Abstract
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.
Similar content being viewed by others
References
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.
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.
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.
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.
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.
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).
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.
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).
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.
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.
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.
Espindula, L. F., Minella, E., & Delatorre, C. A. (2009). Low-P tolerance mechanisms and differential gene expression. Pesquisa Agropecuária Brasileira, 44, 1100–1105.
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.
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.
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.
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.
Heath, M. C. (1981). Resistance of plants to rust infection. Phytopathology, 71, 971–974.
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.
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.
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.
Johnson, R. (1984). A critical analysis of durable resistance. Annual Review of Phytopathology, 22, 309–330.
Kliebenstein, D. J., & Rowe, H. C. (2009). Anti-rust antitrust. Plant Science, 323, 1301–1302.
Kohli, M. M. (1989). Taller sobre la fusariosis de la espiga en América del Sur. México: CIMMYT.
Kohli, M. M., & Skovmand, B. (1997). Wheat varieties of South America. Names, parentage, pedigrees, and origin. Mexico: CIMMYT.
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.
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.
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.
Long, D. L., & Kolmer, J. A. (1989). A North American system of nomenclature for Puccinia recondita f. sp. tritici. Phythopathology, 79, 525–529.
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.
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.
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.
McIntosh, R. A., Wellings, C. R., & Park, R. F. (1995). Wheat rusts: an atlas of resistance genes. East Melbourne: CSIRO.
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.
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.
Montesanto, M., Brader, G., & Palva, E. T. (2003). Pathogen derived elicitors: searching for receptors in plants. Molecular Plant Pathology, 4, 73–79.
Niederhauser, J. S., Cervantes, J., & Servin, L. (1954). Late blight in Mexico and its implications. Phytopathology, 44, 406–408.
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.
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.
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.
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.
Rajaram S, & Campos, A. (1974). Epidemiology of wheat rusts in the Western Hemisphere. CIMMYT Research Bulletin No. 27, México, DF.
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.
Ribeiro do Vale, F. X., Parlevliet, J. E., & Zambolim, L. (2001). Concepts in plant disease resistance. Fitopatologia Brasileira, 26, 577–589.
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.184
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.
Rubiales, D., & Niks, R. E. (1992). Low appressorium formation by rust fungi on Hordeum chilense lines. Phytopathology, 82, 1007–1012.
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.
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.
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.
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.
Sillero, J. C., & Rubiales, D. (2002). Histological characterization of resistance to Uromyces viciae-fabae in faba bean. Phytopathology, 92, 294–299.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Acknowledgments
The authors thank the Brazilian Federal Agency for the Coordination of the Improvement of Higher Education Personnel (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, CAPES) for a scholarship to the first author and the Brazilian National Council for Scientific Research and Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq) and the Foundation for Research Support of Rio Grande do Sul State (Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul, FAPERGS) for financial support.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wesp-Guterres, C., Martinelli, J.A., Graichen, F.A.S. et al. Histopathology of durable adult plant resistance to leaf rust in the Brazilian wheat variety Toropi. Eur J Plant Pathol 137, 181–196 (2013). https://doi.org/10.1007/s10658-013-0232-5
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-013-0232-5