Systemic Signalling in Plant Defence

Abstract

Systemic signalling involves a complex network of signal transduction and amplification that leads to the activation of defence genes and establishment of systemic resistance throughout the entire plant. On microbial invasion, pathogen‐associated molecular patterns and effectors are frequently detected and recognised by plant receptors. Localised perception at the infection site rapidly triggers a cascade of early signalling events, including protein phosphorylation and production of reactive oxygen species. Subsequently, secondary signal molecules are synthesised and involved in amplification of defence signalling and the establishment of systemic acquired resistance (SAR). An increasing number of long‐distance signalling intermediates has been identified. Most of these act together and specifically promote systemic defence via the regulation of the local release of a set of systemically mobile signals. In the systemic tissue, the induction of SAR depends on synergistic interactions between systemic and ubiquitous salicylic acid‐associated immune signals.

Key Concepts

  • Local resistance to pathogen infection generally results from PAMP (pattern‐associated molecular pattern)‐triggered immunity and microbial effector‐triggered immunity.
  • Microbial infection of local tissues often leads to systemic acquired resistance (SAR) in distal tissues which provides long‐lasting broad‐spectrum resistance to a variety of pathogens.
  • Reactive oxygen species mediate systemic immunity acting as both cell‐to‐cell systemic signals and as local signalling partners upstream of other phloem‐mobile signals.
  • Mobile signals for SAR that are translocated via the vasculature may include methyl salicylate, the C9 lipid peroxidation product azelaic acid, one or more lipid transfer proteins, the diterpene dihydroabietinal and the nonprotein amino acid pipecolic acid.
  • Many of the SAR mobile signals cooperate with each other and with salicylic acid in one or more parallel and synergistic signalling pathways.
  • As a form of priming, SAR is supported by epigenetic regulation of defence gene expression.

Keywords: systemic acquired resistance; plant defence response; salicylic acid; long‐distance signalling; signal transduction

Figure 1. Hypersensitive response and systemic acquired resistance (SAR). Tobacco mosaic virus infection of tobacco cultivars carrying a disease resistance gene (e.g. N gene) leads to the HR (hypersensitive response) and subsequent establishment of SAR. The HR is characterised by host cell death and necrosis at the site of infection (left). Several days after the primary infection, SAR is induced throughout the plant. As a result, secondary infections of the plant with the same virus or other unrelated pathogens lead to much smaller lesions or weaker symptoms (right). The leaves are shown 4 days after viral infection.
Figure 2. A working model depicting local and systemic signalling events that are involved in the establishment of systemic immunity. Solid arrows represent established signalling interactions, broken arrows represent hypothetical signalling interactions, the double‐headed arrow represents a physical protein–protein interaction. Proteins are depicted in circles, metabolites are depicted in squares or non‐shape‐coded. Proteins and metabolites in red are putative phloem‐mobile signals. The broken red arrow depicts putative phloem transport, the blue arrows depict a systemic signalling event operating via cell‐to‐cell communication. See text for details and abbreviations.
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References

Alvarez ME, Pennell RI, Meijer PJ and Ishikawa RA (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92: 773–784.

Asai T, Tena G, Plotnikova J, et al. (2002) MAP kinase signaling cascade in Arabidopsis innate immunity. Nature 415: 977–983.

Attaran E, Zeier TE, Griebel T and Zeier J (2009) Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell 21: 954–971.

Beckers GJM, Jaskiewicz M, Liu Y, et al. (2009) Mitogen‐activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21: 944–953.

Bernsdorff F, Döring AC, Gruner K, et al. (2016) Pipecolic acid orchestrates plant systemic acquired resistance and defense priming via salicylic acid‐dependent and ‐independent pathways. Plant Cell 28: 102–129.

Breitenbach HH, Wenig M, Wittek F, et al. (2014) Contrasting roles of apoplastic aspartyl protease APOPLASTIC, ENHANCED DISEASE SUSCEPTIBILITY1‐DEPENDENT1 and LEGUME LECTIN‐LIKE PROTEIN1 in Arabidopsis systemic acquired resistance. Plant Physiology 165: 791–809.

Carella P, Isaacs M and Cameron RK (2015) Plasmodesmata‐located protein overexpression negatively impacts the manifestation of systemic acquired resistance and the long‐distance movement of Defective in Induced Resistance1 in Arabidopsis. Plant Biology 17: 395–401.

Cecchini NM, Steffes K, Schläppi MR, et al. (2015) Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming. Nature Communications 6: 7658.

Champigny MJ, Isaacs M, Carella P, et al (2013) Long distance movement of DIR1 and investigation of the role of DIR1‐like during systemic acquired resistance in Arabidopsis. Frontiers in Plant Science 4: 230.

Chanda B, Xia Y, Mandal MK, et al. (2011) Glycerol‐3‐phosphate is a critical mobile inducer of systemic immunity in plants. Nature Genetics 43: 421–427.

Chaturvedi R, Krothapalli K, Makandar R, et al. (2008) Plastid omega3‐fatty acid desaturase‐dependent accumulation of a systemic acquired resistance inducing activity in petiole exudates of Arabidopsis thaliana is independent of jasmonic acid. Plant Journal 54: 106–117.

Chaturvedi R, Venables B, Petros RA, et al. (2012) An abietane diterpenoid is a potent activator of systemic acquired resistance. Plant Journal 71: 161–172.

Dangl JL and Jones DGJ (2001) Plant pathogens and integrated defense responses to infection. Nature 411: 826–833.

Delaney T, Uknes S, Vernooij B, et al. (1994) A central role of salicylic acid in plant disease resistance. Science 266: 1247–1250.

Dodds PN, Lawrence GJ, Catanzariti AM, et al. (2006) Direct protein interaction underlies gene‐for‐gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proceedings of the National Academy of Sciences of the United States of America 103: 8888–8893.

Dubiella U, Seybold H, Durian G, et al. (2013) Calcium‐dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proceedings of the National Academy of Sciences of the United States of America 110: 8744–8749.

Fu ZQ, Yan S, Saleh A, et al. (2012) NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486: 228–232.

Fu ZQ and Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annual Review of Plant Biology 64: 7.1–7.25.

Hermann M, Maier F, Masroor A, et al. (2013) The Arabidopsis NIMIN proteins affect NPR1 differentially. Frontiers in Plant Science 4: 88.

Jaskiewicz M, Conrath U and Peterhänsel C (2011) Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Reports 12: 50–55.

Jones JDG and Dangl JL (2006) The plant immune system. Nature 444: 323–329.

Jung HW, Tschaplinski TJ, Wang L, Glazebrook J and Greenberg JT (2009) Priming in systemic plant immunity. Science 324: 89–91.

Lim GH, Shine MB, De Lorenzo L, et al. (2016) Plasmodesmata localizing proteins regulate transport and signaling during systemic acquired immunity in plants. Cell Host & Microbe 19: 541–549.

Liu P‐P, Von Dahl CC and Klessig DF (2011a) The extent to which methyl salicylate is required for signaling systemic acquired resistance is dependent on exposure to light after infection. Plant Physiology 157: 2216–2226.

Liu P‐P, von Dahl CC, Park S‐W and Klessig DF (2011b) Interconnection between methyl salicylate and lipid‐based long‐distance signaling during the development of systemic acquired resistance in Arabidopsis and tobacco. Plant Physiology 155: 1762–1768.

Luna E, Bruce TJA, Roberts MR, et al. (2012) Next‐generation systemic acquired resistance. Plant Physiology 158: 844–853.

Mackey D, Holt BF, Wiig A and Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1‐mediated resistance in Arabidopsis. Cell 108: 743–754.

Maldonado AM, Doerner P, Dixon RA, Lamb CJ and Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419: 399–403.

Manosalva PM, Park SW, Forouhar F, et al. (2010) Methyl esterase 1 (StMES1) is required for systemic acquired resistance in potato. Molecular Plant‐Microbe Interactions 23: 1151–1163.

Mishina TE and Zeier J (2006) The Arabidopsis flavin‐dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance. Plant Physiology 141: 1666–1675.

Mishina TE and Zeier J (2007) Pathogen‐associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant Journal 50: 500–513.

Návarová H, Bernsdorff F, Döring AC and Zeier J (2012) Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24: 5123–5141.

Park S‐W, Kaimoyo E, Kumar D, Mosher S and Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318: 113–116.

Pieterse CMJ, van Wees SC, van Pelt JA, et al. (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10: 1571–1580.

Rustérucci C, Espunya MC, Díaz M, Chabannes M and Martínez MC (2007) S‐Nitrosoglutathione reductase affords protection against pathogens in Arabidopsis, both locally and systemically. Plant Physiology 143: 1282–1292.

Saleh A, Withers J, Mohan R, et al. (2015) Posttranslational modifications of the master transcriptional regulator NPR1 enable dynamic but tight control of plant immune responses. Cell Host & Microbe 18: 169–182.

Shulaev V, Léon J and Raskin I (1997) Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385: 718–721.

Song F and Goodman RM (2001) Activity of nitric oxide is dependent on, but is partially required for function of, salicylic acid in the signaling pathway in tobacco systemic acquired resistance. Molecular Plant‐Microbe Interactions 14: 1458–1462.

Spoel SH, Johnson JS and Dong X (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proceedings of the National Academy of Sciences of the United States of America 104: 18842–18847.

Tada Y, Spoel SH, Pajerowska‐Mukhtar K, et al. (2008) Plant immunity requires conformational changes of NPR1 via S‐nitrosylation and thioredoxins. Science 321: 952–956.

Truman W, Bennett MH, Kubigsteltig I, Turnbull C and Grant M (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: 1075–1080.

Vernooij B, Freidrich L, Morse A, et al. (1994) Salicylic acid is not the signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6: 959–965.

Vlot AC, Liu PP, Cameron RK, et al (2008) Identification of likely orthologs of tobacco salicylic acid‐binding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. Plant Journal 56: 445–456.

Wang C, El‐Shetehy M, Shine MB, et al. (2014) Free radicals mediate systemic acquired resistance. Cell Reports 7: 348–355.

Wiermer M, Feys BJ and Parker JE (2005) Plant immunity: the EDS1 regulatory node. Current Opinion in Plant Biology 8: 383–389.

Wittek F, Hoffmann T, Kanawati B, et al. (2014) Arabidopsis ENHANCED DISEASE SUSCEPTIBILITY1 promotes systemic acquired resistance via azelaic acid and its precursor 9‐oxo nonanoic acid. Journal of Experimental Botany 65: 5919–5931.

Wendehenne D, Durner J and Klessig DF (2004) Nitric oxide: a new player in plant signaling and defense responses. Current Opinion in Plant Biology 7: 449–455.

Yu K, Soares JM, Mandal MK, et al. (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.

Zeidler D, Zähringer U, Gerber I, et al. (2004) Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proceedings of the National Academy of Sciences of the United States of America 101: 15811–15816.

Zoeller M, Stingl N, Krischke M, et al. (2012) Lipid profiling of the Arabidopsis hypersensitive response reveals specific lipid peroxidation and fragmentation processes: biogenesis of pimelic and azelaic acid. Plant Physiology 160: 365–378.

Further Reading

Conrath U, Beckers GJM, Langenbach CJG and Jaskiewicz MR (2015) Priming for enhanced defense. Annual Review of Phytopathology 53: 97–119.

Gao QM, Zhu S, Kachroo P and Kachroo A (2015) Signal regulators of systemic acquired resistance. Frontiers in Plant Science 6: 228.

Martinez‐Medina A, Flors V, Heil M, et al. (2016) Recognizing plant defense priming. Trends in Plant Science 21: 818–822.

Pieterse CMJ, Zamioudis C, Berendsen RL, et al. (2014) Induced systemic resistance by beneficial microbes. Annual Review of Phytopathology 52: 347–375.

Shah J, Chaturvedi R, Chowdhury Z, et al. (2014) Signaling by small metabolites in systemic acquired resistance. Plant Journal 79: 645–658.

Skelly MJ, Frungillo L and Spoel SH (2016) Transcriptional regulation by complex interplay between post‐translational modifications. Current Opinion in Plant Biology 33: 126–132.

Spoel SH and Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nature Reviews Immunology 12: 89–100.

Yan S and Dong X (2014) Perception of the plant immune signal salicylic acid. Current Opinion in Plant Biology 20: 64–68.

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Vlot, A Corina, Pabst, Elisabeth, and Riedlmeier, Marlies(Mar 2017) Systemic Signalling in Plant Defence. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001322.pub3]