European Journal of Plant Pathology

, Volume 137, Issue 1, pp 181–196 | Cite as

Histopathology of durable adult plant resistance to leaf rust in the Brazilian wheat variety Toropi

  • Caroline Wesp-Guterres
  • José Antônio Martinelli
  • Felipe André Sganzerla Graichen
  • Márcia Soares Chaves


Leaf rust, caused by the fungus Puccinia triticina is a major disease of wheat (Triticum aestivum) worldwide. This disease is prevalent in southern South America where the environmental conditions and high genetic variability of P. triticina favour epidemics. The primary means of controlling pathogenic P. triticina races has been through using wheat varieties containing race-specific resistance genes. The defence mechanisms involved in durable race non-specific resistance to P. triticina are probably distinct from those involved in non-durable race-specific resistance. We investigated the histological components of resistance to P. triticina present in three wheat genotypes: the race non-specific resistant Brazilian variety Toropi; the race-specific resistant line RL6010 Lr9; and the susceptible Brazilian variety BRS 194. Plants of these three genotypes were inoculated with P. triticina race MFP and tissue samples excised from flag leaves at various times after inoculation to assess the number of infective structures, frequency of cell death and the accumulation of autofluorescent cells and hydrogen peroxide. The genotypes showed different resistance mechanisms active at different times during the infection process. Our results for Toropi indicate that there was a reduction in the extent of formation of stomatal appressoria and all subsequent structures. During attempted penetration we also observed the production of autofluorescent compounds and late cell death, but not peroxide formation. This non-specific resistance to P. triticina involves both pre-haustorial and post-haustorial mechanisms which may be responsible for maintaining the low disease severity observed in this variety even under high inoculum pressure.


Race non-specific resistance mechanisms Post-haustorial resistance Pre-haustorial resistance Puccinia triticina 


  1. Anker, C. C., & Niks, R. E. (2001). Prehaustorial resistance to the wheat leaf rust fungus, Puccinia triticina in Triticum monococcum (s.s.). Euphytica, 117, 209–215.CrossRefGoogle Scholar
  2. Ayliffe, M., Jin, Y., Kang, Z., Persson, M., Steffenson, B., Wang, S., et al. (2011). Determining the basis of nonhost resistance in rice to cereal rusts. Euphytica, 179, 33–40.CrossRefGoogle Scholar
  3. Barcellos, A. L., Roelfs, A. P., & Moraes-Fernandes, M. I. B. (2000). Inheritance of adult plant leaf rust resistance in the Brazilian wheat cultivar Toropi. Plant Disease, 84, 90–93.CrossRefGoogle Scholar
  4. Bender, C. M., Pretorius, Z. A., Kloppers, F. J., & Spies, J. J. (2000). Histopathology of leaf rust infection and development in wheat genotypes containing Lr12 and Lr13. Journal of Phytopathology, 148, 65–76.CrossRefGoogle Scholar
  5. Bozkurt, T. O., Mcgrann, G. R. D., Maccormack, R., Boyd, L. A., & Akkaya, M. S. (2010). Cellular and transcriptional responses of wheat during compatible and incompatible race-specific interactions with Puccinia striiformis f. sp. tritici. Molecular Plant Pathology, 11, 625–640.PubMedGoogle Scholar
  6. Brammer, S. P., Worland, A., Barcellos, A. & Fernandes, M. I. B de M. (1998). Monosomic analysis of adult-plant resistance to lesf rust in the Brazilian wheat cultivar Toropi. (Paper presented at the 9th International wheat genetics symposium, Saskatoon).Google Scholar
  7. Broers, L. H. M., & López-Atilano, R. M. (1996). Effect of quantitative resistance in wheat on the development of Puccinia striiformis during early stages of infection. Plant Disease, 80, 1265–1268.CrossRefGoogle Scholar
  8. Caldwell, R.M. (1968). Breeding for general and/or specific plant disease resistance. In: K.W. Finlay and K.W. Shepherd (Eds.). (Paper presented at the 3rd. International Wheat Genetic Symposium, Canberra).Google Scholar
  9. Dakouri, A., McCallum, B. D., Walichnowski, A. Z., & Cloutier, S. (2010). Fine-mapping of the leaf rust Lr34 locus in Triticum aestivum (L.) and characterization of large germplasm collections support the ABC transporter as essential for gene function. Theoretical and Applied Genetics, 121, 373–384.PubMedCrossRefGoogle Scholar
  10. Dyck, P. L. (1987). The association of a gene for leaf rust resistance with chromosome 7D suppressor of stem rust resistance in common wheat. Genome, 29, 467–469.Google Scholar
  11. Elahinia, S. A. (2008). Microscopic study on expression of Yr-18 gene related to adult plant resistance in a near-isogenic line of spring wheat (Triticum aestivum L.) to the Stripe Rust (Puccinia striiformis f. sp. tritici). Journal of Agriculture. Science and Technology, 10, 359–369.Google Scholar
  12. Espindula, L. F., Minella, E., & Delatorre, C. A. (2009). Low-P tolerance mechanisms and differential gene expression. Pesquisa Agropecuária Brasileira, 44, 1100–1105.CrossRefGoogle Scholar
  13. Fujita, M., Fujita, Y., Noutoshi, Y., Takahashi, F., Narusaka, Y., Yamaguchi-Shinozaki, K., et al. (2006). Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Current Opinion on Plant Biology, 9, 436–442.CrossRefGoogle Scholar
  14. German, S., Barcellos, A., Chaves, M., Kohli, M., Campos, B., & de Viedma, L. (2007). The situation of common wheat rusts in the Southern Cone of America and perspectives for control. Australian Journal of Agricultural Research, 58, 620–630.CrossRefGoogle Scholar
  15. Glombitza, S., Dubuis, P. H., Thulke, O., Welzl, G., Bovet, L., Götz, M., et al. (2004). Crosstalk and differential response to abiotic and biotic stressors reflected at the transcriptional level of effector genes from secondary metabolism. Plant Molecular Biology, 54, 817–835.PubMedCrossRefGoogle Scholar
  16. Graichen, F. A. S., Martinelli, J. A., Wesp, C. L., Federizzi, L. C., & Chaves, M. S. (2011). Epidemiological and histological components of crown rust resistance in oat genotypes. European Journal of Plant Pathology, 131, 497–510.CrossRefGoogle Scholar
  17. Heath, M. C. (1981). Resistance of plants to rust infection. Phytopathology, 71, 971–974.CrossRefGoogle Scholar
  18. Huerta-Espino, J., Singh, R. P., German, S., Mccallum, B. D., Park, R. F., Chen, W. Q., et al. (2011). Global status of wheat leaf rust caused by Puccinia triticina. Euphytica, 179, 143–160.CrossRefGoogle Scholar
  19. Jagger, L. J., Newell, C., Berry, S. T., MacCormack, R., & Boyd, L. A. (2011). Histopathology provides a phenotype by which to characterize stripe rust resistance genes in wheat. Plant Pathology, 60, 640–648.CrossRefGoogle Scholar
  20. Jiang, X. L., & Kang, Z. S. (2010). Ultrastructural changes in the interaction between Puccinia striiformis and wheat cultivar with slow-rusting resistance. Agricultural Sciences in China, 9, 64–70.Google Scholar
  21. Johnson, R. (1984). A critical analysis of durable resistance. Annual Review of Phytopathology, 22, 309–330.CrossRefGoogle Scholar
  22. Kliebenstein, D. J., & Rowe, H. C. (2009). Anti-rust antitrust. Plant Science, 323, 1301–1302.Google Scholar
  23. Kohli, M. M. (1989). Taller sobre la fusariosis de la espiga en América del Sur. México: CIMMYT.Google Scholar
  24. Kohli, M. M., & Skovmand, B. (1997). Wheat varieties of South America. Names, parentage, pedigrees, and origin. Mexico: CIMMYT.Google Scholar
  25. Kowalska, A., & Niks, R. E. (1999). Histology of quantitative resistance in flax to the flax rust fungus (Melampsora lini). Canadian Journal of Plant Pathology, 21, 354–360.CrossRefGoogle Scholar
  26. Krattinger, S. G., Lagudah, E. S., Spielmeyer, W., Singh, R. P., Huerta-Espino, J., McFadden, H., et al. (2009). A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science, 323, 1360–1363.PubMedCrossRefGoogle Scholar
  27. Lipka, V., Dittgen, J., Bednarek, P., Bhat, R., Wiermer, M., Stein, M., et al. (2005). Pre-and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science, 310, 1180–1183.PubMedCrossRefGoogle Scholar
  28. Long, D. L., & Kolmer, J. A. (1989). A North American system of nomenclature for Puccinia recondita f. sp. tritici. Phythopathology, 79, 525–529.CrossRefGoogle Scholar
  29. Manickavelu, A., Kawaura, K., Oishi, K., Shin-I, T., Kohara, Y., Yahiaoui, N., et al. (2010). Comparative gene expression analysis of susceptible and resistant near-isogenic lines common wheat infected by Puccinia triticina. DNA Research, 17, 211–222.PubMedCrossRefGoogle Scholar
  30. Marone, D., Del Olmo, A. I., Laido, G., Sillero, J. C., Emeran, A. A., Russo, M. A., et al. (2009). Genetic analysis of durable resistance against leaf rustin durum wheat. Molecular Breeding, 24, 25–39.CrossRefGoogle Scholar
  31. Martínez, F., Niks, R. E., Singh, R. P., & Rubiales, D. (2001). Characterization of Lr46, a gene conferring partial resistance to wheat leaf rust. Hereditas, 135, 111–114.Google Scholar
  32. McIntosh, R. A., Wellings, C. R., & Park, R. F. (1995). Wheat rusts: an atlas of resistance genes. East Melbourne: CSIRO.CrossRefGoogle Scholar
  33. Melichar, J. P. E., Berry, S., Newell, C., Maccormack, R., & Boyd, L. A. (2008). QTL identification and microphenotype characterization of the developmentally regulated yellow rust resistance in the UK wheat cultivar Guardian. Theoretical and Applied Genetics, 117, 391–399.PubMedCrossRefGoogle Scholar
  34. Moldenhauer, J., Pretorius, Z. A., Moerschbacher, B. M., Prins, R., & Van der Westhuizen, A. J. (2008). Histopathology and PR-protein markers provide insight into adult plant resistance to stripe rust of wheat. Molecular Plant Pathology, 9, 137–145.PubMedCrossRefGoogle Scholar
  35. Montesanto, M., Brader, G., & Palva, E. T. (2003). Pathogen derived elicitors: searching for receptors in plants. Molecular Plant Pathology, 4, 73–79.CrossRefGoogle Scholar
  36. Niederhauser, J. S., Cervantes, J., & Servin, L. (1954). Late blight in Mexico and its implications. Phytopathology, 44, 406–408.Google Scholar
  37. Nirmala, J., Drader, T., Chen, X., Steffenson, B., & Kleinhofs, A. (2010). Stem rust spores elicit rapid RPG1 phosphorylation. Molecular Plant-Microbe Interactions, 23, 1635–1642.PubMedCrossRefGoogle Scholar
  38. Orczyka, W., Dmochowska-Bogutaa, M., Czemborb, H. J., & Nadolska-Orczyka, A. (2010). Spatiotemporal patterns of oxidative burst and micronecrosis in resistance of wheat to brown rust infection. Plant Pathology, 59, 567–575.CrossRefGoogle Scholar
  39. Parry, A. L., & Carver, T. L. W. (1986). Relationship between colony development, resistance to penetration and autofluorescence in oats infected with powdery mildew. Transactions of the British Mycological Society, 3, 355–363.CrossRefGoogle Scholar
  40. Prats, E., Llamas, M. J., Jorrin, J., & Rubiales, D. (2007). Constitutive coumarin accumulation on sunflower leaf surface prevents rust germ tube growth and appressorium differentiation. Crop Science, 47, 1119–1124.CrossRefGoogle Scholar
  41. Rajaram S, & Campos, A. (1974). Epidemiology of wheat rusts in the Western Hemisphere. CIMMYT Research Bulletin No. 27, México, DF.Google Scholar
  42. Raman, H., Zhang, K., Cakir, M., Appels, R., Garvin, D. F., Maron, L. G., et al. (2005). Molecular mapping and characterization of ALMT1, the aluminium-tolerance gene of bread wheat (Triticum aestivum L.). Genome, 48, 781–791.PubMedCrossRefGoogle Scholar
  43. Ribeiro do Vale, F. X., Parlevliet, J. E., & Zambolim, L. (2001). Concepts in plant disease resistance. Fitopatologia Brasileira, 26, 577–589.Google Scholar
  44. Rosa, S.B., Mccallum, B. & Brule-Babel, A. (2011). Quantitative resistance conferring durable leaf rust resistance in wheat cultivar Toropi. In: 2011 Technical Workshop—BGRI, 2011, Saint Paul, Minnesota, U.S.A. Poster abstracts. Saint Paul, Minnesota, U.S.A., 2011. p.184Google Scholar
  45. Rojas-Molina, M. D. M., Rubiales, D., Prats, E., & Sillero, J. C. (2007). Effects of phenylpropanoid and energetic metabolism inhibition on faba bean resistance mechanisms to rust. Phytopathology, 97, 60–65.CrossRefGoogle Scholar
  46. Rubiales, D., & Niks, R. E. (1992). Low appressorium formation by rust fungi on Hordeum chilense lines. Phytopathology, 82, 1007–1012.CrossRefGoogle Scholar
  47. Rubiales, D., & Niks, R. E. (1995). Characterization of Lr34, a major gene conferring non-hypersensitive resistance to wheat leaf rust. Plant Disease, 79, 1208–1212.CrossRefGoogle Scholar
  48. Rubiales, D., & Niks, R. E. (2000). Combination of mechanisms of resistance to rust fungi as a strategy to increase durability. (In: C. Royo, M. M. Nachit, N. Di Fonzo & J. L. Araus (Eds.) Durum wheat improvement in Mediterraneous region: new challenges). Options Mediterraneennes, Series A, 40, 333–339.Google Scholar
  49. Ryan, P. R., Raman, H., Gupta, S., Horst, W. J., & Delhaize, E. (2009). A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiology, 149, 340–351.PubMedCrossRefGoogle Scholar
  50. Shetty, N. P., Jørgensen, H. J. L., Jensen, J. D., Collinge, D. B., & Shetty, H. S. (2008). Roles of reactive oxygen species in interactions between plants and pathogens. European Journal of Plant Pathology, 121, 267–280.CrossRefGoogle Scholar
  51. Sillero, J. C., & Rubiales, D. (2002). Histological characterization of resistance to Uromyces viciae-fabae in faba bean. Phytopathology, 92, 294–299.PubMedCrossRefGoogle Scholar
  52. Singh, R. P. (1992). Genetic association of leaf rust resistance gene Lr34 with adult plant resistance to stripe rust in bread wheat. Phytopathology, 82, 835–838.CrossRefGoogle Scholar
  53. Singh, R. P., Huerta-Espino, J., & Rajaram, S. (2000). Achieving near-immunity to leaf and stripe rusts in wheat by combining slow rusting resistance genes. Acta Phytopathlogica Hungarica, 35, 133–139.Google Scholar
  54. Singh, R. P., & Huerta-Spino, J. (2001). Global monitoring of wheat rusts, and assessment of genetic diversity and vulnerability of popular cultivars. Research Highlights of the CIMMYT wheat program, 1999–2000. Mexico: CIMMYT.Google Scholar
  55. Singh, R. P., Huerta-Espino, J., Bhavani, S., Herrera-Foessel, S. A., Singh, D., Singh, P. K., et al. (2011). Race non-specific resistance to rust diseases in CIMMYT spring wheats. Euphytica, 179, 175–186.CrossRefGoogle Scholar
  56. Spielmeyer, W., McIntosh, R. A., Kolmer, J., & Lagudah, E. S. (2005). Powdery mildew resistance and Lr34/Yr18 genes for durable resistance to leaf and stripe rust cosegregate at a locus on the short arm of chromosome 7D of wheat. Theoretical and Applied Genetics, 111, 731–735.PubMedCrossRefGoogle Scholar
  57. Trethowan, R. M., Reynolds, M., Sayre, K., & Ortiz-Monasterio, I. (2005). Adapting wheat cultivars to resource conserving farming practices and human nutritional needs. Annals of Applied Biology, 146, 405–413.CrossRefGoogle Scholar
  58. Thordal-Christensen, H., Zhang, Z. G., Wei, Y. D., & Collinge, D. B. (1997). Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. The Plant Journal, 11, 1187–1194.CrossRefGoogle Scholar
  59. Vaz Patto, M. C., & Rubiales, D. (2009). Identification and characterization of partial resistance to rust in a germoplasm collection of Lathyrus sativus L. Plant Breeding, 128, 495–500.CrossRefGoogle Scholar
  60. Wang, X., Liu, W., Chen, X., Tang, C., Dong, Y., Ma, J., et al. (2010). Differential gene expression in incompatible interactions between wheat and stripe rust fungus revealed by cDNA-AFLP and comparison to compatible interaction. Plant Biology, 10, 1–15.Google Scholar

Copyright information

© KNPV 2013

Authors and Affiliations

  • Caroline Wesp-Guterres
    • 1
  • José Antônio Martinelli
    • 2
  • Felipe André Sganzerla Graichen
    • 3
  • Márcia Soares Chaves
    • 4
  1. 1.Programa de Pós-Graduação em FitotecniaUniversidade Federal do Rio Grande do SulPorto AlegreBrazil
  2. 2.Departamento de FitossanidadeUniversidade Federal do Rio Grande do SulPorto AlegreBrazil
  3. 3.Universidade Estadual de Mato Grosso do SulAquidauanaBrazil
  4. 4.Embrapa—Centro Nacional de Pesquisa de TrigoPasso FundoBrazil

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