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Riboflavin (Vitamin B2) induces defence responses and resistance to Plasmopara viticola in grapevine

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Abstract

Grapevine (Vitis vinifera) is susceptible to a variety of pathogenic fungi that affect yield and wine quality. Their control is generally achieved by widespread application of fungicides in the vineyards. The economic costs and negative environmental impact associated with these applications has led to a quest for alternative strategies, focusing on manipulation of host defence mechanisms. Here, we evaluated the ability of riboflavin (i.e. Vitamin B2) to induce resistance against downy mildew in grapevine. Our results showed that 2 mM riboflavin applied 1–3 days before pathogen inoculation provided a disease reduction efficiency of 86 %. A microscopic analysis of the time course of P. viticola colonization in riboflavin-treated leaf discs suggests early inhibition of hyphae spreading in the intercellular space. This resistance does not result from a direct fungitoxic effect of riboflavin. However, this vitamin activates host-defence responses including H2O2 generation, upregulation of an array of defence-related genes and synthesis of callose in stomata cells, while stilbene synthesis is not affected. Using a pharmacological approach, we deduced that both jasmonic acid and callose biosynthesis pathways are significantly involved in riboflavin-induced resistance against downy mildew in grapevine.

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Abbreviations

DPI:

Days post-inoculation

DPT:

Days post-treatment

DDG:

2-deoxy-D-glucose

ETYA:

5 8, 11, 14-eicosatetraynoic acid

H2O2 :

Hydrogen peroxide

HPT:

Hours post-treatment

IR:

Induced resistance

JA:

Jasmonic acid

PR:

Pathogenesis related

Rib:

Riboflavin

References

  • Ahn, I. P., Kim, S., & Lee, Y. H. (2005). Vitamin B1 functions as an activator of plant disease resistance. Plant Physiology, 138, 1505–1515.

    Article  PubMed  CAS  Google Scholar 

  • Alvarez, M. E., Pennell, R. I., Meijer, P. J., Ishikawa, A., Dixon, R. A., & Lamb, C. (1998). Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell, 92, 773–784.

    Article  PubMed  CAS  Google Scholar 

  • Asai, S., Mase, K., & Yoshioka, H. (2010). A key enzyme for flavin synthesis is required for nitric oxide and reactive oxygen species production in disease resistance. The Plant Journal, 62, 911–924.

    PubMed  CAS  Google Scholar 

  • Azami-Sardooei, Z., Soraya, C. F., De-Vleesschauwer, D., & Höfte, M. (2010). Riboflavin induces resistance against Botrytis cinerea in bean, but not in tomato, by priming for a hydrogen peroxide-fueled resistance response. Physiological and Molecular Plant Pathology, 75, 23–29.

    Article  CAS  Google Scholar 

  • Belhadj, A., Telef, N., Saigne, C., Cluzet, S., Barrieu, F., Hamdi, S., & Merillon, J. M. (2008). Effect of methyl jasmonate in combination with carbohydrates on gene expression of PR proteins, stilbene and anthocyanin accumulation in grapevine cell cultures. Plant Physiology and Biochemistry, 46, 493–499.

    Article  PubMed  CAS  Google Scholar 

  • Bellincampi, D., Dipierro, N., Salvi, G., Cervone, F., & De-Lorenzo, G. (2000). Extracellular H2O2 induced by oligogalacturonides is not involved in the inhibition of the auxin-regulated rolB gene expression in tobacco leaf explants. Plant Physiology, 122, 1379–1385.

    Article  PubMed  CAS  Google Scholar 

  • Chen, W. J., Delmotte, F., Richard-Cervera, S., Douence, L., Greif, C., & Corio-Costet, M. F. (2007). At least two origins of fungicide resistance in grapevine downy mildew populations. Applied and Environmental Microbiology, 73, 5162–5172.

    Article  PubMed  CAS  Google Scholar 

  • Cohen, Y., Ruban, A. E., & Vaknin, M. (2011). Post infection application of DL-3-amino-butyric acid (BABA)induces multiple forms of resistance against Bremia lactucae in lettuce. European Journal of Plant Pathology, 130, 13–27.

    Article  CAS  Google Scholar 

  • Collinge, B., Kragh, K. M., Mikkelsen, J. D., Nielsen, K. K., Rasmussen, U., & Vad, K. (1993). Plant chitinases. The Plant Journal, 3, 31–40.

    Article  PubMed  CAS  Google Scholar 

  • Conrath, U., Domard, A., & Kauss, H. (1989). Chitosan-elicited synthesis of callose and of coumarin derivatives in parsley cell suspension cultures. Plant Cell Report, 8, 152–155.

    Article  CAS  Google Scholar 

  • Conrath, U., Pieterse, C. M. J., & Mauch-Mani, B. (2002). Priming in plant-pathogen interactions. Trends in Plant Science, 7, 210–216.

    Article  PubMed  CAS  Google Scholar 

  • Dangl, J. L., & Jones, J. D. (2001). Plant pathogens and integrated defense responses to infection. Nature, 411, 826–833.

    Article  PubMed  CAS  Google Scholar 

  • Diez-Navajas, A. M., Greif, C., Poutaraud, A., & Merdinoglu, D. (2007). Two simplified fluorescent staining techniques to observe infection structures of the oomycete Plasmopara viticola in grapevine leaf tissues. Micron, 38, 680–683.

    Article  PubMed  CAS  Google Scholar 

  • Dixon, R. A., & Paiva, N. L. (1995). Stress-induced phenylpropanoid metabolism. The Plant Cell, 71, 085–1097.

    Google Scholar 

  • Dong, H., & Beer, S. V. (2000). Riboflavin induces disease resistance in plants by activating a novel signal transduction pathway. Phytopathology, 90, 801–11.

    Article  PubMed  CAS  Google Scholar 

  • Dorey, S., Kopp, M., Fritig, B., & Kauffman, S. (1999). Induced defense mechanisms in plant-fungus interactions: differences between cells in culture and leaf tissue. In A. Altman, S. Ishar, & M. Ziv (Eds.), Current plant sciences and biotechnology in agriculture, plant biotechnology and in vitro biology in the 21st century (pp. 473–476). Dordrecht: Kluwer Academic Publishers.

    Chapter  Google Scholar 

  • Hamiduzzaman, M. M., Jakab, G., Barnavon, L., Neuhaus, J. M., & Mauch-Mani, B. (2005). β-Aminobutyric acid-induced resistance against downy mildew in grapevine acts through the potentiation of callose formation and jasmonic acid signaling. Molecular Plant-Microbe Interactions, 18, 819–829.

    Article  PubMed  CAS  Google Scholar 

  • Jabs, T., Dietrich, R. A., & Dangl, J. F. (1996). Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science, 273, 1853–1856.

    Article  PubMed  CAS  Google Scholar 

  • Kiefer, B., Riemann, M., Büche, C., Kassemeyer, H. H., & Nick, P. (2002). The host guides morphogenesis and stomatal targeting in the grapevine pathogen Plasmopara viticola. Planta, 215, 387–393.

    Article  PubMed  CAS  Google Scholar 

  • Kortekamp, A. (2006). Expression analysis of defence-related genes in grapevine leaves after inoculation with a host and a non-host pathogen. Plant Physiology and Biochemistry, 44, 58–67.

    Article  PubMed  CAS  Google Scholar 

  • Kortekamp, A., Wind, R., & Zyprian, E. (1998). Investigation of the interaction of Plasmopara viticola with susceptible and resistant grapevine cultivars. Journal of Plant Disease Protection, 105, 475–488.

    Google Scholar 

  • Liu, F., Fang, W., Wang, L., Liu, H., Zhu, X., & Yuancun, L. (2010). Riboflavin activates defense responses in tobacco and induces resistance against Phytophthora parasitica and Ralstonia solanacearum. Physiological and Molecular Plant Pathology, 74, 330–336.

    Article  CAS  Google Scholar 

  • Norman, S. C., Vidal, S., & Palva, T. E. (2000). Interacting signal pathways control defense gene expression in Arabidopsis in response to cell wall-degrading enzymes from Erwinia carotovora. Molecular Plant-Microbe Interactions, 13, 430–438.

    Article  Google Scholar 

  • Omer, A. D., Thaler, J. S., Granett, J., & Karban, R. (2000). Jasmonic acid induced resistance in grapevines to a root and leaf feeder. J Eco Entomol, 93, 840–845.

    Article  CAS  Google Scholar 

  • Perazzoli, M., Dagostin, S., Ferrari, A., Elad, Y., & Pertot, I. (2008). Induction of systemic resistance against Plasmopara viticola in grapevine by Trichoderma harzianum T39 and benzothiadiazole. Biological Control, 47, 228–234.

    Article  Google Scholar 

  • Poutaraud, A., Latouche, G., Martins, S., Meyer, S., Merdinoglu, D., & Cerovic, Z. G. (2007). Fast and local assessment of stilbene content in grapevine leaf by in vivo fluorometry. Journal of Agriculture and Food Chemistry, 55, 4913–4920.

    Article  CAS  Google Scholar 

  • Rumbolz, J., Wirtz, S., Kassemeye, H. H., Guggenheim, R. E., Schäfer, & Büche, C. (2002). Sporulation of Plasmopara viticola: differentiation and light regulation. Plant Biology, 4, 413–422.

    Article  Google Scholar 

  • Ryals, J. A., Neuenschwander, U. M., Willits, M. G., Molina, A., Steiner, H., & Hunt, M. O. (1996). Systemic acquired resistance. The Plant Cell, 8, 1809–1819.

    PubMed  CAS  Google Scholar 

  • Saikia, R., Yadav, M., Varghese, S., Pratap, B., Dip, S., Gogoi, K., Kumar, R., & Arora, D. K. (2006). Role of riboflavin in induced resistance against Fusarium Wilt and Charcoal Rot diseases of Chickpea. Plant Pathology Journal, 22(4), 339–347.

    Article  Google Scholar 

  • Sheehan, D., Meade, G., Vivienne, M. F., & Dowd, C. A. (2001). Structure, function and evolution of glutathione transferase: Implications for classification of non mammalian members of an ancient enzyme super family. Biochemical Journal, 360, 1–16.

    Article  PubMed  CAS  Google Scholar 

  • Sticher, L., Mauch-Mani, B., & Metraux, J. P. (1997). Systemic acquired resistance. Annual Review of Phytopathology, 35, 235–270.

    Article  PubMed  CAS  Google Scholar 

  • Sundravel, S., Shanthi, P., & Sachdanandam, P. (2003). Curative effect of riboflavin, niacin and ascorbic acid on tamoxifen mediated endometrial carcinoma bearing Sprague–Dawley rats with reference to lipid peroxidation and antioxidant status. Journal of Clinical Biochemistry and Nutrition, 33, 39–45.

    Article  CAS  Google Scholar 

  • Taheri, P., & Höfte, M. (2007). Riboflavin-induced resistance against rice sheath blight functions through the potentiation of lignin formation and jasmonic acid signaling pathway. Communications in Agriculture Applied Biological Sciences, 72, 309–313.

    CAS  Google Scholar 

  • Taheri, P., & Tarighi, S. (2010). Riboflavin induces resistance in rice against Rhizoctonia solani via jasmonatemediated priming of phenylpropanoid pathway. Journal of Plant Physiology, 167, 201–208.

    Article  PubMed  CAS  Google Scholar 

  • Taheri, P., & Tarighi, S. (2011). A survey on basal resistance and riboflavin-induced defense responses of sugar beet against Rhizoctonia solani. Journal of Plant Physiology, 168, 1014–1122.

    Article  Google Scholar 

  • Thomma, B. P., Eggermont, K., Penninckx, I. A., Mauch-Mani, B., Vogelsang, R., Cammue, B. P. A., & Broekaert, W. F. (1998). Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proceeding of National Academic Sciences of USA, 95, 15107–15111.

    Article  CAS  Google Scholar 

  • Thordal-Christensen, H., Zhang, Z., 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, 87–94.

    Article  Google Scholar 

  • Trouvelot, S., Varnier, A. L., Allegre, M., Mercier, L., Baillieuil, F., Arnould, C., Gianinazzi-Pearson, V., Klarzynski, O., Joubert, J. M., Pugin, A., & Daire, X. (2008). A beta-1,3 glucan sulfate induces resistance in grapevine against Plasmopara viticola through priming of defense responses, including HR-like cell death. Molecular Plant-Microbe Interactions, 21, 232–243.

    Article  PubMed  CAS  Google Scholar 

  • Unger, S., Bueche, C., Boso, S., & Kassemeyer, H. H. (2007). The course of colonization of two different Vitis genotypes by Plasmopara viticola indicates compatible and incompatible host-pathogen interactions. Phytopathology, 97, 780–786.

    Article  PubMed  Google Scholar 

  • Van Loon, L. C., & Van Strien, E. A. (1999). The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiological and Molecular Plant Pathology, 3, 85–97.

    Article  Google Scholar 

  • Yang, Y., Shah, J., & Klessig, D. F. (1997). Signal perception and transduction in plant defense responses. Genes & Development, 11, 1621–1639.

    Article  CAS  Google Scholar 

  • Zhang, S. J., Yang, X., Sun, M. W., Sun, F., Deng, S., & Dong, H. S. (2009). Riboflavin-induced priming for pathogen defense in Arabidopsis thaliana. Journal of Integrative Plant Biology, 51, 167–74.

    Article  PubMed  Google Scholar 

  • Zubay, G. (1998). Biochemistry. Dubuque: Brown Publishers.

    Google Scholar 

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Acknowledgments

This work was carried out in the “Institut National de Recherche Agronomique- Colmar, France” and supported by grants from the “Ministry of Higher Education and Scientific Research of Tunisia”. We thank M. Perrin and M. Romon for plant material and lab expertise.

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Authors and Affiliations

  1. Laboratoire de Physiologie Moléculaire des Plantes, Centre de Biotechnologie de Borj-Cédria, 2050-Hammam-Lif, Tunisie, Tunisia

    H. Boubakri & A. Mliki

  2. Santé de la Vigne et Qualité du Vin, INRA-UDS UMR 1131, 28 Rue de Herrlisheim, BP 20507, Colmar Cedex, France

    H. Boubakri, C. Schmitt & J. E. Masson

  3. Université de Haute Alsace, Laboratoire Vigne, Biotechnologies et Environnement (LVBE, EA3991), 33 rue de Herrlisheim, 68000, Colmar, France

    J. Chong, C. Bertsch & I. Soustre-Gacougnolle

  4. Unité Mixte de Recherche 1131, Université Louis Pasteur Strasbourg, INRA-Colmar, 28 Rue de Herrlisheim, 68021, Colmar, France

    A. Poutaraud

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  1. H. Boubakri
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  2. J. Chong
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  3. A. Poutaraud
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  4. C. Schmitt
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  5. C. Bertsch
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  8. I. Soustre-Gacougnolle
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Correspondence to H. Boubakri.

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Boubakri, H., Chong, J., Poutaraud, A. et al. Riboflavin (Vitamin B2) induces defence responses and resistance to Plasmopara viticola in grapevine. Eur J Plant Pathol 136, 837–855 (2013). https://doi.org/10.1007/s10658-013-0211-x

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  • DOI: https://doi.org/10.1007/s10658-013-0211-x

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