Benzothiadiazole and BABA improve resistance to Uromyces pisi (Pers.) Wint. in Pisum sativum L. with an enhancement of enzymatic activities and total phenolic content

Abstract

Benzothiadiazole (BTH) and DL-β-aminobutyric acid (BABA) induced systemic resistance was investigated in susceptible and resistant pea genotypes against Uromyces pisi. Resistance was characterized by reduced infection frequency mainly due to decreases in appressorium formation, stomatal penetration, growth of infection hyphae and haustorium formation. Changes in β-1,3-glucanase, chitinase, phenylalanine ammonia-lyase and peroxidase activities and in total phenolics content, demonstrate that U. pisi resistance is induced by BTH and BABA treatments at early and late stages of the fungal infection process, but that the chemicals operate via different mechanisms. In fact, our study showed that BTH treatment primed the activity of pathogenesis related-proteins such as β-1,3-glucanase, chitinase and peroxidase in both susceptible and resistant genotypes. On the other hand, BABA treatment did not increase the enzymatic activities in the studied genotypes, but significantly increased their total phenolic contents.

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Abbreviations

BABA:

DL-3-amino-n-butanoic (DL-β-aminobutyric) acid

BTH:

Benzo [1,2,3]thiadiazole-7-carbothionic acid-S-methyl ester (Bion®)

PR:

Pathogenesis-related (proteins)

TLC:

Thin layer chromatography

References

  1. Amzalek, E., & Cohen, Y. (2007). Comparative efficacy of systemic acquired resistance-inducing compounds against rust infection in sunflower plants. Phytopathology, 97, 179–186.

    CAS  Article  PubMed  Google Scholar 

  2. Anguelova-Merhar, V. S., Van der Westhuizen, A. J., & Pretorius, Z. A. (2002). Intercellular chitinase and peroxidase activities associated with resistance conferred by gene Lr35 to leaf rust of wheat. Journal of Plant Physiology, 159, 1259–1261.

    Article  Google Scholar 

  3. Barilli, E., Serrano, A., Sillero, J. C., & Rubiales, D. (2009a). Differential response of pea (Pisum sativum) to rusts incited by Uromyces viciae-fabae and U. pisi. Crop Protection, 28, 980–986.

    Article  Google Scholar 

  4. Barilli, E., Sillero, J. C., Fernández-Aparicio, M., & Rubiales, D. (2009b). Identification of resistance to Uromyces pisi in Pisum spp. germplasm. Field Crops Research, 114, 198–203.

    Article  Google Scholar 

  5. Barilli, E., Sillero, J. C., Moral, A., & Rubiales, D. (2009c). Characterization of resistance response of pea (Pisum spp.) against rust (Uromyces pisi (Pers.) Wint.). Plant Breeding, 128, 665–670.

    Article  Google Scholar 

  6. Barilli, E., Sillero, J. C., & Rubiales, D. (2009d). Induction of systemic acquired resistance in pea against rust (Uromyces pisi) by exogenous application of biotic and abiotic inducers. Journal of Phytopathology, 158, 30–34.

    Article  Google Scholar 

  7. Beckers, G. J. M., & Conrath, U. (2007). Priming for stress resistance: from the lab to the field. Current Opinion in Plant Biology, 10, 425–431.

    Article  PubMed  Google Scholar 

  8. Chittoor, J. M., Leach, J. E., & White, F. F. (1997). Differential induction of a peroxidase gene family during infection of rice by Xanthomonas oryzae pv. oryzae. Molecular Plant-Microbe Interactions, 10, 861–871.

    CAS  Article  PubMed  Google Scholar 

  9. Cohen, Y., Niderman, T., Mosinger, E., & Fluhr, R. (1994). Beta-aminobutyric acid induces the accumulation of pathogenesis-related proteins in tomato plants and resistance to late blight infection caused by Phytophthora infestans. Plant Physiology, 105, 351–361.

    Google Scholar 

  10. Cohen, Y., Reuveni, M., & Baider, A. (1999). Local and systemic activity of BABA (DL-β-aminobutyric acid) against Plasmopara viticola in grapevines. European Journal of Plant Pathology, 105, 351–361.

    CAS  Article  Google Scholar 

  11. Dann, E. K., & Deverall, B. J. (2000). Activation of systemic disease resistance in pea by an avirulent bacterium or a benzothiadiazole, but not by a fungal leaf spot pathogen. Plant Pathology, 49, 324–332.

    CAS  Article  Google Scholar 

  12. Emeran, A. A., Sillero, J. C., Niks, R. E., & Rubiales, D. (2005). Infection structures of host-specialized isolates of Uromyces viciae-fabae and of others Uromyces infecting leguminous crops. Plant Disease, 89, 17–22.

    Article  Google Scholar 

  13. Görlach, J., Volrath, S., Knauf-Beiter, G., Hengy, G., Beckhove, U., Kogel, K. H., et al. (1996). Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell, 8, 629–643.

    Article  PubMed  Google Scholar 

  14. Gutiérrez-Mellado, M. C., Edwards, R., Tena, M., Cabello, F., Serghini, K., & Jorrín, J. (1996). The production of coumarin phytoalexins in different plant organs of sunflower (Helianthus annuus L.). Journal of Plant Physiology, 149, 261–266.

    Google Scholar 

  15. Hardham, A. R., Jones, D. A., & Takemoto, D. (2007). Cytoskeleton and cell wall function in penetration resistance. Current Opinion in Plant Biology, 10, 342–348.

    CAS  Article  PubMed  Google Scholar 

  16. Hückelhoven, C. (2007). Cell wall-associated mechanisms of disease resistance and susceptibility. Annual Review of Phytopathology, 45, 101–127.

    Article  PubMed  Google Scholar 

  17. Iriti, M., & Faoro, F. (2003). Benzothiadiazole (BTH) induces cell-death independent resistance in Phaseolus vulgaris against Uromyces appendiculatus. Journal of Phytopathology, 151, 171–180.

    CAS  Article  Google Scholar 

  18. Jiang, S., Park, P., & Ishii, H. (2008). Ultrastructural study on Acibenzolar-S-methyl-induced scab resistance in epidermal pectin layers of Japanese pear leaves. Phytopathology, 98, 585–591.

    CAS  Article  PubMed  Google Scholar 

  19. Kushwaha, C., Chand, R., & Srivastava, C. (2006). Role of aeciospores in outbreaks of pea (Pisum sativum) rust (Uromyces fabae). European Journal of Plant Pathology, 115, 323–330.

    Article  Google Scholar 

  20. Lin, T., Ishizaka, M., & Ishii, H. (2008). Acibenzolar-S-methyl-induced systemic resistance against anthracnose and powdery mildew diseases on cucumber plants without accumulation of phytoalexins. Journal of Phytopathology, 157, 40–50.

    Article  Google Scholar 

  21. Mauch, F., Mauch-Mani, B., & Boller, T. (1988). Antifungal hydrolases in pea tissue, II. Inhibition of fungal growth by combination of chitinase and β-1, 3-glucanase. Plant Physiology, 88, 936–942.

    CAS  Article  PubMed  Google Scholar 

  22. Nicholson, R. L., & Hammerschmidt, R. (1992). Phenolic compounds and their role in disease resistance. Annual Review in Phytopathology, 30, 369–389.

    CAS  Article  Google Scholar 

  23. Prats, E., Rubiales, D., & Jorrín, J. (2002). Acibenzolar-S-methyl-induced resistance to sunflower rust (Puccinia helianthi) is associated with an enhancement of coumarins on foliar surface. Physiological and Molecular Plant Pathology, 60, 155–162.

    CAS  Article  Google Scholar 

  24. Prats, E., Bazzalo, M. E., León, A., & Jorrín, J. V. (2003). Accumulation of soluble phenolics compounds in sunflower capitula correlates with resistance to Sclerotinia sclerotiorum. Euphytica, 132, 321–329.

    CAS  Article  Google Scholar 

  25. Prats, E., Bazzalo, M. E., León, A., & Jorrín, J. V. (2006). Fungitoxic effect of scopolin and related coumarins on Sclerotinia sclerotium. A way to overcome sunflower head rot. Euphytica, 147, 451–460.

    CAS  Article  Google Scholar 

  26. Prats, E., Llamas, M. J., Jorrín, J., & Rubiales, D. (2007). Constitutive coumarin accumulation on sunflower leaf surface prevents rust germ tube growth and appressorium differentiation. Crop Science, 47, 1119–1124.

    Article  Google Scholar 

  27. Radman, R., Saez, R., Bucke, C. H., & Keshavarz, T. (2003). Elicitation of plants and microbial cell systems. Biotechnology and Applied Biochemistry, 37, 91–102.

    CAS  Article  PubMed  Google Scholar 

  28. Roldán-Serrano, A., Luna del Castillo, J., Jorrín-Novo, J., Fernandéz, O., & Gómez Rodríguez, M. V. (2007). Chitinase and peroxidase activities in sunflower hypocotyls: effects of BTH and inoculation with Plasmopara halstedii. Biologia Plantarum, 51, 149–152.

    Article  Google Scholar 

  29. Sillero, J. C., & Rubiales, D. (2002). Histological characterization of resistance to Uromyces viciae-fabae in faba bean. Phytopathology, 92, 294–299.

    CAS  Article  PubMed  Google Scholar 

  30. Slaughter, A. R., Hamiduzzaman, M. M., Gindro, K., Neuhaus, J. M., & Mauch-Mani, B. (2008). Beta-aminobutyric acid-induced resistance in grapevine against downy mildew: involvement of pterostilbene. European Journal of Plant Pathology, 122, 185–195.

    CAS  Article  Google Scholar 

  31. Van Loon, L. C. (1997). Induced resistance in plants and the role of pathogenesis-related proteins. European Journal of Plant Pathology, 103, 753–765.

    Article  Google Scholar 

  32. Van Loon, L. C. (2001). Systemic induced resistance. In A. J. Slusarenko, R. S. S. Fraser, & L. C. van Loon (Eds.), Mechanisms of resistance to plant diseases (pp. 521–574). Dordrecht, The Netherlands: Kluwer Academic Publishers.

    Google Scholar 

  33. Wirth, S. J., & Wolf, G. A. (1990). Dye labelled substrates for the assay and detection of chitinase and lysozyme activity. Journal of Microbiological Methods, 12, 197–205.

    CAS  Article  Google Scholar 

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Acknowledgements

The authors are greatly indebted to the Spanish AGL2008-01239/AGR and Andalusian P07-AGR-02883 projects for financial support and to Ana Moral for technical assistance.

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Correspondence to Eleonora Barilli.

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Barilli, E., Prats, E. & Rubiales, D. Benzothiadiazole and BABA improve resistance to Uromyces pisi (Pers.) Wint. in Pisum sativum L. with an enhancement of enzymatic activities and total phenolic content. Eur J Plant Pathol 128, 483–493 (2010). https://doi.org/10.1007/s10658-010-9678-x

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Keywords

  • Chitinase
  • Glucanase
  • Pea rust
  • Peroxidase
  • Phenolics
  • PR-protein