Systemic Signalling in Plant Defence

Emily E Helliwell, Pennsylvania State University, University Park, Pennsylvania, USA
Yinong Yang, Pennsylvania State University, University Park, Pennsylvania, USA

Published online: December 2009

DOI: 10.1002/9780470015902.a0001322.pub2

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 recognized by plant receptors. Localized perception at the infection site rapidly triggers a cascade of early signalling events such as ion fluxes, protein phosphorylation and production of reactive oxygen species. Subsequently, secondary signal molecules are synthesized and involved in amplification of defence signalling and the establishment of systemic acquired resistance. In addition, crosstalks often occur among various signalling pathways, which further modulate host defence in response to different types of pathogen attack.

Key concepts:

  • Local resistance to pathogen infection generally results from PAMP (pattern-associated molecular pattern)-triggered immunity, otherwise known as basal defence, and microbial effector-triggered immunity.
  • Microbial infection of local tissues often leads to systemic acquired resistance in distal tissues which provides long-lasting broad-spectrum resistance to a variety of pathogens.
  • Mobile signals for systemic acquired resistance are translocated via vasculature and may include small peptides such as AtPep1, methyl salicylate, jasmonate, azelaic acid and other lipid-derived molecules.
  • Both local and systemic resistance involve a complex network of signal transduction which includes extensive crosstalks among reactive oxygen species (e.g. hydrogen peroxide and nitric oxide), salicylic acid, jasmonic acid, ethylene, abscisic acid, auxin and MAP kinase signalling pathways.

Keywords: systemic acquired resistance; plant defence response; salicylic acid; jasmonic acid; signal transduction

Figure 1. Hypersensitive response and systemic acquired resistance. Tobacco mosaic virus infection of tobacco cultivars carrying a disease resistance gene (e.g. N gene) leads to the HR and subsequent establishment of SAR. The HR is characterized 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 four days after viral infection.
Figure 2. A working model depicting the initial perception of the invading pathogen, signal transduction and activation of defence response in local tissues, generation and translocation of systemic signals via vasculature, and establishment of SAR in distal tissues.
close
 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.
    Anderson JP, Badruzsaufari E, Schenk PM et al. (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16: 3460–3479.
    Arasimowicz M and Floryszak-Wieczorek J (2007) Nitric oxide as a bioactive signaling molecule in plant stress responses. Plant Science 172: 876–887.
    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.
    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.
    Chern M, Canlas PE, Fitzgerald HA and Ronald PC (2005) Rice NRR, a negative regulator of disease resistance, interacts with Arabidopsis NPR1 and rice NH1. Plant Journal 43: 623–635.
    Choi HW, Kim YJ, Lee SC, Hong JK and Hwang BK (2007) Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens. Plant Physiology 145: 890–904.
    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 USA 103: 8888–8893.
    Feys BJ, Wiermer M, Bhat RA et al. (2005) Arabidopsis SENESCENCE-ASSOCIATED GENE 101 stabilizes and signals within an enhanced disease susceptibility1 complex in plant innate immunity. Plant Cell 17: 2601–2613.
    Hufftaker A, Pearce G and Ryan CA (2006) An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proceedings of the National Academy of Sciences of the USA 103: 10098–10103.
    Huffaker A and Ryan CA (2007) Endogenous peptide defense signals in Arabidopsis differentially amplify signaling for the innate immune response. Proceedings of the National Academy of Sciences of the USA 104: 10732–10736.
    Jung HW, Tschaplinski TJ, Wang L, Glazebrook J and Greenberg JT (2009) Priming in systemic plant immunity. Science 324: 89–91.
    Li J, Brader G and Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16: 319–331.
    Lorenzo O, Piqueras R, Sanches-Serrano JJ and Solano R (2003) Ethylene response factor 1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15: 165–178.
    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.
    Mauch-Mani B and Mauch F (2005) The role of abscisic acid in plant–pathogen interactions. Current Opinion in Plant Biology 8: 409–414.
    Mosher RA, Durrant WE, Wang D, Song J and Dong X (2006) A comprehensive structure-function analysis of Arabidopsis SNI1 defines essential regions and transcriptional repressor activity. Plant Cell 18: 1750–1765.
    Mou Z, Fan W and Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113: 935–944.
    Mur LAJ, Kenton P, Atzorn R, Miersch O and Wasternack C (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: 249–262.
    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.
    Petersen M, Brodersen P, Naested H et al. (2000) Arabidopsis map kinase 4 negative regulates systemic acquired resistance. Cell 103: 1111–1120.
    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.
    Shulaev V, Léon J and Raskin I (1997) Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385: 718–721.
    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 USA 104: 18842–18847.
    Staswick PE (2007) JAZing up jasmonate signaling. Trends in Plant Science 13: 66–71.
    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 USA 104: 1075–1080.
    Verberne MC, Hoekstra J, Bol JF and Linthorst HJM (2003) Signaling of systemic acquired resistance in tobacco depends on ethylene perception. Plant Journal 35: 27–32.
    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.
    Vijayan P, Shockey J, Levesque CA, Cook RJ and Browse J (1998) A role for jasmonate in pathogen defense of Arabidopsis. Proceedings of the National Academy of Sciences of the USA 95: 7209–7214.
    Wang D, Pajerowska-Mukhtar K, Culler AH and Dong X (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Current Biology 17: 1784–1790.
    Weigel RR, Pfitzner UM and Gatz C (2005) Interaction of NIMIN1 with NPR1 modulates PR gene expression in Arabidopsis. Plant Cell 17: 1279–1291.
    Weirmer M, Feys BJ and Parker JE (2005) Plant immunity: the EDS1 regulatory node. Current Opinion in Plant Biology 8: 383–389.
    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.
    Yasuda M, Ishikawa A, Jikumaru Y et al. (2008) Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. Plant Cell 20: 1678–1692.
    Yamaguchi Y, Pearce G and Ryan CA (2006) The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. Proceedings of the National Academy of Sciences of the USA 103: 10104–10109.
    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 USA 101: 15811–15816.
    Zhang X, Dai Y, Xiong Y et al. (2007a) Overexpression of Arabidopsis MAP kinase kinase 7 leads to activation of plant basal and systemic acquired resistance. Plant Journal 52: 1066–1079.
    Zhang Z, Li Q, Zhimiao L et al. (2007b) Dual regulation role of GH3.5 in salicylic acid and auxin signaling during Arabidopsis–Pseudomonas syringae interaction. Plant Physiology 145: 450–464.
 Further Reading
    Bent AF and Mackey D (2007) Elicitors, effectors and R genes: the new paradigm and a lifetime supply of questions. Annual Review of Phytopathology 45: 399–436.
    Dong X (2004) NPR1, all things considered. Current Opinion in Plant Biology 7: 547–552.
    Durrant WE and Dong X (2004) Systemic acquired resistance. Annual Review of Phytopathology 42: 185–209.
    Grant M and Lamb C (2006) Systemic immunity. Current Opinion in Plant Biology 9: 414–420.
    Jones JDG and Dangl JL (2006) The plant immune system. Nature 444: 323–329.
    Vallad GE and Goodman RM (2004) Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Science 44: 1920–1934.
    Vlot AC, Klessig DF and Park S-W (2008) Systemic acquired resistance: the elusive signal(s). Current Opinion in Plant Biology 11: 436–442.

Related Sub-Topics:

Intracellular and Extracellular Signalling | Cell Signalling | Plant Disease | Plant Genetics and Molecular Biology
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Systemic Signalling in Plant Defence
 
How to Cite close
Helliwell, Emily E, and Yang, Yinong(Dec 2009) Systemic Signalling in Plant Defence. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001322.pub2]