, Colletotrichum lindemuthianum, must be understood and the emergence of new races monitored to ensure the development of broad-spectrum, durable resistance. In the present study, 28 isolates of C. lindemuthianum collected in Pernambuco, Brazil, were characterized: i) for their pathogenicity on a differential common bean cultivar set, ii) for their genetic variability, based on the Internally Transcribed Spacer (ITS) region sequences, and iii) for their ability to cause anthracnose on a selection of 20 common bean accessions. The 12 differential cultivars were inoculated with the 28 isolates, identifying 16 races of C. lindemuthianum: 2, 3, 8, 9, 10, 64, 65, 72, 73, 75, 81, 85, 89, 117, 139, and 331. Except for race 81, all were reported for the first time in Pernambuco; this was the first report of race 139 in Brazil and of race 331 in the world. The ITS region sequence of 17 isolates revealed the presence of 27 SNPs, four SNPs in the ITS 1 region, and 23 SNPs in the ITS 2 region. Of the 20 common bean accessions screened for resistance with the 16 isolates of C. lindemuthianum, the Andean accessions ‘Praia’ and ‘Africano 4’ were the most resistant. The broad resistance detected in some common bean accessions indicates their utility as potential sources of resistance to C. lindemuthianum, particularly in areas where Mesoamerican beans and Mesoamerican races of the pathogen are predominant.
Similar content being viewed by others
References
Abud, R. O. G., Wendland, A., Pereira, R. J., Melo, L. C., Pereira, H. S., & Costa, J. G. C. (2011). Frequência de patótipos de Colletotrichum lindemuthianum nos estados brasileiros produtores de feijoeiro comum. Congresso Brasileiro de Melhoramento de Plantas. https://ainfo.cnptia.embrapa.br/digital/bitstream/item/41031/1/3660.pdf. Accessed 11 November 2015.
Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25(17), 3389–3402. https://doi.org/10.1093/nar/25.17.3389.
Balardin, R. S., Jarosz, A. M., & Kelly, J. D. (1997). Virulence and molecular diversity in Colletotrichum lindemuthianum from south, central, and North America. Phytopathology, 87, 1184–1191. https://doi.org/10.1094/PHYTO.1997.87.12.1184.
Balardin, R. S., Smith, J. J., & Kelly, J. D. (1999). Ribosomal DNA polymorphism in Colletotrichum lindemuthianum. Mycological Research, 103(7), 841–848. https://doi.org/10.1017/S095375629800776X.
Blair, M. W., Brondani, V. P., Díaz, L. M., & Del Peloso, M. J. (2013). Diversity and population structure of common bean from Brazil. Crop Science, 53, 1983–1993. https://doi.org/10.2135/cropsci2012.09.0516.
Burle, M. L., Fonseca, J., Kami, J., & Gepts, P. (2010). Microsatellite diversity and genetic structure among common bean (Phaseolus vulgaris L.) landraces in Brazil, a secondary center of diversity. Theoretical and Applied Genetics, 121, 801–813. https://doi.org/10.1007/s00122-010-1350-5.
Cárdenas, F., Adams, M. W., & Andersen, A. (1964). The genetic system for reaction of field beans (Phaseolus vulgaris L.) to infection by three physiologic races of C. lindemuthianum. Euphytica, 13, 178–186.
Cárdenas, G. M., Galván, M., Barrera, V., & Carmona, M. (2012). First report of target spot of tobacco caused by Rhizoctonia solani AG-2.1. Plant Disease, 96, –456. https://doi.org/10.1094/PDIS-08-11-0696.
Coêlho, M., Gonçalves-Vidigal, M. C., Sousa, L. L., Nunes, M. P. B. A., Felipin-Azevedo, R., & Galván, M. Z. (2016). Characterization of race 65 of Colletotrichum lindemuthianum by sequencing ITS regions. Acta Scientiarum. Agronomy, 38(4), 429–438. https://doi.org/10.4025/actasciagron.v38i4.30586.
Dean, R., Vab Kan, J. A. L., Pretorius, Z. A., Hammond-Kosack, K. E., Pietro, A. D., Spanu, P. D., et al. (2012). The top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology, 13(4), 414–430. https://doi.org/10.1111/j.1364-3703.2011.00783.x.
Dongfang, Y., Conner, R. L., Yu, K., Balasubramanian, P., Penner, W. C., & Yager, L. M. (2008). Identification of anthracnose resistance genes in dry bean cultivars grown in Manitoba. Canadian Journal of Plant Science, 88, 771–781. https://doi.org/10.4141/CJPS07145.
FAO. (2019). Faostat database gateway. http://www.fao.org. Accessed 10 December 2019.
Gardes, M., & Bruns, T. D. (1993). ITS primers with enhanced specificity for basidiomycetes—Application to the identification of mycorrhizae and rusts. Molecular Ecology, 2, 113–118.
Geffroy, V., Sicard, D., Oliveira, J. C. F., Sévignac, M., Cohen, S., Gepts, P. et al. (1999) Identification of an ancestral resistance gene cluster involved in the coevolution process between Phaseolus vulgaris and its fungal pathogen Colletotrichum lindemuthianum. Molecular Plant-Microbe Interactions, 12(9), 774–784. 10.1094/MPMI.1999.12.9.774
Gepts, P. (1987). Phenology and development. In K. Wisiol, J. D. Hesketh (Eds.), Plant growth modeling for resource management (pp. 1–24). Boca Raton: CRC press 2.
Gonçalves-Vidigal, M. C., & Kelly, J. D. (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, M. C., Silva, C. R., Vidigal Filho, P. S., Gonela, A., & Kvitschal, M. V. (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. https://doi.org/10.1590/S1415-47572007000400015.
Gonçalves-Vidigal, M. C., Thomazella, C., Vidigal Filho, P. S., Kvitschal, M. V., & Elias, H. T. (2008). Characterization of Colletotrichum lindemuthianum isolates using differential cultivars of common bean in Santa Catarina state, Brazil. Brazilian Archives of Biology and Technology, 51(5), 883–888. https://doi.org/10.1590/S1516-89132008000500002.
Gonçalves-Vidigal, M. C., Gilio, T. A. S., Valentini, G., Vaz-Bisneta, M., Vidigal Filho, P. S., Song, Q., Oblessuc, P. R., & 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(6), e0235215. https://doi.org/10.1371/journal.pone.0235215.
Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium, 41, 95–98.
Ishikawa, F. H., Souza, E. A., & Davide, L. M. C. (2008). Genetic variability within isolates of Colletotrichum lindemuthianum belonging to race 65 from the state of Minas Gerais, Brazil. Biologia, 63(2), 156–161. https://doi.org/10.2478/s11756-008-0039-6.
Kado, C. I., & Heskett, M. G. (1970). Selective media for isolation of agrobacterium, Corynebacterium, Erwinia, Pseudomonas, and Xanthomonas. Phytopathology, 60, 969–976. https://doi.org/10.1094/Phyto-60-969.
Kelly, J. D., Afanador, L., & Cameron, L. S. (1994). New races of Colletotrichum lindemuthianum in Michigan and implications in dry bean resistance breeding. Plant Disease, 78(9), 892–894. https://doi.org/10.1094/PD-78-0892.
Mahuku, G. S., & Riascos, J. J. (2004). Virulence and molecular diversity within Colletotrichum lindemuthianum isolates from Andean and Mesoamerican bean varieties and regions. European Journal of Plant Pathology, 110(3), 253–263. https://doi.org/10.1023/B:EJPP.0000019795.18984.74.
Martiniano-Souza, M. C., Gonçalves-Vidigal, M. C., Castro, S. A. L., Costa, A. F., Dartibale, G. B., Franzon, R. C., et al. (2016). Sources of resistance to anthracnose in traditional accessions of common bean from Pernambuco state, Brazil. Annual Report of the Bean Improvement Cooperative, 59, 65–66 http://arsftfbean.uprm.edu/bic/wp-content/uploads/2018/05/BIC_2016_Annual_Report.pdf.
Mastenbroek, C. (1960). A breeding program for resistance to anthracnose in dry shell haricot beans, based on a new gene. Euphytica, 9, 177–184. https://doi.org/10.1007/BF00022219.
Mathur, R. S., Barnett, H. L., & Lilly, V. G. (1950). Sporulation of Colletotrichum lindemuthianum in culture. Phytopathology, 40(1), https://www.cabdirect.org/cabdirect/abstract/19501101352
Melotto, M., & Kelly, J. D. (2000). An allelic series at the Co-1 locus conditioning resistance to anthracnose in common bean of Andean origin. Euphytica, 116, 143–149. https://doi.org/10.1023/A:1004005001049.
Menezes, M., & Silva-Hanlin, D. M. W. (1997). Guia prático para fungos fitopatogênicos. Recife, PE: Imprensa Universitária.
Padder, B. A., Sharma, P. N., Awale, H. E., & Kelly, J. D. (2017). Colletotrichum lindemuthianum, the causal agent of bean anthracnose. Journal of Plant Pathology, 99, 317–330. https://doi.org/10.4454/jpp.v99i2.3867.
Pastor-Corrales, M. A., Otoya, M. M., Molina, A., & Singh, S. P. (1995). Resistance to Colletotrichum lindemuthianum isolates from middle America and Andean South America in different common bean races. Plant Disease, 79, 63–67 https://www.apsnet.org/publications/PlantDisease/BackIssues/Documents/1995Articles/PlantDisease79n01_63.pdf.
Rodríguez-Guerra, R., Ramírez-Rueda, M. T., Martínez de la Vega, O., & Simpson, J. (2003). Variation in genotype, pathotype and anastomosis groups of Colletotrichum lindemuthianum isolates from Mexico. Plant Pathology, 52(2), 228–235. https://doi.org/10.1046/j.1365-3059.2003.00808.x.
Rosada, L. J., Franco, C. C., Sant'Anna, J. R., Kaneshima, E. N., Gonçalves-Vidigal, M. C., & Castro-Prado, M. A. (2010). Parasexuality in race 65 Colletotrichum lindemuthianum isolates. Journal of Eukaryotic Microbiology, 57(4), 383–384. https://doi.org/10.1111/j.1550-7408.2010.00486.x.
Saitou, N., & Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4), 406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454.
Schwartz, H. F., Pastor Corrales, M. A., & Singh, S. P. (1982). New sources of resistance to anthracnose and angular leaf spot of beans (Phaseolus vulgaris L.). Euphytica, 31, 741–754. 10.1007/BF00039213
Singh, S. P., & Schwartz, H. F. (2010). Breeding common bean for resistance to diseases: A review. Crop Science, 50(6), 2199–2223. https://doi.org/10.2135/cropsci2009.03.0163.
Stewart, E., Liu, Z., Crous, P. W., & Szabo, L. J. (1999). Phylogenetic relationships among some cercosporoid anamorphs of Mycosphaerella based on rDNA sequence analysis. Mycological Research, 103(11), 1491–1499. https://doi.org/10.1017/S0953756299008680.
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10), 2731–2739. https://doi.org/10.1093/molbev/msr121.
Thomazella, C., Gonçalves-Vidigal, M. C., Vidigal Filho, P. S., Nunes, W. M. C., & Vida, J. B. (2002). Characterization of Colletotrichum lindemuthianum races in Paraná state, Brazil. Crop Breeding and Applied Biotechnology, 2(1), 55–60. https://doi.org/10.1590/S1516-89132008000500002.
Vidigal Filho, P. S., Gonçalves-Vidigal, M. C., Kelly, J. D., & Kirk, W. W. (2007). Sources of resistance to anthracnose in traditional common beans cultivars from Paraná, Brazil. Journal of Phytopathology, 155(2), 108–113. https://doi.org/10.1111/j.1439-0434.2007.01203.x.
Vidigal Filho, P. S., Gonçalves-Vidigal, M. C., Vaz Bisneta, M., Souza, V. B., Gilio, T. A., Calvi, A. A., et al. (2020). Genome-wide association study of resistance to anthracnose and angular leaf spot in Brazilian Mesoamerican and Andean common bean cultivars. Crop Science, 60, 1–20. https://doi.org/10.1002/csc2.20308.
White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetic. In M. A. Innis, D. H. Gelfald, J. J. Sninsky, & T. J. White (Eds.), PCR protocols: A guide to methods and applications (pp. 315–322). San Diego: Academic Press.
Young, R. A., Melotto, M., Nodari, R. O., & Kelly, J. D. (1998). Marker-assisted dissection of the oligogenic anthracnose resistance in the common bean cultivar, ‘G2333’. Theoretical and Applied Genetics, 96, 87–94. https://doi.org/10.1007/s001220050713.
Acknowledgments
This research was financially supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). Maria da Conceição Martiniano de Souza was supported by a scholarship from CNPq. Maria Celeste Gonçalves-Vidigal received grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). The authors acknowledge Dr. Antonio Felix da Costa of Instituto Agronômico de Pernambuco (IPA), Recife, Pernambuco for kindly donated the seeds, and Dr. Pedrina Gonçalves Vidigal for the first critical reading and final English edits of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Informed consent
All authors have approved the manuscript and agreed with its submission to the European Journal of Plant Pathology.
Human participants and/or animals
The research does not involve human participants and/or animals.
Rights and permissions
About this article
Cite this article
Martiniano-Souza, M.d.C., Gonçalves-Vidigal, M.C., da Costa, A.F. et al. Virulence and genetic diversity of Colletotrichum lindemuthianum and resistance of local common bean germplasm to anthracnose in Pernambuco State, Brazil. Eur J Plant Pathol 159, 727–740 (2021). https://doi.org/10.1007/s10658-020-02179-3
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-020-02179-3