Phenotypical and genotypical characterization of Pyrenophora tritici-repentis races in Brazil

Abstract

Tan spot, caused by Pyrenophora tritici-repentis, is one of the major wheat diseases in southern Brazil as well as in the wheat production areas of several other countries. The fungal isolates have been classified into eight races according to the production of three fungal necrotrophic effectors. The knowledge about the pathogen population structure is essential for disease control strategies, but such information is lacking in Brazil. The aim of this study was to determine the P. tritici-repentis race structure of Brazilian isolates using, for the first time, biological and molecular techniques. P. tritici-repentis isolates were characterized for their virulence on a set of wheat genotypes, and for the presence of ToxA and ToxB gene. The results from the PCR amplification with the gene specific primers showed that all Brazilian P. tritici-repentis isolates carried ToxA, but no ToxB is present. Race typing on the set of wheat genotypes indicate 65% of the isolates were race 2 while 35% were race 1. This is the first study on the P. tritici-repentis race structure in Brazil and the information will be useful to the local wheat breeders who aim to improve tan spot resistance in wheat cultivars.

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References

  1. Ali, S., & Francl, L. J. (2002). A new race of Pyrenophora tritici-repentis from Brazil. Plant Disease, 86(9), 1050.

    Article  CAS  PubMed  Google Scholar 

  2. Ali, S., & Francl, L. J. (2003). Population race structure of Pyrenophora tritici-repentis prevalent on wheat and noncereal grasses in the Great Plains. Plant Disease, 87(4), 418–422.

    Article  PubMed  Google Scholar 

  3. Ali, S., Gurung, S., & Adhikari, T. B. (2010). Identification and characterization of novel isolates of Pyrenophora tritici-repentis from Arkansas. Plant Disease, 94(2), 229–235.

    Article  CAS  PubMed  Google Scholar 

  4. Ameen, G., Kariyawasam, G., Shi, G., Friesen, T. L., Faris, J. D., Ali, S., Rasmussen, J. B., & Liu, Z. (2017). Molecular manipulation of the mating-type system and development of a new approach for characterizing pathogen virulence in Pyrenophora tritici-repentis. Fungal Genetics and Biology, 109, 16–25. https://doi.org/10.1016/j.fgb.2017.10.004.

    Article  CAS  PubMed  Google Scholar 

  5. Andrie, R. M., Pandelova, I., & Ciuffetti, L. M. (2007). A combination of phenotypic and genotypic characterization strengthens Pyrenophora tritici-repentis race identification. Phytopathology, 97(6), 694–701.

    Article  CAS  PubMed  Google Scholar 

  6. Antoni, E. A., Rybak, K., Tucker, M. P., Hane, J. K., Solomon, P. S., Drenth, A., Shankar, M., & Oliver, R. P. (2010). Ubiquity of ToxA and absence of ToxB in australian populations of Pyrenophora tritici-repentis. Australasian Plant Pathology, 39, 63–68.

    Article  CAS  Google Scholar 

  7. Barnett, H. L., & Hunter, B. B. (1972). Illustred fungi of imperfect fungi. Minneapolis: Burgess Publishing Company.

    Google Scholar 

  8. Benslimane, H. (2018). Virulence phenotyping and molecular characterization of a new virulence. Plant Pathology Journal, 34(2), 139–142.

    CAS  PubMed  Google Scholar 

  9. Bertagnolli, V. V., Bertagnolli Neto, P., Riva, G., Corá, J., & Deuner, C. C. (2017a). Caracterização fenotípica de raças de Drechslera tritici-repentis. 50o Congresso Brasileiro de Fitopatologia. http://www.cbfito.com.br/cd/Resumos/Resumo50CBFito_0639.pdf. Acessed 25 June 2018.

  10. Bertagnolli, V. V., Deuner, C. C., Frizon, P., & Ghissi, V. C. (2017b). Water potential and time of Pyrenophora tritici-repentis inoculation in wheat seeds. Semina: Ciências Agrárias, 38(4), 1681–1690.

    Google Scholar 

  11. Bhathal, J. S., Loughman, R., & Speijers, J. (2003). Yield reduction in wheat in relation to leaf disease from yellow (tan) spot and septoria nodorum blotch. European Journal of Plant Pathology, 109, 435–443.

    Article  CAS  Google Scholar 

  12. BRASIL. (2008a). Ministério da Agricultura, Pecuária e Abastecimento. Instrução Normativa n° 3, de 14 de outubro de 2008. Brasília, DF: Diário Oficial [da] República Federativa do Brasil.

  13. BRASIL. (2008b). Ministério da Agricultura, Pecuária e Abastecimento. Instrução Normativa no 58, de 19 de novembro de 2008. Brasília, DF: Diário Oficial [da] República Federativa do Brasil.

  14. Ciuffetti, L. M., Tuori, R. P., & Gaventa, M. (1997). A single gene encodes a selective toxin causal to the development of tan spot on wheat. Plant Cell, 9, 135–144.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. dos Santos, A. M. P. V., Matsumura, A. T. S., & Van Der Sand, S. T. (2002). Intraspecific genetic diversity of Drechslera tritici-repentis as detected by random amplified polymorphic DNA analysis. Genetics and Molecular Biology, 25(2), 243–250. https://doi.org/10.1590/S1415-47572002000200020.

    Article  Google Scholar 

  16. Effertz, R. J., Anderson, J. A., & Francl, L. J. (2001). Restriction fragment length polymorphism mapping of resistance to two races of Pyrenophora tritici-repentis in adult and seedling wheat. Phytopathology, 91, 572–578.

    Article  CAS  PubMed  Google Scholar 

  17. Effertz, R. J., Meinhardt, S. W., Anderson, J. A., Jordahl, J. G., & Francl, L. J. (2002). Identification of a chlorosis-inducing toxin from Pyrenophora tritici-repentis and the chromosomal location of an insensitivity locus in wheat. Phytopathology, 92, 527–533.

    Article  CAS  PubMed  Google Scholar 

  18. Faris, J. D., & Friesen, T. L. (2005). Identification of quantitative trait loci for race-nonspecific resistance to tan spot in wheat. Theoretical and Applied Genetics, 111, 386–392.

    Article  CAS  PubMed  Google Scholar 

  19. Faris, J. D., Anderson, J. A., Francl, L. J., & Jordahl, J. G. (1996). Cromossomal location of a gene conditioning insensivity in wheat to a necrosis-inducing culture filtrate from Pyrenophora tritici-repentis. Phytopathology, 86(5), 459–463.

    Article  CAS  Google Scholar 

  20. Faris, J. D., Liu, Z., & Xu, S. S. (2013). Genetics of tan spot resistance in wheat. Theoretical and Applied Genetics, 126(9), 2197–2217.

    Article  CAS  PubMed  Google Scholar 

  21. Friesen, T. L., & Faris, J. D. (2004). Molecular mapping of resistance to Pyrenophora tritici-repentis race 5 and sensitivity to Ptr ToxB in wheat. Theoretical and Applied Genetics, 109, 464–471.

    Article  CAS  PubMed  Google Scholar 

  22. Friesen, T. L., Ali, S., Klein, K. K., & Rasmussen, J. B. (2005). Population genetic analysis of a global collection of Pyrenophora tritici repentis, causal agent of tan spot of wheat. Phytopathology, 95(10), 1144–1150.

    Article  CAS  PubMed  Google Scholar 

  23. Gomes, D. P., Rocha, V. S., Pereira, O. L., & de Souza, M. A. (2011). Sanidade de sementes de trigo provenientes do programa de melhoramento da UFV. In: XIV encontro latino americano de iniciação científica e X Encontro latino americano de pós-graduação. Anais. São José dos Campos. http://www.inicepg.univap.br/cd/INIC_2011/anais/arquivos/RE_0279_0277_01.pdf>. Acessed 20 june 2018.

  24. Hosford, R. M., Jr. (1971). A form of Pyrenophora trichostoma pathogenic to wheat and other grasses. Phytopathology, 61, 28–32.

    Article  Google Scholar 

  25. Jørgensen, L. N., & Olsen, L. V. (2007). Control of tan spot (Drechslera tritici-repentis) using cultivar resistance, tillage methods and fungicides. Crop Protection, 26, 1606–1616.

    Article  CAS  Google Scholar 

  26. Kariyawasam, G. K., Carter, A. H., Rasmussen, J. B., Faris, J., Xu, S. S., Mergoum, M., & Liu, Z. (2016). Genetic relationships between race-nonspecific and race-specific interactions in the wheat–Pyrenophora tritici-repentis pathosystem. Theoretical and Applied Genetics, 129, 897–908.

    Article  CAS  PubMed  Google Scholar 

  27. Kenny, P., Deák, Z., Csôsz, M., Purnhauser, L., & Vass, I. (2011). Characterization and early detection of tan spot disease in wheat in vivo with chlorophyll fluorescence imaging. Acta Biologica Szegediensis, 55(1), 87–90.

    Google Scholar 

  28. Kobayasti, L., & Pires, A. P. (2011). Levantamento de fungos em sementes de trigo. Pesquisa Agropecuária Tropical, 41(4), 572–578.

    Article  Google Scholar 

  29. Krupinsky, J. M. (1992). Grass hosts of Pyrenophora tritici-repentis. Plant Disease, 76(1), 92–95.

    Article  Google Scholar 

  30. Lamari, L., & Bernier, C. C. (1989a). Evalution of wheat lines and cultivars to tan spot (pyrenophora tritici-repentis) based on lesion type. Canadian Journal of Plant Pathology, 11, 49–56.

    Article  Google Scholar 

  31. Lamari, L., & Bernier, C. C. (1989b). Virulence of isolates of Pyrenophora tritici-repentis on 11 wheat cultivars and cytology of the differential host reactions. Canadian Journal of Plant Pathology, 11, 284–290.

    Article  Google Scholar 

  32. Lamari, L., & Bernier, C. C. (1989c). Toxin of Pyrenophora tritici-repentis: Host-specificity, significance in disease. and inheritance of host reaction. Phytopathology, 79, 740–744.

    CAS  Google Scholar 

  33. Lamari, L., Sayoud, R., Boulif, M., & Bernier, C. C. (1995). Identification of a new race of Pyrenophora tritici-repentis: Implications for the current pathotype classification system. Canadian Journal of Plant Pathology, 17, 312–318.

    Article  Google Scholar 

  34. Lamari, L., Strelkov, S., Yahyaoui, A., Orabi, J., & Smith, R. B. (2003). The identification of two new races of Pyrenophora tritici-repentis from the host center of diversity confirms a one-to-one relationship in tan spot of wheat. Phytopathology, 93, 391–396.

    Article  CAS  PubMed  Google Scholar 

  35. Leisová, L., Hanzalová, A., & Kucera, L. (2008). Genetic diversity of Pyrenophora tritici-repentis isolates as revealed by AFLP analysis. Journal of Plant Pathology, 90(2), 233–245.

    Google Scholar 

  36. Lepoint, P., Renard, M.-E., Legrève, A., Duveiller, E., & Maraite, H. (2010). Genetic diversity of the mating type and toxin production genes in Pyrenophora tritici-repentis. Phytopathology, 100(5), 474–483.

    Article  CAS  PubMed  Google Scholar 

  37. Liu, Z., El-Basyoni, I., Kariyawasam, G., Zhang, G., Fritz, A., Hansen, J., Marais, F., Friskop, A., Chao, S., Akhunov, E., & Baenziger, P. S. (2015). Evaluation and association mapping of resistance to tan spot and Stagonospora nodorum blotch in adapted winter wheat germplasm. Plant Disease, 99, 1333–1341.

    Article  CAS  PubMed  Google Scholar 

  38. Manning, V. A., Andrie, R. M., Trippe, A. F., & Ciuffetti, L. M. (2004). Ptr ToxA requires multiple motifs for complete activity. Molecular Plant-Microbe Interactions, 17, 491–501.

    Article  CAS  PubMed  Google Scholar 

  39. Manning, V. A., Chu, A. L., Steeves, J. E., Wolpert, T. J., & Ciuffetti, L. M. (2009). A host selective toxin of Pyrenophora tritici-repentis, Ptr ToxA, induces photosystem changes and reactive oxygen species accumulation in sensitive wheat. Molecular Plant-Microbe Interactions, 22, 665–676.

    Article  CAS  PubMed  Google Scholar 

  40. Martinez, J. P., Oesch, N. W., & Ciuffetti, L. M. (2004). Characterization of the multiple-copy host-selective toxin gene, ToxB, in pathogenic and nonpathogenic isolates of Pyrenophora tritici-repentis. Molecular Plant-Microbe Interactions, 17(5), 467–474.

  41. Mehta, Y. R. (1993). Manejo integrado de enfermidades del trigo. Santa Cruz de la Sierra: Imprenta Landivar S.R.L.

  42. Misra, A. P., & Singh, R. A. (1972). Pathogenic differences among three isolates of Helminthosporium tritici-repentis and the performance of wheat varieties against them. Indian Phytopathology, 25, 350–353.

    Google Scholar 

  43. Momeni, H., Aboukhaddour, R., Javan-Nikkhah, M., Razavi, M., Naghavi, M. R., Akhavan, A., & Strelkov, S. E. (2014). Race identification of Pyrenophora tritici-repentis in Iran. Journal of Plant Pathology, 96(2), 287–294.

    Google Scholar 

  44. Moreno, M. V., Stenglein, S., & Perelló, A. E. (2015). Distribution of races and Tox genes in Pyrenophora tritici-repentis isolates from wheat in Argentina. Tropical plant pathology, 40, 141–146.

    Article  Google Scholar 

  45. Oralaza, N. P., Lamari, L., & Ballance, G. M. (1995). Evidence of a host-specific chlorosis toxin from Pyrenophora tritici-repentis, causal agent of tan spot of wheat. Molecular Plant-Microbe Interactions, 3, 221–224.

    Google Scholar 

  46. Raymond, P. J., Bockus, W. W., & Norman, B. L. (1985). Tan spot of winter wheat: Procedures to determine host response. Phytopathology, 75, 686–690.

    Article  Google Scholar 

  47. Santana, F. M., Clebsch, C. C., & Friesen, T. L. (2008). Caracterização de raças de Pyrenophora tritici-repentis, agente etiológico da mancha-amarela do trigo, no sul do Brasil. Passo Fundo: Embrapa Trigo. (Boletim de Pesquisa e Desenvolvimento Online, 60). http://www.cnpt.embrapa.br/biblio/bp/p_bp60.htm. Acessed 05 june 2018.

  48. Strelkov, S. E., Lamari, L., Ballance, G. M., & Orolaza, N. P. (1998). Isolation and mode of action of Ptr chlorosis toxin from Pyrenophora tritici-repentis. In: K. Kohmoto, & O. C. Yoder (Eds.), Molecular Genetics of Host-Specific Toxins in Plant Disease (pp. 137–138). Tottori: Kluwer Academic Publishers.

  49. Strelkov, S. E., Lamari, L., & Ballance, G. M. (1999). Characterization of a host-specific protein toxin (Ptr ToxB) from Pyrenophora tritici-repentis. Molecular Plant-Microbe Interactions, 2, 728–732.

    Article  Google Scholar 

  50. Strelkov, S. E., Lamari, L., Sayoud, R., & Smith, R. B. (2002). Comparative virulence of chlorosis-inducing races of Pyrenophora tritici-repentis. Canadian Journal of Plant Pathology, 24, 29–35.

    Article  Google Scholar 

  51. Tomas, A., Feng, G. H., Reeck, G. R., Bockus, W. W., & Leach, J. E. (1990). Purification of a cultivar-specific toxin from Pyrenophora tritici-repentis, causal agent of tan spot of wheat. Molecular Plant-Microbe Interactions, 3, 221–224.

    Article  CAS  Google Scholar 

  52. Tuori, R. P., Wolpert, T. J., & Ciuffetti, L. M. (1995). Purification and immunological characterization of toxin components from cultures of Pyrenophora tritici-repentis. Molecular Plant-Microbe Interactions, 8(1), 41–48.

    Article  CAS  PubMed  Google Scholar 

  53. Wiese, M. V. (1987). Compendium of wheat diseases. 2th ed. St. Paul. APS Press.

  54. Zadocks, J. C., Chang, T. T., & Konzak, C. F. (1974). A decimal code for the growth stages of cereals. Weed Research, 14, 415–421.

    Article  Google Scholar 

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Acknowledgments

We are thankful to Passo Fundo University and North Dakota State University for the facility, Capes (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for financial support, Biotrigo Genética Ltda. for the networking support, Dr. Flávio Martins Santana and his team from Embrapa Trigo for the concession of some isolates, and MSc. Augusto Bittencourt Vieira for helping with the English review.

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Correspondence to Victória Vieira Bertagnolli.

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Supplementary Figure 1
figure6

BLAST search. A) Results of blast search considering the sequence of S30 isolate (accession MK490983). B). Sequence of Pyrenophora chaetomioides presenting 100% of identities with S30 isolate sequence. (PNG 695 kb)

Supplementary Figure 2
figure7

BLAST search. A) Results of blast search considering the sequence of S31 isolate (accession MK490984). B). Sequence of Drechslera avenae presenting 99% of identities with S31 isolate sequence. (PNG 642 kb)

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Bertagnolli, V.V., Ferreira, J.R., Liu, Z. et al. Phenotypical and genotypical characterization of Pyrenophora tritici-repentis races in Brazil. Eur J Plant Pathol 154, 995–1007 (2019). https://doi.org/10.1007/s10658-019-01720-3

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Keywords

  • Differential set
  • Isolates
  • Tan spot
  • Toxins
  • Wheat