Properties of vanillyl nonanoate for protection of pepper plants against Phytophthora capsici and Botrytis cinerea

Article
  • 45 Downloads

Abstract

The properties of a capsinoid, vanillyl nonanoate (VNT), to control P. capsici and B. cinerea were studied both in vitro and in vivo. In vitro tests showed that VNT inhibits the germination of P. capsici spores, but not of B. cinerea spores. The antifungal effect was caused by the whole molecule, but not by the precursor molecules corresponding to the aromatic ring and the linear chain. In vivo assays, where plants were sprayed with VNT, then inoculated, showed that the compound protected the plant from the diseases caused by P. capsici and B. cinerea. VNT induced an enhanced expression of several pepper genes related to plant defence, namely CaBGLU1, CaSC1 and CaPAL1. Because VNT had no direct toxic effect against B. cinerea, and it induced pepper defence genes, the observed protection should be due to induced resistance.

Keywords

Capsinoids Capsicum annuum Fungicide Induced resistance 

Abbreviations

NNA

Nonanoic acid

VNT

Vanillyl nonanoate

VOH

Vanillyl alcohol

Notes

Acknowledgements

J.V. is in receipt of a Posdoctoral Contract from Xunta de Galicia.

Compliance with ethical standards

The manuscript complies with the Ethical Rules applicable for this journal.

Conflict of interest

José Díaz has received a research grant from Xunta de Galicia (Grant 10MRU103009PR). Javier Veloso is in receipt of a Posdoctoral Contract from Xunta de Galicia.

References

  1. Aneja, M., Gianfagna, T. J., & Hebbar, P. K. (2005). Trichoderma harzianum produces nonanoic acid, an inhibitor of spore germination and mycelial growth of two cacao pathogens. Physiological and Molecular Plant Pathology, 67, 304–307.CrossRefGoogle Scholar
  2. Aranda, F. J., Villalaín, J., & Gómez-Fernández, J. C. (1995). Capsaicin affects the structure and phase organization of phospholípid membranes. Biochimica et Biophysica Acta(BBA)-Biomembranes, 1234, 225–234.CrossRefGoogle Scholar
  3. Arora, R., Gill, N. S., Chauhan, G., & Rana, A. C. (2011). An overview about versatile molecule capsaicin. International Journal of Pharmaceutical Sciences and Drug Research, 3, 280–286.Google Scholar
  4. Back, K., He, S., Kim, K. U., & Shin, D. H. (1998). Cloning and bacterial expression of sesquiterpene cyclase, a key branch point enzyme for the synthesis of sesquiterpenoid phytoalexin capsidiol in UV challenged leaves of Capsicum annuum. Plant and Cell Physiology, 39, 899–904.CrossRefPubMedGoogle Scholar
  5. Bajpai, V. K., Cho, M. J., & Kang, S. C. (2010). Control of plant pathogenic bacteria of Xanthomonas spp. by the essential oil and extracts of Metasequoia glyptostroboides Miki ex Hu in vitro and in vivo. Journal of Phytopathology, 158, 479–486.CrossRefGoogle Scholar
  6. Billing, J., & Sherman, P. W. (1998). Antimicrobial functions of spices: why some like it hot. The Quarterly Review of Biology, 73, 3–49.CrossRefPubMedGoogle Scholar
  7. Buonaurio, R., Scarponi, L., Ferrara, M., Sidoti, P., & Bertona, A. (2002). Induction of systemic acquired resistance in pepper plants by acibenzolar-S-methyl against bacterial spot disease. European Journal of Plant Pathology, 108, 41–49.CrossRefGoogle Scholar
  8. Ceylan, E., & Fung, D. Y. C. (2004). Antimicrobial activity of spices 1. Journal of Rapid Methods & Automation in Microbiology, 12, 1–55.CrossRefGoogle Scholar
  9. Choi, H. W., & Hwang, K. H. (2015). Molecular and cellular control of cell death and defence signalling in pepper. Planta, 241, 1–27.CrossRefPubMedGoogle Scholar
  10. Cichewicz, R. H., & Thorpe, P. A. (1996). The antimicrobial properties of chile peppers (Capsicum species) and their uses in Mayan medicine. Journal of Ethnopharmacology, 52, 61–70.CrossRefPubMedGoogle Scholar
  11. Conover, W. J. (1980). Practical nonparametric statistics. John Wiley & Sons, Inc.Google Scholar
  12. Díaz, J., ten Have, A., & van Kan, J. A. (2002). The role of ethylene and wound signaling in resistance of tomato to Botrytis cinerea. Plant Physiology, 129, 1341–1351.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Díaz, J., Pomar, F., Bernal, A., & Merino, F. (2004). Peroxidases and the metabolism of capsaicin in Capsicum annuum L. Phytochemistry Reviews, 3, 141–157.CrossRefGoogle Scholar
  14. Doehlemann, G., Berndt, P., & Hahn, M. (2006). Different signaling pathways involving a Gα protein, cAMP and a MAP kinase control germination of Botrytis cinerea conidia. Molecular Microbiology, 59, 821–835.CrossRefPubMedGoogle Scholar
  15. Elad, Y. (2016). Cultural and integrated control of Botrytis spp. In Botrytis–the Fungus, the Pathogen and its Management in Agricultural Systems (pp. 149–164). Springer International Publishing.Google Scholar
  16. Fenn, M. E., & Coffey, M. D. (1984). Studies on the in vitro and in vivo antifungal activity of fosetyl-Al and phosphorous acid. Phytopathology, 74, 606–611.CrossRefGoogle Scholar
  17. Fernández-Ortuño, D., Grabke, A., Li, X., & Schnabel, G. (2015). Independent emergence of resistance to seven chemical classes of fungicides in Botrytis cinerea. Phytopathology, 105, 424–432.CrossRefPubMedGoogle Scholar
  18. Fitzgerald, D. J., Stratford, M., Gasson, M. J., Ueckert, J., Bos, A., & Narbad, A. (2004). Mode of antimicrobial action of vanillin against Escherichia coli, Lactobacillus plantarum and Listeria innocua. Journal of Applied Microbiology, 97, 104–113.CrossRefPubMedGoogle Scholar
  19. 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. The Plant Cell, 8, 629–643.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gozzo, F., & Faoro, F. (2013). Systemic acquired resistance (50 years after discovery): moving from the lab to the field. Journal of Agricultural and Food Chemistry, 61, 12473–12491.CrossRefPubMedGoogle Scholar
  21. He, G. J., Ye, X. L., Mou, X., Chen, Z., & Li, X. G. (2009). Synthesis and antinociceptive activity of capsinoid derivatives. European Journal of Medicinal Chemistry, 44, 3345–3349.CrossRefPubMedGoogle Scholar
  22. Hoagland, D. R. & Arnon, D. I. (1950). The water-culture method for growing plants without soil. California Agricultural Experiment Station Circular 347.Google Scholar
  23. Kim, D. S., & Hwang, B. K. (2014). An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in salicylic acid-dependent signalling of the defence response to microbial pathogens. Journal of Experimental Botany, 65, 2295–2306.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kim, B. S., Lee, J. Y., & Hwang, B. K. (2000). In vivo control and in vitro antifungal activity of rhamnolipid B, a glycolipid antibiotic, against Phytophthora capsici and Colletotrichum orbiculare. Pest Management Science, 56, 1029–1035.CrossRefGoogle Scholar
  25. Konstantinou, S., Veloukas, T., Leroch, M., Menexes, G., Hahn, M., & Karaoglanidis, G. (2015). Population structure, fungicide resistance profile, and sdhB mutation frequency of Botrytis cinerea from strawberry and greenhouse-grown tomato in Greece. Plant Disease, 99, 240–248.CrossRefGoogle Scholar
  26. Kurita, S., Kitagawa, E., Kim, C.-H., Momose, Y., & Iwahashi, H. (2002). Studies on the antimicrobial mechanisms of capsaicin using yeast DNA microrray. Bioscience Biotechnoloy and Biochemistry, 66, 532–536.CrossRefGoogle Scholar
  27. Latijnhouwers, M., de Wit, P. J. G. M., & Govers, F. (2003). Oomycetes and fungi: similar weaponry to attack plants. Trends in Microbiology, 11, 462–469.CrossRefPubMedGoogle Scholar
  28. Liu, X., Han, R., Wang, Y., Li, X., Zhang, M., & Yan, Y. (2014). Fungicidal activity of a medium-chain fatty acids mixture comprising caprylic, pelargonic and capric acids. Plant Pathology Journal, 13, 65–70.CrossRefGoogle Scholar
  29. López-Malo, A., Alzamora, S. M., & Argaiz, A. (1995). Effect of natural vanillin on germination time and radial growth of moulds in fruit-based agar systems. Food Microbiology, 12, 213–219.CrossRefGoogle Scholar
  30. Luo, X.-J., Peng, J., & Li, Y.-J. (2011). Recents advances in the study on capsaicinoids and capsinoids. European Journal of Pharmacology, 650, 1–7.CrossRefPubMedGoogle Scholar
  31. Malo, I., De Bastiani, M., Arevalo, P., & Bernacchia, G. (2017). Natural extracts from pepper, wild rue and clove can activate defences against pathogens in tomato plants. European Journal of Plant Pathology, 149, 89–101.CrossRefGoogle Scholar
  32. Matheron, M. E., & Porchas, M. (2000). Impact of azoxystrobin, dimethomorph, fluazinam, fosetyl-Al, and metalaxyl on growth, sporulation, and zoospore cyst germination of three Phytophthora spp. Plant Disease, 84, 454–458.CrossRefGoogle Scholar
  33. Molina-Torres, J., Garcı́a-Chávez, A., & Ramı́rez-Chávez, E. (1999). Antimicrobial properties of alkamides present in flavouring plants traditionally used in Mesoamerica: affinin and capsaicin. Journal of Ethnopharmacology, 64, 241–248.CrossRefPubMedGoogle Scholar
  34. Oliveira, M. D. M., Varanda, C. M. R., & Félix, M. R. F. (2016). Induced resistance during the interaction pathogen x plant and the use of resistance inducers. Phytochemistry Letters, 15, 152–158.CrossRefGoogle Scholar
  35. Parra, G., & Ristaino, J. B. (2001). Resistance to mefenoxam and metalaxyl among field isolates of Phytophthora capsici causing Phytophthora blight of bell pepper. Plant Disease, 85, 1069–1075.CrossRefGoogle Scholar
  36. Reddy, K. K. (2013). Chemo-enzymatic synthesis of novel phenolic lipids and their evaluation for antioxidant and antimicrobial activities. (Doctoral dissertation, CSIR-Indian Institute of Chemical Technology, Hyderabad).Google Scholar
  37. Reddy, K. K., Ravinder, T., & Kanjilal, S. (2012). Synthesis and evaluation of antioxidant and antifungal activities of novel ricinoleate-based lipoconjugates of phenolic acids. Food Chemistry, 134, 2201–2207.CrossRefPubMedGoogle Scholar
  38. Ristaino, J. B., & Johnston, S. A. (1999). Ecologically based approaches to management of Phytophthora blight on bell pepper. Plant Disease, 83, 1080–1089.CrossRefGoogle Scholar
  39. Šašek, V., Nováková, M., Dobrev, P. I., Valentová, O., & Burketová, L. (2012). β-aminobutyric acid protects Brassica napus plants from infection by Leptosphaeria maculans. Resistance induction or a direct antifungal effect? European Journal of Plant Pathology, 133, 279–289.CrossRefGoogle Scholar
  40. Silvar, C., Duncan, J. M., Cooke, D. E. L., Williams, N. A., Díaz, J., & Merino, F. (2005). Development of specific PCR primers for identification and detection of Phytophthora capsici Leon. European Journal of Plant Pathology, 112, 43–52.CrossRefGoogle Scholar
  41. Silvar, C., Merino, F., & Díaz, J. (2009). Resistance in pepper plants induced by Fusarium oxysporum f. sp. lycopersici involves different defence-related genes. Plant Biology, 11, 68–74.CrossRefPubMedGoogle Scholar
  42. Singh, S., Jarret, R., Russo, V., Majetich, G., Shimkus, J., Bushway, R., & Perkins, B. (2009). Determination of capsinoids by HPLC-DAD in Capsicum species. Journal of Agricultural and Food Chemistry, 57, 3452–3457.CrossRefPubMedGoogle Scholar
  43. Song, G. C., Ryu, S. Y., Kim, Y. S., Lee, J. Y., Choi, J. S., & Ryu, C.-M. (2013). Elicitation of induced resistance against Pectobacterium carotovorum and Pseudomonas syringae by specific individual compounds derived from native Korean plant species. Molecules, 18, 12877–12895.CrossRefPubMedGoogle Scholar
  44. Strobel, G. A., Torczynski, R., & Bollon, A. (1997). Acremonium sp.—a leucinostatin a producing endophyte of European yew (Taxus baccata). Plant Science, 128, 97–108.CrossRefGoogle Scholar
  45. Tanaka, K., Ishihara, A., & Nakajima, H. (2014). Isolation of anteiso-C17, iso-C17, iso-C16, and iso-C15 Bacillomycin D from Bacillus amyloliquefaciens SD-32 and their antifungal activities against plant pathogens. Journal of Agricultural and Food Chemistry, 62, 1469–1476.CrossRefPubMedGoogle Scholar
  46. Tewksbury, J. J., Reagan, K. M., Machnicki, N. J., Carlo, T. A., Haak, D. C., Peñaloza, A. L. C., & Levey, D. J. (2008). Evolutionary ecology of pungency in wild chilies. Proceedings of the National Academy of Sciences, 105, 11808–11811.CrossRefGoogle Scholar
  47. Veloso, J., Prego, C., Varela, M. M., Carballeira, R., Bernal, A., Merino, F., & Díaz, J. (2014). Properties of capsaicinoids for the control of fungi and oomycetes pathogenic to pepper. Plant Biology, 16, 177–185.CrossRefPubMedGoogle Scholar
  48. Zimmerli, L., Métraux, J.-P., & Mauch-Mani, B. (2001). β-Aminobutyric acid-induced protection of Arabidopsis against the necrotrophic fungus Botrytis cinerea. Plant Physiology, 126, 517–523.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2017

Authors and Affiliations

  1. 1.Grupo de Investigación de Fisioloxía e aplicacións das plantas, Departamento de Bioloxía, Facultade de CienciasUniversidade da CoruñaA CoruñaSpain

Personalised recommendations