Genetic diversity of Colletotrichum lindemuthianum races based on ITS-rDNA regions

  • Marcela Coêlho Universidade Estadual do Maringá https://orcid.org/0000-0002-5472-6486
  • Maria Celeste Gonçalves Vidigal Universidade Estadual de Maringá
  • Pedro Soares Vidigal Filho Universidade Estadual de Maringá
  • Rodrigo Chimenez Franzon Universidade Estadual de Maringá
  • Vanusa Silva Ramos Martins Universidade Estadual de Maringá https://orcid.org/0000-0003-1876-5768
Keywords: Anthracnose, physiological races, ITS regions, genetic variability.

Abstract

Colletotrichum lindemuthianum is the causal agent of anthracnose in common bean. Favorable conditions for this disease might result in up to 100% yield losses. One of the main challenges for common bean producers and breeders still remains the management disease, since this pathogen exhibits a wide genetic variability probably due to its recombination sexual reproduction. The 5·8S gene and the flanking internal transcribed spacer regions (ITS1 and ITS2) of 40 different isolates of C. lindemuthianum collected in Brazil were amplified by PCR, and sequenced in order to determine genetic variability. The results revealed that 46.88% of SNPs were detected in the ITS1 region, while 53.12% of them were located in the ITS2 region. The genetic distance ranged from 0.000 to 0.169 between races. The greatest distance was observed between the races 10 and 73 with a value of 0.169, indicating a wide genetic variability between them. The phylogenetic tree was composed of three groups. Group I had five subgroups. Similar results were also observed through population structure analysis, which revealed the presence of three clusters. These results suggest that sequence analysis of ITS rDNA regions of C. lindemuthianum may be a valuable tool to identify this pathogen through design of specific primers.

CROSSMARK_Color_horizontal.svg

Downloads

Download data is not yet available.

Author Biographies

Marcela Coêlho, Universidade Estadual do Maringá

Departamento de Agronomia

Maria Celeste Gonçalves Vidigal, Universidade Estadual de Maringá

Departamento de Agronomia

Pedro Soares Vidigal Filho, Universidade Estadual de Maringá

Departamento de Agronomia

Rodrigo Chimenez Franzon, Universidade Estadual de Maringá

Departamento de Agronomia

Vanusa Silva Ramos Martins, Universidade Estadual de Maringá

Departamento de Agronomia

References

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 data base search programs. Nucleic Acids Research, 25(17), 3389-3402. https://doi.org/10.1093/nar/25.17.3389

Alzate-Marin, A. L., & Sartorato, A. (2004). Analysis of the pathogenic variability of Colletotrichum lindemuthianum in Brazil. Annual Report of the Bean Improvement Cooperative, 47, 241-242.

Ansari, K. I., Palacios, N., Araya, C., Langin, T., Egan, D., & Doohan, F. M. (2004). Pathogenic and genetic variability among Colletotrichum lindemuthianum isolates of different geographic origins. Plant Pathology, 53(5), 635-642. https://doi.org/10.1111/j.0032-0862.2004.01057.x

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(12), 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

Beebe, S. E., Rengifo, J., Gaitan, E., Duque, M. C. C., & Tohme, J. (2001). Diversity and origin of Andean landraces of common bean. Crop Science, 41(3), 854-862. https://doi.org/10.2135/cropsci2001.413854x

Beebe, S. E., Skroch, P. W., Tohme, J., Duque, M. C., Pedraza, F., & Nienhuis, J. (2000). Structure of genetic diversity among common bean landraces of Middle American origin based on correspondence analysis of RAPD. Crop Science, 40(1), 264-273, 2000. https://doi.org/10.2135/cropsci2000.401264x

Briosi, G., & Cavara, F. (1889). I Fungi Parassiti della Piante Coltivate od utili essicati, delineati e descritti. Fasc. II, nos. 26-50.

Broughton, W. J., Hernández, G., Blair, M., Beebe, S., Gepts, P., & Vanderleyden, J. (2003). Beans (Phaseolus spp.) �?? model food legumes. Plant and Soil, 252, 55-128. https://doi.org/10.1023/A:1024146710611

Bunting, T. E., Plumley, K. A., Clarke, B. B., & Hillman, B. I. (1996). Identification of Magnaporthe poae by PCR and examination of its relationship to other fungi by analysis of their nuclear rDNA ITS-1 regions. Phytopathology, 86, 398-404. https://doi.org/10.1094/Phyto-86-398

Carbonell, S. A. M., Ito, M. F., Pompeu, A. S., Francisco, F. G., Ravagnani, S., Almeida, A. L. L. (1999). Raças fisiológicas de Colletotrichum lindemuthianum e reação de cultivares e linhagens de feijoeiro no Estado de São Paulo. Fitopatologia Brasileira, 24(1), 60-65.

Chacón, S. M. I., Pickersgill, B., & Debouck, D. G. (2005). Domestication patterns in common bean (Phaseolus vulgaris L.) and the origin of the Mesoamerican and Andean cultivated races. Theoretical and Applied Genetics, 110, 432-444. https://doi.org/10.1007/s00122-004-1842-2

Chen, Y. Y., Conner, R. L., Gillard, C. L., Boland, G. J., Babcock, C., Chang, K. F., Hwang, S. F., & Balasubramanian, P. M. (2007). A specific and sensitive method for the detection of Colletotrichum lindemuthianum in dry bean tissue. Plant Disease, 91(10), 1271-1276. https://doi.org/10.1094/ PDIS-91-10-1271

Chiorato, A. F., Carbonell, S. A. M., Moura, R. R., Ito, M. F., & Colombo, C. A. (2006). Co-evolução entre raças fisiológicas de Colletotrichum lindemuthianum e feijoeiro. Bragantia, 65(3), 381-388. https://doi.org/10.1590/S0006-87052006000300003

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

Cooke, D. E. L., & Duncan, J. M. (1997). Phylogenetic analysis of Phytophthora species based on ITS I and ITS II sequences of the ribosomal RNA gene repeat. Mycological Research, 101(6), 667-677. https://doi.org/10.1017/S0953756296003218

Crouch, J. A., Clarke, B. B., & Hillman, B.I. (2009). What is the value of ITS sequence data in Colletotrichum systematics and species diagnosis? A case study using the falcate-spored graminicolous Colletotrichum group. Mycologia, 101(5), 648-656. https://doi.org/10.3852/08-231

Davide, L. M. C., & Souza, E. A. (2009). Pathogenic variability within race 65 of Colletotrichum lindemuthianum and its implications for common bean breeding. Crop Breeding and Applied Biotechnology, 9(1), 23-30. https://doi.org/10.12702/1984-7033.v09n01a04

Del Río, L. E., Lamppa, R. S., Gross, P. L., Brolley, B., & Prischmann, J. (2003). Identification of Colletotrichum lindemuthianum race 73 in Manitoba, Canada. Canadian Journal of Plant Pathology, 25(1), 104-107. https://doi.org/10.1080/07060660309507055

Earl, D. A., & Vonholdt, B. M. (2012). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359-361. https://doi.org/10.1007/s12686-011-9548-7

Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software Structure: a simulation study. Molecular Ecology, 14(8), 2611-2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x

Falconi, E., Ochoa, J., Peralta, E., & Danial, D. (2003). Virulence patterns of Colletotrichum lindemuthianum in common bean in Ecuador. Annual Report of Bean Improvement Cooperative, 46, 167-168.

Felipin-Azevedo, R., Gonçalves-Vidigal, M. C., Lacanallo, G. F., Souza, M. C. M., Castro, S. A. L., Caixeta, M. P., & Vidigal Filho, P. S. (2014). Analysis of diverse Colletotrichum lindemuthianum isolates of common bean (Phaseolus vulgaris L.) from Mato Grosso State, Brazil. Annual Report of the Bean Improvement Cooperative, 57, 143-144.

Ferreira, J. J., Campa, A., Pérez-Veja, E., & Giraldez, R. (2008). Reaction of a bean germplasm collection against five races of Colletotrichum lindemuthianum Identified in Northern Spain and implications for breeding. Plant Disease, 92(5), 705-708. https://doi.org/10.1094/PDIS-92-5-0705

Frias, A. A. T., Gonçalves-Vidigal, M. C., Nanami, D. S. Y., Castro, S. A. de L., Vidigal Filho, P. S., & Lacanallo, G. F. (2016). Genetic resistance to Colletotrichum lindemuthianum in the Andean cultivar Jalo Pintado 2 of common bean. Agronomy Science and Biotechnology, 2(1), 21-28. https://doi.org/10.33158/ASB.2016v2i1p21

Fungaro, M. H. P. (2000). PCR na micologia. Biotecnologia Ciência e Desenvolvimento, 14, 12-16.

Gardes, M., & Bruns, T. D. (1993). ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Molecular Ecology, 2(2), 113-118. https://doi.org/10.1111/j.1365-294x.1993.tb00005.x

Gepts, P., & Debouck, D. G. (1991). Origin, domestication, and evolution of the common bean, Phaseolus vulgaris. In O. Voysest, A. Van Schoonhoven (Ed.), Common beans: research for crop improvement (pp.7-53). Wallingford: CAB International.

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. Brazil Archives of Biology and Technology, 51(5), 883-888. https://doi.org/10.1590/S1516-89132008000500002

Goswami, R. S., Del Rio-Mendoza, L. E., Lamppa, R. S., & Prischmann, J. (2011). Colletotrichum lindemuthianum races prevalent on dry beans in North Dakota and potential sources of resistance. Plant Disease, 95(4), 408-412. https://doi.org/ 10.1094/pdis-06-10-0429

Guzmán, P., Gilbertson, R. L., Nodari, R., Johnson, W. C., Temple, S. R., Mandala, D., Mkandawire, A. B. C., & Gepts, P. (1995). Characterization of variability in the fungus Phaeoisariopsis griseola suggest coevolution with the common bean (Phaseolus vulgaris). Phytopathology, 85(5), 600-607. https://doi.org/10.1094/Phyto-85-600

Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95-98.

Halvorson, J. M., Lamppa, R. S., Markell, S. G., & Pasche, J. S. (2016). Characterization of Colletotrichum lindemuthianum races infecting dry edible bean in North Dakota. Canadian Journal of Plant Pathology, 38(1), 64-69. https://doi.org/10.1080/07060661.2015.1137081

Hefni, M., �?hrvik, V., Tabekha, M., & Witthoft, C. (2010). Folate content in foods commonly consumed in Egypt. Food chemistry, 121(2), 540-545. https://doi.org/10.1016/j.foodchem.2009.12.044

Hlinka, O., Murrell, A., & Barker, S.C. (2002). Evolution of secondary structure of the rRNA internal transcribed spacer 2 (ITS2) in hard ticks (Ixodidae, Arthropoda). Heredity, 88, 275-279. https://doi.org/10.1038/sj.hdy.6800040

Jehan, T., & Lakhanpaul, S. (2006). Single Nucleotide Polymorphism (SNP) �?? Methods and application in plant genetics: a review. Indian Journal of Biotechnology, 5(4), 435- 459.

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.

Kiryakov, I., & Genchev, D. (2009). Races of Colletitrichum lindemuthianum in Rhodoppi Mountains, Bulgaria and landraces resistance. Annual Report of the Bean Improvement Cooperative, 52, 34-35.

Kumar, S., Stecher, G., & Tamura K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33(7), 1870-1874. https://doi.org/ 10.1093/molbev/msw054

Lobuglio, K. F., & Pfister, D. H. (2008). A Glomerella species phylogenetically related to Colletotrichum acutatum on Norway maple in Massachussetts. Mycologia, 100, 710-715.

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., Lacanallo, G. F., Costa, A. F., Vidigal Filho, P. S., Dartibale, G. B., Coêlho, M., Calvi, A. C., & Felipin-Azevedo, R. (2017). Genetic variability of Colletotrichum lindemuthianum by sequencing its regions. Annual Report of the Bean Improvement Cooperative, 60, 9-10.

Menezes, J. R., & Dianese, J. C. (1988). Race characterization of Brazilian isolates of Colletotrichum lindemuthianum and detection of resistance to anthracnose in Phaseolus vulgaris. Phytopathology, 78:650-655. https://doi.org/10.1094/Phyto-78-650

Morin, P. A., Luikart, G., & Wayne, R. K. (2004). SNPs in ecology, evolution and conservation. Trends in Ecology and Evolution, 19(4), 208-216. https://doi.org/10.1016/j.tree.2004.01.009

Moriwaki, J., Tsukiboshi, T., & Sato, T. (2002). Grouping of Colletotrichum species in Japan based on rDNA sequences. Journal of General Plant Pathology, 68, 307-320. https://doi.org/10.1007/PL00013096

Muth, P., & Liebenberg, M. M. (2009). Resistance of dry bean to south African races of Colletotrichum lindemuthianum. Annual Report of Bean Improvement Cooperative, 52, 40-41.

Nanami, D. S. Y., Vidigal, M. C. G., Castro, S. A. de L., Frias, A. A. T., Vidigal Filho, P. S., & Elias, H. T. (2017). Characterization of genetic resistance in Andean common bean cultivar Amendoim Cavalo to Colletotrichum lindemuthianum. Agronomy Science and Biotechnology, 3(1), 43-52. https://doi.org/10.33158/ASB.2017v3i1p43

Navajas, M., Lagnel, J., Fauvel, G., & Moraes, G. (1999). Sequence variation of ribossomal internal trascribed spacers (ITS) in commercially important phytoseiidae mites. Experimental and Applied Acarology, 23, 851-859. https://doi.org/10.1023/A:1006251220052

Nei, M., & Kumar, S. (2000). Molecular Evolution and Phylogenetics. New York, NY: Oxford University Press.

Nunes, M. P., Gonçalves-Vidigal, M. C., Lacanallo, G. F., & Coimbra, G. K. (2013). Comprehension of genetic variability and virulence of Colletotrichum lindemuthianum in common bean. Biennial Meeting of the Bean Improvement Cooperative, Portland, State Oregon/USA.

Padder, B. A., Sharma, P. N., & Sharma, O. P. (2010). Distribution of Colletotrichum lindemuthianum Race Flora and its Implication in Deployment of Resistant Sources across Himachal Pradesh. Research Journal of Agricultural Sciences, 1(1), 1-6.

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(2), 317-330. https://doi.org/10.4454/jpp.v99i2.3867

Pastor-Corrales, M. A., & Tu, J. C. (1989). Anthracnose. In H. F. Schwartz, & Pastor-Corrales, M. A. (Eds.), Bean production problems in the tropics. (p. 77-104). Cali: CIAT.

Pastor-Corrales, M. A., Otoya, M. M., & Molina, A. (1995). Resistance to C. lindemuthianum isolates from Middle America and Andean South America in different common beans races. Plant Disease, 79, 63-67. https://doi.org/10.1094/PD-79-0063

Pastor-Corrales, M. A. (1996). Traditional and molecular confirmation of the coevolution of beans and pathogens in Latin America. Annual Report of the Bean Improvement Cooperative, 39, 46-47.

Pereira, R., Ishikawa, F. H., Pinto, J. M. A., & Souza, E. A. (2010). Occurrence of anthracnose in common bean cultivars colleted in the state of Minas Gerais �?? Brasil. Annual Report of the Bean Improvement Cooperative, 53, 224-225.

Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155(2), 945-959.

Raeder, U., & Broda, P. (1985). Rapid preparation of DNA from filamentous fungi. Letters in Applied Microbiology, 1(1), 17-20. https://doi.org/10.1111/j.1472-765X.1985.tb01479.x

Rava, C. A., Purchio, A., & Sartorato, A. (1994). Caracterização de patótipos de Colletotrichum lindemuthianum que ocorrem em algumas regiões produtoras de feijoeiro comum. Fitopatologia Brasileira, 19(2), 167-172.

Roca, M. G., Davide, L. C., Mendes-Costa, M. C., & Wheals, A. E. (2003). Conidial anastomosis tubes in Colletotrichum. Fungal Genetics and Biology, 40(2), 138-145. http://dx.doi.org/10.1016/s1087-1845(03)00088-4

Rodríguez-Guerra, R., Ramírez-Rueda, M. T., Vega, O. M., & Simpson, J. (2003). Variation in genotype, pathotype and anastomosis groups of Colletotrichum lindemuthianum isolates from México. Plant Pathology, 52(2), 228-235. https://doi.org/10.1046/j.1365-3059.2003.00808.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

Santos, J., Antunes, I. F., Rey, M. S., & Rossetto, E. A. (2008). Virulência das raças 65, 73 e 81 de Colletotrichum lindemuthianum (Sacc. & Magn.) Scrib. e determinação de fontes de resistência em Phaseolus vulgaris L. Agrociência, 14(3), 115-124. https://doi.org/10.18539/cast.v14i3.1940

Schoch, C. L., Seifert, K. A., Huhndorf, S., Robert, V., Levesque, C. A., & Wen, C. (2012). Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proceedings of the National Academy of Science, 109(16), 6241-6246. https://doi.org/10.1073/pnas.1117018109

Sharma, P. N., Padder, B. A., Sharma, O. P., Pathania, A., & Sharma, P. (2007). Pathological and molecular diversity in Colletotrichum lindemuthianum (bean anthracnose) across Himachal Pradesh, a north-western Himalayan State of India. Australian Plant Pathology, 36, 191-197. https://doi.org/10.1071/AP07013

Sherriff, C., Whelan, M. J., Arnold, G. M., Lafay, J. F., Brygoo, Y., & Bailey, J. A. (1994). Ribosomal DNA sequence analysis reveals new species groupings in the genus Colletotrichum. Experimental Mycology, 18(2), 121-138. https://doi.org/10.1006/emyc.1994.1014

Sicard, D., Michalakis, Y., Dron, M., & Neema, C. (1997). Genetic diversity and pathogenic variation of Colletotrichum lindemuthianum in the three centers of diversity of its host, Phaseolus vulgaris. Phytopathology, 87(8), 807- 813. https://doi.org/10.1094/PHYTO.1997.87.8.807

Sileshi, G. W., Mafongoya, P. L., Akinnifesi, F. K., Phiri, E., Chirwa, P., Beedy, T., Makumba, W., Nyamadzawo, G., Njoloma, J., Wuta, M., Nyamugafata, P., & Jiri, O. (2014). Fertilizer trees. In Encyclopedia of Agriculture and Food Systems (pp. 222-234) San Diego: Elsevier.

Silva, K. J. D., Souza, E. A., & Ishikawa, F. H. (2007). Characterization of Colletotrichum lindemuthianum isolates from the State of Minas Gerais, Brazil. Phytopathology, 155(4), 241-247. https://doi.org/10.1111/j.1439-0434.2007.01226.x

Sreenivasaprasad, S., Mills, P. R., Meehan, B. M., & Brown, A. E. (1996). Phylogeny and systematics of 18 Colletotrichum species based on ribosomal DNA spacer sequences. Genome, 39(3), 499-512. https://doi.org/10.1139/g96-064

Talamini, V., Souza, E. A., Pozza, E. A., Silva, G. F., Ishikawa, F. H., & Camargo Júnior, O. A. (2006). Genetic divergence among and within Colletotrichum lindemuthianum races assessed by RAPD. Fitopatologia Brasileira, 31(6), 545-550. https://doi.org/10.1590/S0100-41582006000600002

Thomazella, C., Gonçalves-Vidigal, M. C., Vidigal Filho, P. S., Nunes, W. M. C., & Vida, J. B. (2002b). Characterization of Colletotrichum lindemuthianum races in Paraná state, Brazil. Crop Breeding and Applied Biotechnology, 2(1), 55-60. https://doi.org/10.12702/1984-7033.v02n01a08

Thomazella, C., Gonçalves-Vidigal, M. C., Vidigal Filho, P. S., Sakiyama, N. S., Barelli, M. A. A., & Silvério, L. (2002a). Genetic variability among Colletotrichum lindemuthianum races using RAPD markers. Annual Report of the Bean Improvement Cooperative, 45, 44-45.

Torres, R. A., Ganal, M., & Hemleben, V. (1990). GC balance in the internal transcribed spacers ITS1 and ITS2 of nuclear ribossomal RNA genes. Journal of Molecular Evolution, 30, 170-181. https://doi.org/10.1007/BF02099943

Uchôa, E. B., Gonçalves-Vidigal, M. C., Souza, M. C. M., Vidigal Filho, P. S., Castro, S. A. L., & Poletine, J. P. (2015). New races of Colletotrichum lindemuthianum in common bean from Parana state, Brazil. Annual Report of the Bean Improvement Cooperative, 58, 41-42.

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.

Published
2020-11-27
How to Cite
Coêlho, M., Gonçalves Vidigal, M. C., Vidigal Filho, P. S., Franzon, R. C., & Martins, V. S. R. (2020). Genetic diversity of Colletotrichum lindemuthianum races based on ITS-rDNA regions. Agronomy Science and Biotechnology, 6, 1-18. https://doi.org/10.33158/ASB.r112.v6.2020

Most read articles by the same author(s)