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Impact of abiotic stresses on the protection efficacy of defence elicitors and on metabolic regulation in tomato leaves infected by Botrytis cinerea

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Abstract

Finding sustainable plant protection strategies is a major challenge for agriculture. Taking advantage of the plant natural immune system by using plant defence elicitors is an interesting avenue to explore. However, transfer to field application is often difficult, mostly due to the complexity of interactions between plants and their environment, involving biotic and abiotic stresses. The protection efficacy against gray mold and the modes of action of potential elicitors were studied on tomato. Modulation of plant defense was studied using both global and targeted metabolic profiling. We identified seven potential elicitors showing good plant protection efficacy and able to trigger the oxylipin pathway, including jasmonic acid production, after inoculation with Botrytis cinerea. Following preliminary assays, seven elicitors including two well-studied elicitors (Bion 50WG® and BABA) showing good plant protection efficacy and low fungitoxic effect were selected to assay the effect of abiotic stresses (wounding, water stress and nitrogen deficiency) on their protection efficacy. Our results showed that the protection efficacy of all products was reduced when plants were exposed to abiotic stresses, suggesting an antagonistic interaction between the tomato responses to abiotic stresses and product treatments. We found that responses to leaf cuttings and product treatments induced metabolic changes in a time-dependent manner, and that both of which mainly activated the oxylipin and JA pathway. However, the negative effects of wounding on tomato protection efficacy of defence elicitors suggest that interplay with other antagonistic signalling pathways is also involved in the tomato responses to this combination of stress.

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References

  • Achuo, E., Prinsen, E., & Höfte, M. (2006). Influence of drought, salt stress and abscisic acid on the resistance of tomato to Botrytis cinerea and Oidium neolycopersici. Plant Pathology, 55(2), 178–186.

    Article  CAS  Google Scholar 

  • Amborabe, E., Aziz, A., Trotel-Aziz, P., Quantinet, D., Dhuicq, L., & Vernet, G. (2004). Stimulation des défenses naturelles de la vigne: Essais d’emploi du chitosan contre Botrytis cinerea. Phytoma-La Défense des Végétaux, 571, 26–29.

    CAS  Google Scholar 

  • Anderson, J. P., Badruzsaufari, E., Schenk, P. M., Manners, J. M., Desmond, O. J., Ehlert, C., et al. (2004). Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. The Plant Cell Online, 16(12), 3460–3479.

    Article  CAS  Google Scholar 

  • Angulo, C., De la O Leyva, M., Finiti, I., López-Cruz, J., Fernández-Crespo, E., García-Agustín, P., & González-Bosch, C. (2015). Role of dioxygenase α-DOX2 and SA in basal response and in hexanoic acid-induced resistance of tomato (Solanum lycopersicum) plants against Botrytis cinerea. Journal of Plant Physiology, 175(2015), 163–173.

  • Asselbergh, B., De Vleesschauwer, D., & Höfte, M. (2008). Global switches and fine-tuning-ABA modulates plant pathogen defense. Molecular Plant-Microbe Interactions: MPMI, 21(6), 709–719. doi:10.1094/MPMI-21-6-0709.

    Article  CAS  PubMed  Google Scholar 

  • Atkinson, N. J., & Urwin, P. E. (2012). The interaction of plant biotic and abiotic stresses: from genes to the field. Journal of Experimental Botany. doi:10.1093/jxb/ers100.

    PubMed Central  Google Scholar 

  • Audenaert, K., De Meyer, G. B., & Höfte, M. M. (2002). Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiology, 128(2), 491–501. doi:10.1104/pp.010605.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Azami-Sardooei, Z., Seifi, H. S., Vleesschauwer, D. D., & Höfte, M. (2013). Benzothiadiazole (BTH)-induced resistance against Botrytis cinerea is inversely correlated with vegetative and generative growth in bean and cucumber, but not in tomato. Australasian Plant Pathology, 42(4), 485–490. doi:10.1007/s13313-013-0207-1.

    Article  CAS  Google Scholar 

  • Aziz, A., Poinssot, B., Daire, X., Adrian, M., Bézier, A., Lambert, B., et al. (2003). Laminarin elicits defense responses in grapevine and induces protection against Botrytis cinerea and Plasmopara viticola. Molecular Plant-Microbe Interactions, 16(12), 1118–1128.

    Article  CAS  PubMed  Google Scholar 

  • Aziz, A., Trotel-Aziz, P., Dhuicq, L., Jeandet, P., Couderchet, M., & Vernet, G. (2006). Chitosan oligomers and copper sulfate induce grapevine defense reactions and resistance to gray mold and downy mildew. Phytopathology, 96(11), 1188–1194. doi:10.1094/PHYTO-96-1188.

    Article  CAS  PubMed  Google Scholar 

  • Ballester, A. R., Lafuente, M. T., Forment, J., Gadea, J., De Vos, R. C. H., Bovy, A. G., et al. (2011). Transcriptomic profiling of citrus fruit peel tissues reveals fundamental effects of phenylpropanoids and ethylene on induced resistance. Molecular Plant Pathology, 12(9), 879–897. doi:10.1111/j.1364-3703.2011.00721.x.

    Article  CAS  PubMed  Google Scholar 

  • Brisset, M. N., Cesbron, S., Thomson, S. V., & Paulin, J. P. (2000). Acibenzolar-S-methyl induces the accumulation of defense-related enzymes in apple and protects from fire blight. European Journal of Plant Pathology, 106(6), 529–536.

    Article  CAS  Google Scholar 

  • Chassot, C., Buchala, A., Schoonbeek, H. J., et al. (2008). Wounding of Arabidopsis leaves causes a powerful but transient protection against Botrytis infection. The Plant Journal, 55(4), 555–567. doi:10.1111/j.1365-313X.2008.03540.x.

  • Cohen, Y., Niderman, T., Mosinger, E., & Fluhr, R. (1994). β-Aminobutyric acid induces the accumulation of pathogenesis-related proteins in tomato (Lycopersicon esculentum L.) plants and resistance to late blight infection caused by Phytophthora infestans. Plant Physiology, 104(1), 59–66.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Curvers, K., Seifi, H., Mouille, G., de Rycke, R., Asselbergh, B., Van Hecke, A., et al. (2010). Abscisic acid deficiency causes changes in cuticle permeability and pectin composition that influence tomato resistance to Botrytis cinerea. Plant Physiology, 154(2), 847–860. doi:10.1104/pp.110.158972.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dietrich, R., Ploss, K., & Heil, M. (2005). Growth responses and fitness costs after induction of pathogen resistance depend on environmental conditions. Plant, Cell & Environment, 28(2), 211–222.

    Article  CAS  Google Scholar 

  • Dinh, S. Q., Joyce, D. C., Irving, D. E., & Wearing, A. H. (2007). Field applications of three different classes of known host plant defence elicitors did not suppress infection of Geraldton waxflower by Botrytis cinerea. Australasian Plant Pathology, 36(2), 142. doi:10.1071/ap07001.

    Article  CAS  Google Scholar 

  • Dufour, M. C., Lambert, C., Bouscaut, J., Mérillon, J. M., & Corio-Costet, M. F. (2013). Benzothiadiazole-primed defence responses and enhanced differential expression of defence genes in Vitis vinifera infected with biotrophic pathogens Erysiphe necator and Plasmopara viticola. Plant Pathology, 62(2), 370–382. doi:10.1111/j.1365-3059.2012.02628.x.

    Article  CAS  Google Scholar 

  • El Oirdi, M., El Rahman, T. A., Rigano, L., et al. (2011). Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. The Plant Cell Online, 23(6), 2405–2421.

    Article  Google Scholar 

  • Eyre, J., Faragher, J., Joyce, D., & Franz, P. (2006). Effects of postharvest methyl jasmonate treatments against Botrytis cinerea on Geraldton waxflower (Chamelaucium uncinatum). Animal Production Science, 46(5), 717–723.

    Article  CAS  Google Scholar 

  • Ferrari, S., Galletti, R., Denoux, C., De Lorenzo, G., Ausubel, F. M., & Dewdney, J. (2007). Resistance to Botrytis cinerea induced in arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3. Plant Physiology, 144(1), 367–379. doi:10.1104/pp.107.095596.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fu, Z. Q., & Dong, X. (2013). Systemic acquired resistance: turning local infection into global defense. Annual Review of Plant Biology, 64, 839–863. doi:10.1146/annurev-arplant-042811-105606.

    Article  CAS  PubMed  Google Scholar 

  • Glauser, G. (2010). Etude de la réponse à la blessure mécanique chez les plantes: une approche métabolomique. University of Geneva, from http://archive-ouverte.unige.ch/unige:5274.

  • Heil, M., Hilpert, A., Kaiser, W., & Linsenmair, K. E. (2000). Reduced growth and seed set following chemical induction of pathogen defence: does systemic acquired resistance (SAR) incur allocation costs? Journal of Ecology, 88(4), 645–654. doi:10.1046/j.1365-2745.2000.00479.x.

    Article  CAS  Google Scholar 

  • Jakab, G., Cottier, V., Toquin, V., Rigoli, G., Zimmerli, L., Métraux, J.-P., et al. (2001). β-Aminobutyric acid-induced resistance in plants. European Journal of Plant Pathology, 107(1), 29–37.

    Article  CAS  Google Scholar 

  • Jones, J. D. G., & Dangl, J. L. (2006). The plant immune system. Nature, 444(7117), 323–329. doi:10.1038/nature05286.

    Article  CAS  PubMed  Google Scholar 

  • Kettner, J., & Dörffling, K. (1995). Biosynthesis and metabolism of abscisic acid in tomato leaves infected with Botrytis cinerea. Planta, 196(4), 627–634. doi:10.1007/BF01106753.

    Article  CAS  Google Scholar 

  • Klarzynski, O., Plesse, B., Joubert, J. M., Yvin, J. C., Kopp, M., Kloareg, B., et al. (2000). Linear beta-1,3 glucans are elicitors of defense responses in tobacco. Plant Physiology, 124(3), 1027–1038.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lou, B., Wang, A., Lin, C., Xu, T., & Zheng, X. (2011). Enhancement of defense responses by oligandrin against Botrytis cinerea in tomatoes. African Journal of Biotechnology, 10(55), 442–449.

    Google Scholar 

  • Mansfield, J. W. (1980). Mechanisms of resistance to ‘Botrytis’. In J. R. Coley-Smith, K. Verhoeff, & W. R. Jarvis (Eds.), The biology of Botrytis (pp. 181–218). New York: Academic Press.

    Google Scholar 

  • Massoud, K., Barchietto, T., Le Rudulier, T., Pallandre, L., Didierlaurent, L., Garmier, M., et al. (2012). Dissecting phosphite-induced priming in Arabidopsis infected with Hyaloperonospora arabidopsidis. Plant Physiology, 159(1), 286–298.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Métraux, J. P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., et al. (1990). Increase in salicylic Acid at the onset of systemic acquired resistance in cucumber. Science (New York, N.Y.), 250(4983), 1004–1006. doi:10.1126/science.250.4983.1004.

    Article  Google Scholar 

  • Mohr, P. G., & Cahill, D. M. (2003). Abscisic acid influences the susceptibility of Arabidopsis thaliana to Pseudomonas syringae pv. tomato and Peronospora parasitica. Functional Plant Biology, 30(4), 461–469.

    Article  CAS  Google Scholar 

  • Mur, L. A., Kenton, P., Atzorn, R., et al. (2006). The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiology, 140(1), 249–262.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Niinemets, Ü. (2010). Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: past stress history, stress interactions, tolerance and acclimation. Forest Ecology and Management, 260(10), 1623–1639. doi:10.1016/j.foreco.2010.07.054.

    Article  Google Scholar 

  • Pastor, V., Luna, E., Mauch-Mani, B., Ton, J., & Flors, V. (2013). Primed plants do not forget. Environmental and Experimental Botany, 94, 46–56. doi:10.1016/j.envexpbot.2012.02.013.

    Article  CAS  Google Scholar 

  • Pozo, M. J., & Azcón-Aguilar, C. (2007). Unraveling mycorrhiza-induced resistance. Current Opinion in Plant Biology, 10(4), 393–398. doi:10.1016/j.pbi.2007.05.004.

    Article  CAS  PubMed  Google Scholar 

  • Ryan, C. A., & Moura, D. S. (2002). Systemic wound signaling in plants: a new perception. Proceedings of the National Academy of Sciences, 99(10), 6519–6520. doi:10.1073/pnas.112196499.

    Article  CAS  Google Scholar 

  • Salt, S. D., Tuzun, S., & Kuc, J. (1986). Effects of β-ionone and abscisic acid on the growth of tobacco and resistance to blue mold. Mimicry of effects of stem infection by Peronospora tabacina Adam. Physiological and Molecular Plant Pathology, 28(2), 287–297.

    Article  CAS  Google Scholar 

  • Sanchez, L., Courteaux, B., Hubert, J., Kauffmann, S., Renault, J.-H., Clément, C., et al. (2012). Rhamnolipids elicit defense responses and induce disease resistance against biotrophic, hemibiotrophic, and necrotrophic pathogens that require different signaling pathways in Arabidopsis and highlight a central role for salicylic acid. Plant Physiology, 160(3), 1630–1641.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sandermann, H. (2004). Molecular ecotoxicology: from man-made pollutants to multiple environmental stresses. In P. D. H. Sandermann (Ed.), Molecular ecotoxicology of plants (pp. 1–16, Ecological Studies). Berlin: Springer.

    Chapter  Google Scholar 

  • Small, I., Flett, B., Marasas, W., McLeod, A., & Viljoen, A. (2012). Use of resistance elicitors to reduce Fusarium ear rot and fumonisin accumulation in maize. Crop Protection, 41, 10–16.

    Article  CAS  Google Scholar 

  • Stout, M. J., Brovont, R. A., & Duffey, S. S. (1998). Effect of nitrogen availability on expression of constitutive and inducible chemical defenses in tomato, lycopersicon esculentum. Journal of Chemical Ecology, 24(6), 945–963. doi:10.1023/A:1022350100718.

    Article  CAS  Google Scholar 

  • Suzuki, N., Rivero, R. M., Shulaev, V., Blumwald, E., & Mittler, R. (2014). Abiotic and biotic stress combinations. New Phytologist, 203(1), 32–43. doi:10.1111/nph.12797.

    Article  PubMed  Google Scholar 

  • Teng, P. S. (1994). Epidemiological basis for blast management.

  • Ton, J., & Mauch-Mani, B. (2004). β-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. The Plant Journal, 38(1), 119–130. doi:10.1111/j.1365-313X.2004.02028.x.

    Article  CAS  PubMed  Google Scholar 

  • Ton, J., Flors, V., & Mauch-Mani, B. (2009). The multifaceted role of ABA in disease resistance. Trends in Plant Science, 14(6), 310–317.

    Article  CAS  PubMed  Google Scholar 

  • Trouvelot, S., Varnier, A. L., Allègre, M., Mercier, L., Baillieul, F., Arnould, C., et al. (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: MPMI, 21(2), 232–243. doi:10.1094/MPMI-21-2-0232.

    Article  CAS  PubMed  Google Scholar 

  • Truman, W., Bennett, M. H., Kubigsteltig, I., et al. (2007). Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proceedings of the National Academy of Sciences of the United States of America, 104(3), 1075–1080. doi:10.1073/pnas.0605423104.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Veloso, J., & Díaz, J. (2013). Induced resistance to Botrytis cinerea in Capsicum annuum by a Fusarium crude elicitor fraction, free of proteins. Plant Biology, 15(6), 1040–1044.

    Article  CAS  PubMed  Google Scholar 

  • Walters, D., Walsh, D., Newton, A., & Lyon, G. (2005). Induced resistance for plant disease control: maximizing the efficacy of resistance elicitors. Phytopathology, 95(12), 1368–1373. doi:10.1094/PHYTO-95-1368.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y., Loake, G. J., & Chu, C. (2013). Cross-talk of nitric oxide and reactive oxygen species in plant programed cell death. Frontiers in Plant Science, 4, 314.

    PubMed Central  PubMed  Google Scholar 

  • Zhu, Z., & Tian, S. (2012). Resistant responses of tomato fruit treated with exogenous methyl jasmonate to Botrytis cinerea infection. Scientia Horticulturae, 142, 38–43.

    Article  CAS  Google Scholar 

  • 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(2), 517–523. doi:10.1104/pp.126.2.517.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgment

This work was financially supported by Vegenov-BBV, GCSAR (General Commission for Scientific Agricultural Research-Syria) and the French Ministry of Agriculture. It was also supported by companies providing the different PDE products. We are grateful to the plant pathology team in Vegenov for their technical assistance and their advices.

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Correspondence to Turner Marie.

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Maymoune, A., Adeline, P., Marie, T. et al. Impact of abiotic stresses on the protection efficacy of defence elicitors and on metabolic regulation in tomato leaves infected by Botrytis cinerea . Eur J Plant Pathol 142, 223–237 (2015). https://doi.org/10.1007/s10658-015-0606-y

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