Abstract
Pseudomonas cannabina pv. alisalensis (Pcal), which causes bacterial blight of brassicaceous plants, is an economically important pathogen worldwide. Copper fungicide and antibiotics are major strategies to manage the disease caused by Pcal; however, a Pcal strain resistant to these chemicals has already been found, and severe outbreaks of bacterial blight have been reported on cabbage in Japan. Therefore, there is an urgent need to develop new Pcal management strategies. Plant defense activators could be useful not only to protect plants against invading pathogens, but also to reduce the amount of copper fungicides and antibiotics applied. However, the mechanisms by which plant defense activators contribute to controlling diseases remains unclear. In this work, we focused on cabbage and acibenzolar-S-methyl (ASM), a well-known plant defense activator. Expression profiles revealed that ASM induced expression of systemic acquired resistance (SAR) marker genes including PR1, PR2, and PR5 in cabbage plants. We also demonstrated that a soil drench with ASM 2 h before transplanting clearly reduced bacterial blight symptoms and reduced Pcal bacterial populations in cabbage. ASM application was also able to prime cabbage for Pcal resistance by activating stomatal-based defense. Our findings highlight that ASM protects plants from bacterial pathogens by activating stomatal-based defense.
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Bektas Y, Eulgem T (2015) Synthetic plant defense elicitors. Front Plant Sci 5:804
Chanda B, Xia Y, Mandal MK, Yu K, Sekine KT, Gao QM, Selote D, Hu Y, Stromberg A, Navarre D, Kachroo A, Kachroo P (2011) Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat Genet 43:421–427
Chaturvedi R, Venables B, Petros RA, Nalam V, Li M, Wang X, Takemoto LJ, Shah J (2012) An abietane diterpenoid is a potent activator of systemic acquired resistance. Plant J 71:161–172
Chitrakar R, Melotto M (2010) Assessing stomatal response to live bacterial cells using whole leaf imaging. J Vis Exp 44:e2185
Friedrich L, Lawton K, Ruess W, Masner P, Specker N, Rella MG, Meier B, Dincher S, Staub T, Uknes S, Métraux JP, Kessmann H, Ryals J (1996) A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant J 10:61–70
Görlach J, Volrath S, Knauf-Beiter G, Hengy G, Beckhove U, Kogel KH, Oostendorp M, Staub T, Ward E, Kessmann H, Ryals J (1996) Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8l:629–643.
Hacquard S, Spaepen S, Garrido-Oter R, Schulze-Lefert P (2017) Interplay between innate immunity and the plant microbiota. Annu Rev Phytopathol 55:565–589
Horinouchi H (2010) Occurrence and control of root browning symptom of Japanese radish caused by Pseudomonas syringae pv. maculicola (in Japanese). Plant Prot (Shokubutsu Boueki) 64:220–223
Ishiga Y, Ichinose Y (2016) Pseudomonas syringae pv. tomato OxyR is required for virulence in tomato and Arabidopsis. Mol Plant Microbe Interact 29:119–131
Ishiga T, Ishiga Y, Betsuyaku S, Nomura N (2018) AlgU contributes to the virulence of Pseudomonas syringae pv. tomato DC3000 by regulating production of the phytotoxin coronatine. J Gen Plant Pathol 84:189–201
Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329
Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Science 324:89–91
Keane PJ, Kerr A, New PB (1970) Crown gall of stone fruit II. Identification and nomenclature of Agrobacterium isolates. Aust J Biol Sci 23:585–595
Kunz W, Schurter R, Maetzke T (1997) The chemistry of benzothiadiazole plant activators. Pestic Sci 50:275–282
Lawton KA, Hunt Friedrich L, M, Weymann K, Delaney T, Kessmann H, Staub T, Ryals J, (1996) Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J 10:71–82
Lozano-Durán R, Bourdais G, He SY, Robatzek S (2014) The bacterial effector HopM1 suppresses PAMP-triggered oxidative burst and stomatal immunity. New Phytol 202:259–269
Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980
Melotto M, Underwood W, He SY (2008) Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytopathol 46:101–122
Melotto M, Zhang L, Oblessuc PR, He SY (2017) Stomatal defense a decade later. Plant Physiol 174:561–571
Morris SW, Vernooij B, Titatarn S, Starrett M, Thomas S, Wiltse CC, Frederiksen RA, Bhandhufalck A, Hulbert S, Uknes S, (1998) Induced resistance responses in maize. Mol Plant Microbe Interact 11:643–658
Oostendorp M, Kunz W, Dietrich B, Staub T (2001) Induced disease resistance in plants by chemicals. Eur J Plant Pathol 107:19–28
Prodhan MY, Issak M, Nakamura T, Munemasa S, Nakamura Y, Murata Y (2017) Chitosan signaling in guard cells requires endogenous salicylic acid. Biosci Biotechnol Biochem 81:1536–1541
Prodhan MY, Munemasa S, Nahar MN, Nakamura Y, Murata Y (2018) Guard cell salicylic acid signaling is integrated into abscisic acid signaling via the Ca2+/CPK-dependent pathway. Plant Physiol 178:441–450
Sarris PF, Trantas EA, Baltrus DA, Bull CT, Wechter WP, Yan S, Ververidis F, Almeida NF, Jones CD, Dangl JL, Panopoulos NJ, Vinatzer BA, Goumas DE (2013) Comparative genomics of multiple strains of Pseudomonas cannabina pv. alisalensis, a potential model pathogen of both monocots and dicots. PLoS ONE 8:59366
Takahashi F, Ochiai M, Ikeda K, Takikawa Y (2013a) Streptomycin and copper resistance in Pseudomonas cannabina pv. alisalensis (abstract in Japanese). Jpn J Phytopathol 79:35
Takahashi F, Ogiso H, Fujinaga M, Ishiyama Y, Inoue Y, Shirakawa T, Takikawa Y (2013b) First report of bacterial blight of crucifers caused by Pseudomonas cannabina pv. alisalensis in Japan. J Gen Plant Pathol 79:260–269
Takikawa Y, Takahashi F (2014) Bacterial leaf spot and blight of crucifer plants (Brassicaceae) caused by Pseudomonas syringae pv. maculicola and P. cannabina pv. alisalensis. J Gen Plant Pathol 80:466–474
Toum L, Torres PS, Gallego SM, Benavídes MP, Vojnov AA, Gudesblat GE (2016) Coronatine inhibits stomatal closure through guard cell-specific inhibition of NADPH oxidase-dependent ROS production. Front Plant Sci 7:1851
Tripathi D, Jiang YL, Kumar D (2010) SABP2, a methyl salicylate esterase is required for the systemic acquired resistance induced by acibenzolar-S-methyl in plants. FEBS Lett 584:3458–3463
Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusarenko A, Ward E, Ryals J (1992) Acquired resistance in Arabidopsis. Plant Cell 4:645–656
Underwood W, Melotto M, He SY (2007) Role of plant stomata in bacterial invasion. Cell Microbiol 9:1621–1629
Vlot AC, Liu PP, Cameron RK, Park SW, Yang Y, Kumar D, Zhou F, Padukkavidana T, Gustafsson C, Pichersky E, Klessig DF (2008) Identification of likely orthologs of tobacco salicylic acid-binding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. Plant J 56:445–456
Yu K, Soares J, Mandal MK, Wang C, Chanda B, Gifford AN, Fowler JS, Navarre D, Kachroo A, Kachroo P (2013) A feedback regulatory loop between G3P and lipid transfer proteins DIR1 and AZI1 mediates azelaic-acid-induced systemic immunity. Cell Reports 3:1266–1278
Zhou M, Wang W (2018) Recent advances in synthetic chemical inducers of plant immunity. Front Plant Sci 9:1613
Zipfel C (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20:10–16
Zipfel C, Felix G (2005) Plants and animals: a different taste for microbes? Curr Opin Plant Biol 8:353–360
Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767
Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760
Acknowledgements
We thank Dr. Christina Baker for editing the manuscript. Pcal was kindly provided by the Nagano Vegetable and Ornamental Crops Experiment Station, Nagano, Japan. This work was supported in part by the JST ERATO NOMURA Microbial Community Control Project, JST, Japan.
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Ishiga, T., Iida, Y., Sakata, N. et al. Acibenzolar-S-methyl activates stomatal-based defense against Pseudomonas cannabina pv. alisalensis in cabbage. J Gen Plant Pathol 86, 48–54 (2020). https://doi.org/10.1007/s10327-019-00883-5
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DOI: https://doi.org/10.1007/s10327-019-00883-5