Arabidopsis ENHANCED DISEASE SUSCEPTIBILITY1 promotes systemic acquired resistance via azelaic acid and its precursor 9-oxo nonanoic acid

Journal of Experimental Botany

Volumn 65, Issue 20, 2014, Pages 5919-5931

  Wittek, Finni ^a   Hoffmann, Thomas ^b   Kanawati, Basem ^a   Bichlmeier, Marlies ^a   Knappe, Claudia ^a   Wenig, Marion ^a   Schmitt Kopplin, Philippe ^a   Parker, Jane E ^c   Schwab, Wilfried ^b   Vlot, A Corina ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

9 oxo nonanoic acid; Arabidopsis thaliana; azelaic acid; EDS1; lipid peroxidation; systemic acquired resistance

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

9-HYDROPEROXY-10,12-OCTADECADIENOIC ACID; ARABIDOPSIS PROTEIN; AZELAIC ACID; DICARBOXYLIC ACID; DNA BINDING PROTEIN; EDS1 PROTEIN, ARABIDOPSIS; FATTY ACID; LINOLEIC ACID; LIPID PEROXIDE; NONANOIC ACID; SALICYLIC ACID;

ARABIDOPSIS; DISEASE RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PSEUDOMONAS SYRINGAE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DICARBOXYLIC ACIDS; DISEASE RESISTANCE; DNA-BINDING PROTEINS; FATTY ACIDS; GENE EXPRESSION REGULATION, PLANT; LINOLEIC ACIDS; LIPID PEROXIDES; PLANT DISEASES; PLANT LEAVES; PSEUDOMONAS SYRINGAE; SALICYLIC ACID;

EID: 84913534139     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru331     Document Type: Article

References (63)

1. Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE. 1998. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Pro ceedings of the National Acadamy of Sciences, USA 95, 10306-10311.
2. Afendi FM, Okada T, Yamazaki M, et al. 2012. KNApSAcK family databases: integrated metabolite-plant species databases for multifaceted plan t research. Plant and Cell Physiology 53, e1.
3. Armijo G Salinas P Monteoliva MI Seguel A García C Villarroel-Candia E Song W Van der Krol AR Á lvarez ME Holuigue L. 2013. A salicylic acid-induced lectin-like protein plays a positive role in the effectortriggered immunity response of Arabidopsis thaliana to Pseudomonas syringae Avr-Rpm1. Molecular Plant-Microbe Interactions 26 1395-1406.
4. BartschS M, Gobb ato E, Bednarek P, Debey S, Schultze JL, Bautor J, Parker JE. 2006. Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the nu dix hydrolase NUDT7. The Plant Cell 18, 1038-1051.
5. Bhattacharjee S, Halane MK, Kim SH, Gassmann W. 2011. Pathogen effectors target Arabidopsis EDS1 and alter its interactions with immune regulators. Science 334, 1405-1408.
6. Bonardi V, Dangl JL. 2012. How complex are intracellular immune receptor signaling complexesfi Frontiers in Plant Science 3, 237.
7. Bonardi V, Tang S, Stallmann A, Roberts M, Cherkis K, Dangl JL. 2011. Expanded funct ions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. Proceedings of the National Academy of Sciences, USA 108, 16463-16468.
8. 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.
9. Cameron RK, Dixon RA, Lamb CJ. 1994. Biologically induced systemic acquired resistance in Arabidopsis thaliana. The Plant Journal 5, 715-725.
10. Cao H, Glazebrook J, Clarke JD, Volko S, Dong X. 1997. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88, 57-63.
11. Champigny MJ, Isaacs M, Carella P, Faubert J, Fober t PR, Cameron RK. 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.
12. Chanda B, Xia Y, Mand al MK, et al. 2011. Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nature Genetics 43, 421-427.
13. Chaturvedi R, Krothapalli K, Makandar R, Nandi A, Sparks AA, Ro th MR, Welti R, Shah J. 2008. Plastid omega 3-fatty acid desaturasedependent accumulation of a systemic acquired resistance inducing activity in petiole exudates of Arabidopsis thaliana is independent of jasmonic acid. The Plant Jour nal 54, 106-117.
14. 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. The Plan t Journal 71, 161-172.
15. Dempsey DA, Klessig DF. 2012. SOS-too many signals for systemic acquired resistancefi Trends in Plant Science 17, 538-545.
16. Durrant WE, Dong X. 2004. Systemic acquired resistance. Annual Reviews of Phytopathology 42, 185-209.
17. Falk A, Feys BJ, Frost LN, Jones JDG, Daniels MJ, Parker JE. 1999. EDS 1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proceedings of the National Academy of Sciences, USA 96, 3292-3297.
18. Farmer EE, Mueller MJ. 2013. ROS-mediated lipid peroxidation and RES-activated signaling. Annual Review of Plant Biology 64, 429-450.
19. Feys BJ, Wiermer M, Bhat RA, Moisan LJ, Medina-Escobar N, Neu C, Cabral A, Parker JE. 20 05. Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. The Plant Cell 17, 2601-2613.
20. Fu ZQ, Dong X. 2013. Systemi c acquired resistance: turning local infection into global defense. Annual Review of Plant Biology 64, 839-863.
21. Gao Q-M, Kachroo A, Kachroo P. 2014. Chemical inducers of systemic immunity in plants. Journal of Experimental Botany 65, 1849 -1855.
22. Garcia AV, Blanvillain-Baufume S, Huibers RP, Wiermer M, Li G, Gobbato E, Rietz S, Parker JE. 2010. Balanced nuclear and cytoplasmic activities of EDS1 a re required for a complete plant innate immune response. PLoS Pathogens 6, e1000970.
23. Heidrich K, Wirthmueller L, Tasset C, Pouzet C, Deslandes L, Parker JE. 2011. Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science 334, 1401-1404.
24. Jing B, Xu S, Xu M, Li Y, Li S, Ding J, Zhang Y. 2011. Brush and spray: a high-throughput systemic acq uired resistance assay suitable for largescale genetic screening. Plant Physiology 157, 973-980.
25. Jones JD Dangl JL. 2006 The plant immune system Nature 444 323-329
26. Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT. 2009. Priming in systemic plant immunity. Science 324, 89-91.
27. Kachroo A, Venugopal SC, Lapchyk L, Falcone D, Hildebrand D, Kachro o P. 2004. Oleic acid levels regulated by glycerolipid metabolism modulate defense gene expression in Arabidopsis. Proceedings of the National Academy of Sciences, USA 101, 5152-5157.
28. Kanehisa M, Goto S, Sa to Y, Kawashima M, Furumichi M, Tanabe M. 2014. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Research 42, D199-D205.
29. Kim T-H, Kunz H-H, Bhattacharjee S, et al. 2012. Natural variation in small molecule-induced TIR-NB-LRR signaling induces root growth arrest via EDS1-and PAD4-complexed R protein VICTR in Arabidopsis. The Plant Cell 24, 5177-5192.
30. Liu PP, Bhattacharjee S, Klessig DF, Moffett P. 2010. Systemic acquired resistance is induced by R gene-mediated responses independent of cell death. Molecular Plant Pathology 11, 155-160.
31. Mackey D, Holt BF, Wiig A, 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.
32. Maekawa T, Kufer TA, Schulze-Lefert P. 2011. NLR functions in plant and animal immune systems: so far and yet so close. Nature Immunology 12, 817-826.
33. Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK. 2002. A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419, 399-403.
34. Mateo A, Mü hlenbock P, Rustérucci C, Chang CC-C, Miszalski Z, Karpinska B, Parker JE, Mullineaux PM, Karpinski S. 2004. LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiology 136, 2818-2830.
35. Mishina TE, Zeier J. 2006. The Arabidopsis flavin-dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance. Plant Physiology 141, 1666-1675.
36. Mishina TE, Zeier J. 2007. Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. The Plant Journal 50, 500-513.
37. Mueller MJ, Mè ne-Saffrané L, Grun C, Karg K, Farmer EE. 2006. Oxylipin analysis methods. The Plant Journal 45, 472-489.
38. Mü hlenbock P, Szechynska-Hebda M, Plaszczyca M, Baudo M, Mateo A, Mullineaux PM, Parker JE, Karpinska B, Karpinski S. 2008. Chloroplast signaling and LESION SIMULATING DISEASE1 regulate crosstalk between light acclimation and immunity in Arabidopsis. The Plant Cell 20, 2339-2356.
39. Navarova H, Bernsdorff F, Doring AC, Zeier J. 2012. Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. The Plant Cell 24, 5123-5141.
40. Ochsenbein C, Przybyla D, Danon A, Landgraf F, Gobel C, Imboden A, Feussner I, Apel K. 2006. The role of EDS1 (enhanced disease susceptibility) during singlet oxygen-mediated stres s responses of Arabidopsis. The Plant Journal 47, 445-456.
41. Oliveros JC. 2007. VENNY. An interactive tool for comparing lists with Venn Diagrams. http://bioinfogp.cnb.csic.es/tools/venny/index.html.
42. Park SW, Ka imoyo E, Kumar D, Mosher S, Klessig DF. 2007. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318, 113-116.
43. Rietz S, Stamm A, Malonek S, Wagner S, Becker D, Medin a-Escobar N, Vlot AC, Feys BJ, Niefind K, Parker JE. 2011. Different roles of Enhanced Disease Susceptibility1 (EDS1) bound to and dissociated from Phytoalexin Deficient4 (PAD4) in Arabidopsis immunity. New Phytologist 191, 107-119.
44. Roberts M, Tang S, Stallmann A, Dangl JL, Bonardi V. 2013. Genetic requirements for signaling from an autoactive plant NB-LRR intracellular innate immune receptor. PLoS Genetics 9, e1003465.
45. Rusté rucci C, Aviv DH, Holt BF III, Dangl JL, Parker JE. 2001. The disease resistance signaling components EDS1 and PAD4 are essential regulators of the cell death pathway controlled by LSD1 in Arabidopsis. The Plan t Cell 13, 2211-2224.
46. Shah J, Chaturvedi R, Chowdhury Z, Venables B, Petros RA. 2014. Signaling by small metabolites in systemic acquired resistance. The Plant Journal (in press).
47. Shah J Zeier J 2013 Long-distance communication and signal amplification in systemic acquired resistance. Frontiers in Plant Science 4 30.
48. Spoel SH, Dong X. 2012. How do plants achieve immunityfi Defence without specialized immune cells. Nature Reviews Immunology 12, 89-100.
49. Straus MR, Rietz S, Ver Loren van Themaat E, Bartsch M, Parker JE. 2010. Salicylic acid antagonism of EDS1-driven cell death is important for immune and oxidative stress responses in Arabidopsis. The Plant Journal 62, 628-640.
50. Truman W, Bennett MH, Kubigsteltig I, Turnbull C, Grant M. 2007. Arabidopsis systemic imm unity uses conserved defense signaling pathways and is mediated by jasmonates. Proceedings of the National Acadamy of Sciences, USA 104, 1075-1080.
51. Tsuda K, Katagiri F. 2010. Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Current Opinion in Plant Biology 13, 459-465.
52. Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F. 2009. Network properties of robust immunity in plants. PLoS Genetics 5, e1000772.
53. Venugopal SC, Jeong RD, Mandal MK, et al. 2009. Enhanced disease susceptibility 1 and salicylic acid act redundantly to regulate resistance gene-mediated signaling . PLoS Genetics 5, e1000545.
54. Vicente J, Cascon T, Vicedo B, Garcia-Agustin P, Hamberg M, Castresana C. 2012. Role of 9-lipoxygenase and alpha-dioxygenase oxylipin pathways as modulators of loca l and systemic defense. Molecular Plant 5, 914-928.
55. Vlot AC, Dempsey DA, Klessig DF. 2009. Salicylic acid, a multifaceted hormone to combat disease. Annual Review of Phytopathology 47, 177-206.
56. Wagner S, Stuttmann J, Rietz S, Guerois R, Brunstein E, Bautor J, Niefind K, Parker JE. 2013. Structural basis for signaling by exclusive EDS1 heteromeric complexes with SAG101 or PAD4 in plant innate i mmunity. Cell Host and Microbe 14, 619-630.
57. Wang C, El-Shetehy M, Shine MB, Yu K, Navarre D, Wendehenne D, Kachroo A, Kachroo P. 2014. Free radicals mediate systemic acquired resistance. Cel l Reports 7, 348-355.
58. Wildermuth MC, Dewdney J, Wu G, Ausubel FM. 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414, 562-565.
59. Wishart DS, Tzur D, Knox C, et al. 2007. HMDB: the human metabolome database. Nucleic Acids Research 35, D521-D526.
60. Wituszynska W, Slesak I, Vanderauwera S, et al. 2013. LESION SIMULATING DISEASE1, ENHANCED DISEASE SUSCEPTIBILITY1, and PHYTOALEXIN DEFICIENT4 conditionally regulate cellular signaling homeostasis, photosynthesis, water use efficiency, and seed yield in Arabidopsis. Plant Physiology 161, 1795 -1805.
61. Yu K, Soares JM, 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 azelaicacid-induced systemic immunity. Cell Reports 3, 1266-1278.
62. Zhu S, Jeong RD, Venugopal SC, Lapchyk L, Navarre D, Kachroo A, Kachroo P. 2011. SAG101 forms a ternary complex with E DS1 and PAD4 and is required for resistance signaling against turnip crinkle virus. PLoS Pathogens 7, e1002318.
63. Zoeller M, Stingl N, Krischke M, Fekete A, Waller F, Berger S, Mueller MJ. 2012. L ipid profiling of the Arabidopsis hypersensitive response reveals specific lipid peroxidation and fragmentation processes: biogenesis of pimelic and azelaic acid. Plant Physiology 160, 365-378.