Abstract
The hemibiotrophic fungus Zymoseptoria tritici is the causative agent of Septoria tritici leaf blotch (STB) disease of wheat (Triticum aestivum L.), the economically most damaging disease of wheat in Europe. Today, ecofriendly plant protection methods compatible with sustainable agriculture are strongly desirable. Here, we tested two chemical inducers β-aminobutyric acid (BABA) and benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester (BTH) and the two biotic inducers Pseudomonas protegens CHA0 (CHA0) and P. chlororaphis PCL1391 (PCL) for their ability to induce resistance against STB in wheat seedlings. At 21 days after inoculation, only plants treated with BABA showed a smaller area covered by lesions and less pycnidia compared to the untreated control plants. We evaluated spore germination and fungal development on inoculated wheat leaves at early infection stages using calcofluor white staining. Overall, spores of Z. tritici germinated less on plants soil-drenched with BABA and BTH and their hyphal growth was significantly delayed. On the contrary, CHA0 and PCL seed treatments did not affect fungal growth in wheat leaves. In conclusion, BABA efficiently enhanced plant resistance to Z. tritici, BTH delayed fungal development at early stages while the two biotic inducers did not influence the resistance against STB disease.
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Abdel-Monaim, M. F., Ismail, M. E., & Morsy, K. M. (2011). Induction of systemic resistance of benzothiadiazole and humic acid in soybean plants against Fusarium wilt disease. Mycobiology, 39(4), 290–298.
Aktar, W., Sengupta, D., & Chowdhury, A. (2009). Impact of pesticides use in agriculture: their benefits and hazards. Interdisciplinary toxicology, 2(1), 1–12.
Amzalek, E., & Cohen, Y. (2007). Comparative efficacy of systemic acquired resistance-inducing compounds against rust infection in sunflower plants. Phytopathology, 97(2), 179–186.
Azami-Sardooei, Z., Seifi, H. S., De Vleesschauwer, 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.
Balmer, A., Pastor, V., Gamir, J., Flors, V., & Mauch-Mani, B. (2015). The ‘prime-ome’: towards a holistic approach to priming. Trends in plant science, 20(7), 443–452.
Bardas, G. A., Lagopodi, A. L., Kadoglidou, K., & Tzavella-Klonari, K. (2009). Biological control of three Colletotrichum lindemuthianum races using Pseudomonas chlororaphis PCL1391 and Pseudomonas fluorescens WCS365. Biological control, 49(2), 139–145.
Barilli, E., Sillero, J. C., & Rubiales, D. (2010). Induction of systemic acquired resistance in pea against rust (Uromyces pisi) by exogenous application of biotic and abiotic inducers. Journal of phytopathology, 158(1), 30–34.
Benhamou, N., & Bélanger, R. R. (1998). Benzothiadiazole-Mediated Induced Resistance to Fusarium oxysporum f. sp. radicis-lycopersici in Tomato. Plant physiology, 118(4), 1203–1212.
Berny, P. (2007). Pesticides and the intoxication of wild animals. Journal of Veterinary pharmacology and therapeutics, 30(2), 93–100.
Chaudhary, T., & Shukla, P. (2019). Bioinoculants for Bioremediation Applications and Disease Resistance: Innovative Perspectives. Indian journal of microbiology, 59(2), 129–136.
Cheval, P., Siah, A., Bomble, M., Popper, A. D., Reignault, P., & Halama, P. (2017). Evolution of QoI resistance of the wheat pathogen Zymoseptoria tritici in Northern France. Crop protection, 92, 131–133.
Chin-A-Woeng, T. F., Bloemberg, G. V., van der Bij, A. J., van der Drift, K. M., Schripsema, J., Kroon, B., et al. (1998). Biocontrol by phenazine-1-carboxamide-producing Pseudomonas chlororaphis PCL1391 of tomato root rot caused by Fusarium oxysporum f. sp. radicis-lycopersici. Molecular plant-microbe interactions, 11(11), 1069–1077.
Cohen, Y., & Gisi, U. (1994). Systemic translocation of 14C-DL-3-aminobutyric acid in tomato plants in relation to induced resistance against Phytophthora infestans. Physiological and molecular plant pathology, 45(6), 441–456.
Cohen, Y., Vaknin, M., & Mauch-Mani, B. (2016). BABA-induced resistance: milestones along a 55-year journey. Phytoparasitica, 44(4), 513–538.
R Core Team (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at https://www.R-project.org/.
Cowger, C., Hoffer, M., & Mundt, C. (2000). Specific adaptation by Mycosphaerella graminicola to a resistant wheat cultivar. Plant pathology, 49(4), 445–451.
Defago, G., Berling, C., Burger, U., Haas, D., Kahr, G., Keel, C., et al. (1990). Suppression of black root rot of tobacco and other root diseases by strains of Pseudomonas fluorescens: potential applications and mechanisms. In R. J. Cook, Y. Henis, & D. Hornby (Eds.), Biological control of soil-borne plant pathogens (pp. 93–108). CAB International.
Dimkpa, C., Weinand, T., & Asch, F. (2009). Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant cell and environment, 32(12), 1682–1694.
Douaiher, M. N., Nowak, E., Durand, R., Halama, P., & Reignault, P. (2007). Correlative analysis of Mycosphaerella graminicola pathogenicity and cell wall-degrading enzymes produced in vitro: the importance of xylanase and polygalacturonase. Plant pathology, 56(1), 79–86.
El-Sharkawy, H. H., Rashad, Y. M., & Ibrahim, S. A. (2018). Biocontrol of stem rust disease of wheat using arbuscular mycorrhizal fungi and Trichoderma spp. Physiological and molecular plant pathology, 103, 84–91.
Fischer, M. J., Farine, S., Chong, J., Guerlain, P., & Bertsch, C. (2009). The direct toxicity of BABA against grapevine ecosystem organisms. Crop protection, 28(8), 710–712.
Flaishman, M. A., Eyal, Z., Zilberstein, A., Voisard, C., & Haas, D. (1996). Suppression of Septoria tritici blotch and leaf rust of wheat by recombinant cyanide-producing strains of Pseudomonas putida. Molecular plant microbe interactions, 9(7), 642–645.
Flury, P., Vesga, P., Péchy-Tarr, M., Aellen, N., Dennert, F., Hofer, N., et al. (2017). Antimicrobial and Insecticidal: Cyclic Lipopeptides and Hydrogen Cyanide Produced by Plant-Beneficial Pseudomonas Strains CHA0, CMR12a, and PCL1391 Contribute to Insect Killing. Frontiers in microbiology, 8(100).
Fones, H., & Gurr, S. (2015). The impact of Septoria tritici Blotch disease on wheat: An EU perspective. Fungal genetics and biology, 79, 3–7.
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(4), 629–643.
Haas, D., & Défago, G. (2005). Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature reviews microbiology, 3(4), 307.
Hase, C., Hottinger, M., Moënne-Loccoz, Y., & Défago, G. (2000). Survival and cell culturability of biocontrol Pseudomonas fluorescens CHA0 in the rhizosphere of cucumber grown in two soils of contrasting fertility status. Biology and fertility of soils, 32(3), 217–221.
Henkes, G. J., Jousset, A., Bonkowski, M., Thorpe, M. R., Scheu, S., Lanoue, A., et al. (2011). Pseudomonas fluorescens CHA0 maintains carbon delivery to Fusarium graminearum-infected roots and prevents reduction in biomass of barley shoots through systemic interactions. Journal of experimental botany, 62(12), 4337–4344.
Hol, W., Bezemer, T. M., & Biere, A. (2013). Getting the ecology into interactions between plants and the plant growth-promoting bacterium Pseudomonas fluorescens. Frontiers in Plant Science, 4, 81.
Iavicoli, A., Boutet, E., Buchala, A., & Métraux, J.-P. (2003). Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Molecular plant-microbe interactions, 16(10), 851–858.
Imperiali, N., Chiriboga, X., Schlaeppi, K., Fesselet, M., Villacrés, D., Jaffuel, G., et al. (2017). Combined field inoculations of Pseudomonas bacteria, arbuscular mycorrhizal fungi, and entomopathogenic nematodes and their effects on wheat performance. Frontiers in Plant Science, 8, 100.
Iriti, M., Rossoni, M., Borgo, M., & Faoro, F. (2004). Benzothiadiazole enhances resveratrol and anthocyanin biosynthesis in grapevine, meanwhile improving resistance to Botrytis cinerea. Journal of agricultural and food chemistry, 52(14), 4406–4413.
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.
Jørgensen, L. N., Hovmøller, M. S., Hansen, J. G., Lassen, P., Clark, B., Bayles, R., et al. (2014). IPM strategies and their dilemmas including an introduction to www. Eurowheat. org. Journal of integrative agriculture, 13(2), 265–281.
Karthikeyan, V., & Gnanamanickam, S. (2011). Induction of systemic resistance in rice to bacterial blight by 1, 2, 3-benzothiadiazole 7-carbothioic acid-S-methyl ester (BTH) treatments. Archives of phytopathology and plant protection, 44(3), 269–281.
Kema, G. H., Yu, D., Rijkenberg, F. H., Shaw, M. W., & Baayen, R. P. (1996). Histology of the pathogenesis of Mycosphaerella graminicola in wheat. Phytopathology, 86(7), 777–786.
Keon, J., Antoniw, J., Carzaniga, R., Deller, S., Ward, J. L., Baker, J. M., et al. (2007). Transcriptional adaptation of Mycosphaerella graminicola to programmed cell death (PCD) of its susceptible wheat host. Molecular plant-microbe interactions, 20(2), 178–193.
Landa, B. B., Mavrodi, O. V., Raaijmakers, J. M., Gardener, B. B. M., Thomashow, L. S., & Weller, D. M. (2002). Differential ability of genotypes of 2, 4-diacetylphloroglucinol-producing Pseudomonas fluorescens strains to colonize the roots of pea plants. Applied environmental microbiology, 68(7), 3226–3237.
Levy, E., Gough, F., Berlin, K., Guiana, P., & Smith, J. (1992). Inhibition of Septoria tritici and other phytopathogenic fungi and bacteria by Pseudomonas fluorescens and its antibiotics. Plant pathology, 41(3), 335–341.
Liu, H., Jiang, W., Bi, Y., & Luo, Y. (2005). Postharvest BTH treatment induces resistance of peach (Prunus persica L. cv. Jiubao) fruit to infection by Penicillium expansum and enhances activity of fruit defense mechanisms. Postharvest biology and technology, 35(3), 263–269.
Mauchline, T. H., & Malone, J. G. (2017). Life in earth–the root microbiome to the rescue? Current opinion in microbiology, 37, 23–28.
Maurhofer, M., Hase, C., Meuwly, P., Metraux, J.-P., & Defago, G. (1994). Induction of systemic resistance of tobacco to tobacco necrosis virus by the root-colonizing Pseudomonas fluorescens strain CHA0: influence of the gacA gene and of pyoverdine production. Phytopathology, 84(2), 139–146.
Mejri, S., Siah, A., Coutte, F., Magnin-Robert, M., Randoux, B., Tisserant, B., et al. (2018). Biocontrol of the wheat pathogen Zymoseptoria tritici using cyclic lipopeptides from Bacillus subtilis. Environmental science and pollution research, 25(30), 29,822–29,833.
Mejri, S., Siah, A., Abuhaie, C. M., Halama, P., Magnin-Robert, M., Randoux, B., et al. (2019). New salicylic acid and pyroglutamic acid conjugated derivatives confer protection to bread wheat against Zymoseptoria tritici. Journal of the science of food and agriculture, 99(4), 1780–1786.
Mercado-Blanco, J., & Bakker, P. A. (2007). Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection. Antonie van Leeuwenhoek, 92(4), 367–389.
Natsch, A., Keel, C., Pfirter, H. A., Haas, D., & Défago, G. (1994). Contribution of the global regulator gene gacA to persistence and dissemination of Pseudomonas fluorescens biocontrol strain CHA0 introduced into soil microcosms. Applied environmental microbiology, 60(7), 2553–2560.
O’Driscoll, A., Kildea, S., Doohan, F., Spink, J., & Mullins, E. (2014). The wheat–Septoria conflict: a new front opening up? Trends in plant science, 19(9), 602–610.
Palmer, C. L., & Skinner, W. (2002). Mycosphaerella graminicola: latent infection, crop devastation and genomics. Molecular plant pathology, 3(2), 63–70.
Pierson, E. A., & Weller, D. M. (1994). Use of mixtures of fluorescent pseudomonads to Suppress Take-all and Improve the Growth of Wheat. Phytopathology, 84, 940–947.
Ponomarenko, A., Goodwin, S., & Kema, G. H. (2011). Septoria tritici blotch (STB). Plant health instructor. https://doi.org/10.1094/PMI-I-2011-0407-01.
Porat, R., Vinokur, V., Weiss, B., Cohen, L., Daus, A., Goldschmidt, E. E., et al. (2003). Induction of resistance to Penicillium digitatum in grapefruit by β-aminobutyric acid. European journal of plant pathology, 109(9), 901–907.
Ramette, A., Frapolli, M., Fischer-Le Saux, M., Gruffaz, C., Meyer, J.-M., Défago, G., et al. (2011). Pseudomonas protegens sp. nov., widespread plant-protecting bacteria producing the biocontrol compounds 2, 4-diacetylphloroglucinol and pyoluteorin. Systematic and applied microbiology, 34(3), 180–188.
Rudd, J. J. (2015). Previous bottlenecks and future solutions to dissecting the Zymoseptoria tritici–wheat host-pathogen interaction. Fungal Genetics and Biology, 79, 24–28.
Sari, E., Etebarian, H. R., & Aminian, H. (2008). Effects of Pseudomonas fluorescens CHA0 on the resistance of wheat seedling roots to the take-all fungus Gaeumannomyces graminis var. tritici. Plant production science, 11(3), 298–306.
Schaad, N., Levy Häner, L., Bertossa, M., Michaud, L., Bernet, R., Girard, M., Courvoisier, N., Berberat, J., Grandgirard, R., Graf, B., Hofer, H., and Weisflog, T. (2019). Liste recommandée des variétés de céréales pour la récolte 2020. Recherche agronomique suisse 10 (6): enclosure.
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature methods, 9(7), 671–675.
Shetty, N., Kristensen, B., Newman, M.-A., Møller, K., Gregersen, P. L., & Jørgensen, H. L. (2003). Association of hydrogen peroxide with restriction of Septoria tritici in resistant wheat. Physiological and molecular plant pathology, 62(6), 333–346.
Siah, A., Deweer, C., Duyme, F., Sanssené, J., Durand, R., Halama, P., et al. (2010). Correlation of in planta endo-beta-1, 4-xylanase activity with the necrotrophic phase of the hemibiotrophic fungus Mycosphaerella graminicola. Plant PATHOLOGY, 59(4), 661–670.
Soleimani, M., & Kirk, W. (2012). Enhance resistance to Alternaria alternata causing potato brown leaf spot disease by using some plant defense inducers. Journal of plant protection research, 52(1), 83–90.
Sprouffske, K., & Wagner, A. (2016). Growthcurver: an R package for obtaining interpretable metrics from microbial growth curves. BMC bioinformatics, 17(1), 172.
Stewart, E. L., Hagerty, C. H., Mikaberidze, A., Mundt, C. C., Zhong, Z., & McDonald, B. A. (2016). An improved method for measuring quantitative resistance to the wheat pathogen Zymoseptoria tritici using high-throughput automated image analysis. Phytopathology, 106(7), 782–788.
Stutz, E., Défago, G., & Kern, H. (1986). Naturally occurring fluorescent pseudomonads involved in suppression of black root rot of tobacco. Phytopathology, 76(2), 181–185.
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.
Torriani, S. F., Melichar, J. P., Mills, C., Pain, N., Sierotzki, H., & Courbot, M. (2015). Zymoseptoria tritici: a major threat to wheat production, integrated approaches to control. Fungal genetics and biology, 79, 8–12.
Tziros, G. T., Lagopodi, A. L., & Tzavella-Klonari, K. (2007). Reduction of Fusarium wilt in watermelon by Pseudomonas chlororaphis PCL1391 and P. fluorescens WCS365. Phytopathologia mediterranea, 46(3), 320–323.
Vacheron, J., Desbrosses, G., Bouffaud, M.-L., Touraine, B., Moënne-Loccoz, Y., Muller, D., et al. (2013). Plant growth-promoting rhizobacteria and root system functioning. Frontiers in Plant Science, 4, 356.
Vallad, G. E., & Goodman, R. M. (2004). Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Science, 44(6), 1920–1934.
van Hulten, M., Pelser, M., Van Loon, L., Pieterse, C. M., & Ton, J. (2006). Costs and benefits of priming for defense in Arabidopsis. Proceedings of the national academy of sciences, 103(14), 5602–5607.
Vurukonda, S. S., Vardharajula, S., Shrivastava, M., & Sk, Z. A. (2016). Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiological research, 184, 13–24.
Wang, W., & Zhou, M. (2018). Recent advances in synthetic chemical inducers of plant immunity. Frontiers in Plant Science, 9, 1613.
Weller, D. M., Landa, B., Mavrodi, O., Schroeder, K., De La Fuente, L., Bankhead, S. B., et al. (2007). Role of 2, 4-diacetylphloroglucinol-producing fluorescent Pseudomonas spp. in the defense of plant roots. Plant biology, 9(01), 4–20.
Yu, G.-Y., & Muehlbauer, G. J. (2001). Benzothiadiazole-induced gene expression in wheat spikes does not provide resistance to Fusarium head blight. Physiological and molecular plant pathology, 59(3), 129–136.
Zhan, J., Kema, G. H., Waalwijk, C., & McDonald, B. A. (2002). Distribution of mating type alleles in the wheat pathogen Mycosphaerella graminicola over spatial scales from lesions to continents. Fungal genetics and biology, 36(2), 128–136.
Zhan, J., Linde, C. C., Jürgens, T., Merz, U., Steinebrunner, F., & McDonald, B. A. (2005). Variation for neutral markers is correlated with variation for quantitative traits in the plant pathogenic fungus Mycosphaerella graminicola. Molecular ecology, 14(9), 2683–2693.
Zimmerli, L., Jakab, G., Métraux, J.-P., & Mauch-Mani, B. (2000). Potentiation of pathogen-specific defense mechanisms in Arabidopsis by β-aminobutyric acid. Proceedings of the national academy of sciences, 97(23), 12,920–12,925.
Acknowledgements
We thank Daniel Croll, Leen Abraham and Nikhil Kumar Singh from the Evolutionary Genetics Laboratory, University of Neuchâtel, for technical support and advice to handle the STB pathogen. FB gratefully acknowledges the financial support by the Swiss Federal Commission for Scholarships for Foreign Students and BMM the financial support of the Swiss National Science Foundation, Grant No. 310030_160162).
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Bellameche, F., Pedrazzini, C., Mauch-Mani, B. et al. Efficiency of biological and chemical inducers for controlling Septoria tritici leaf blotch (STB) on wheat (Triticum aestivum L.). Eur J Plant Pathol 158, 99–109 (2020). https://doi.org/10.1007/s10658-020-02057-y
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DOI: https://doi.org/10.1007/s10658-020-02057-y