title: Arabidopsis ENHANCED DISEASE SUSCEPTIBILITY1 promotes systemic acquired resistance via azelaic acid and its precursor 9-oxo nonanoic acid.
abstract: Systemic acquired resistance (SAR) is a form of inducible disease resistance that depends on salicylic acid and its upstream regulator ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1). Although local Arabidopsis thaliana defence responses activated by the Pseudomonas syringae effector protein AvrRpm1 are intact in eds1 mutant plants, SAR signal generation is abolished. Here, the SAR-specific phenotype of the eds1 mutant is utilized to identify metabolites that contribute to SAR. To this end, SAR bioassay-assisted fractionation of extracts from the wild type compared with eds1 mutant plants that conditionally express AvrRpm1 was performed. Using high-performance liquid chromatography followed by mass spectrometry, systemic immunity was associated with the accumulation of 60 metabolites, including the putative SAR signal azelaic acid (AzA) and its precursors 9-hydroperoxy octadecadienoic acid (9-HPOD) and 9-oxo nonanoic acid (ONA). Exogenous ONA induced SAR in systemic untreated leaves when applied at a 4-fold lower concentration than AzA. The data suggest that in planta oxidation of ONA to AzA might be partially responsible for this response and provide further evidence that AzA mobilizes Arabidopsis immunity in a concentration-dependent manner. The AzA fragmentation product pimelic acid did not induce SAR. The results link the C9 lipid peroxidation products ONA and AzA with systemic rather than local resistance and suggest that EDS1 directly or indirectly promotes the accumulation of ONA, AzA, or one or more of their common precursors possibly by activating one or more pathways that either result in the release of these compounds from galactolipids or promote lipid peroxidation.
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology, Ingolstaedter Landstr. 1, D-85764 Neuherberg, Germany.
authors.forename: Finni
authors.initials: F
authors.lastname: Wittek
authors.affiliation: Technical University Munich, Biotechnology of Natural Products, Liesel-Beckmann-Str. 1, D-85354 Freising, Germany.
authors.forename: Thomas
authors.initials: T
authors.lastname: Hoffmann
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Research Unit Analytical Biogeochemistry, Ingolstaedter Landstr. 1, D-85764 Neuherberg, Germany.
authors.forename: Basem
authors.initials: B
authors.lastname: Kanawati
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology, Ingolstaedter Landstr. 1, D-85764 Neuherberg, Germany.
authors.forename: Marlies
authors.initials: M
authors.lastname: Bichlmeier
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology, Ingolstaedter Landstr. 1, D-85764 Neuherberg, Germany.
authors.forename: Claudia
authors.initials: C
authors.lastname: Knappe
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology, Ingolstaedter Landstr. 1, D-85764 Neuherberg, Germany.
authors.forename: Marion
authors.initials: M
authors.lastname: Wenig
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Research Unit Analytical Biogeochemistry, Ingolstaedter Landstr. 1, D-85764 Neuherberg, Germany.
authors.forename: Philippe
authors.initials: P
authors.lastname: Schmitt-Kopplin
authors.affiliation: Max-Planck Institute for Plant Breeding Research, Department of Plant-Microbe Interactions, Carl-von-Linné-Weg 10, D-50829 Cologne, Germany.
authors.forename: Jane E
authors.initials: JE
authors.lastname: Parker
authors.affiliation: Technical University Munich, Biotechnology of Natural Products, Liesel-Beckmann-Str. 1, D-85354 Freising, Germany.
authors.forename: Wilfried
authors.initials: W
authors.lastname: Schwab
authors.affiliation: Helmholtz Zentrum Muenchen, Department of Environmental Sciences, Institute of Biochemical Plant Pathology, Ingolstaedter Landstr. 1, D-85764 Neuherberg, Germany corina.vlot@helmholtz-muenchen.de.
authors.forename: A Corina
authors.initials: AC
authors.lastname: Vlot
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000276:immunology* / Q000382:microbiology; D029681:Arabidopsis Proteins / Q000235:genetics* / Q000378:metabolism; D004268:DNA-Binding Proteins / Q000235:genetics* / Q000378:metabolism; D003998:Dicarboxylic Acids / Q000378:metabolism*; D060467:Disease Resistance; D005227:Fatty Acids / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant; D008041:Linoleic Acids / Q000378:metabolism; D008054:Lipid Peroxides / Q000378:metabolism; D010935:Plant Diseases / Q000276:immunology*; D018515:Plant Leaves / Q000235:genetics / Q000276:immunology / Q000382:microbiology; D044224:Pseudomonas syringae / Q000502:physiology; D020156:Salicylic Acid / Q000378:metabolism
chemical_list: C506899:9-hydroperoxy-10,12-octadecadienoic acid; D029681:Arabidopsis Proteins; D004268:DNA-Binding Proteins; D003998:Dicarboxylic Acids; C118837:EDS1 protein, Arabidopsis; D005227:Fatty Acids; D008041:Linoleic Acids; D008054:Lipid Peroxides; C008776:pelargonic acid; C010038:azelaic acid; D020156:Salicylic Acid
keywords: 9-oxo nonanoic acid; Arabidopsis thaliana; EDS1; azelaic acid; lipid peroxidation; systemic acquired resistance.
references.citation: Nature. 2002 Sep 26;419(6905):399-403
references.pmid: 12353036
references.citation: Trends Plant Sci. 2012 Sep;17(9):538-45
references.pmid: 22749315
references.citation: Nucleic Acids Res. 2014 Jan;42(Database issue):D199-205
references.pmid: 24214961
references.citation: Front Plant Sci. 2012 Oct 23;3:237
references.pmid: 23109935
references.citation: Plant Cell. 2012 Dec;24(12):5177-92
references.pmid: 23275581
references.citation: Cell. 2002 Mar 22;108(6):743-54
references.pmid: 11955429
references.citation: Front Plant Sci. 2013 Jul 04;4:230
references.pmid: 23847635
references.citation: Nucleic Acids Res. 2007 Jan;35(Database issue):D521-6
references.pmid: 17202168
references.citation: Mol Plant Pathol. 2010 Jan;11(1):155-60
references.pmid: 20078784
references.citation: Plant Cell. 2012 Dec;24(12):5123-41
references.pmid: 23221596
references.citation: Plant J. 2007 May;50(3):500-13
references.pmid: 17419843
references.citation: Plant J. 2012 Jul;71(1):161-72
references.pmid: 22385469
references.citation: J Exp Bot. 2014 Apr;65(7):1849-55
references.pmid: 24591049
references.citation: Mol Plant Microbe Interact. 2013 Dec;26(12):1395-406
references.pmid: 24006883
references.citation: Plant Physiol. 2013 Apr;161(4):1795-805
references.pmid: 23400705
references.citation: Plant Physiol. 2011 Nov;157(3):973-80
references.pmid: 21900483
references.citation: Plant J. 2006 Feb;45(4):472-89
references.pmid: 16441344
references.citation: Nat Immunol. 2011 Aug 18;12(9):817-26
references.pmid: 21852785
references.citation: PLoS Genet. 2009 Jul;5(7):e1000545
references.pmid: 19578402
references.citation: Annu Rev Plant Biol. 2013;64:429-50
references.pmid: 23451784
references.citation: Plant Physiol. 2004 Sep;136(1):2818-30
references.pmid: 15347794
references.citation: PLoS Pathog. 2010 Jul 01;6:e1000970
references.pmid: 20617163
references.citation: Plant Cell. 2005 Sep;17(9):2601-13
references.pmid: 16040633
references.citation: Nat Genet. 2011 May;43(5):421-7
references.pmid: 21441932
references.citation: Plant J. 2014 Aug;79(4):645-58
references.pmid: 24506415
references.citation: Science. 2011 Dec 9;334(6061):1401-4
references.pmid: 22158818
references.citation: Cell. 1997 Jan 10;88(1):57-63
references.pmid: 9019406
references.citation: Annu Rev Phytopathol. 2009;47:177-206
references.pmid: 19400653
references.citation: Plant Cell. 2008 Sep;20(9):2339-56
references.pmid: 18790826
references.citation: PLoS Genet. 2013;9(4):e1003465
references.pmid: 23633962
references.citation: Proc Natl Acad Sci U S A. 2007 Jan 16;104(3):1075-80
references.pmid: 17215350
references.citation: Nat Rev Immunol. 2012 Jan 25;12(2):89-100
references.pmid: 22273771
references.citation: Cell Host Microbe. 2013 Dec 11;14(6):619-30
references.pmid: 24331460
references.citation: Curr Opin Plant Biol. 2010 Aug;13(4):459-65
references.pmid: 20471306
references.citation: Plant Physiol. 2012 Sep;160(1):365-78
references.pmid: 22822212
references.citation: Cell Rep. 2013 Apr 25;3(4):1266-78
references.pmid: 23602565
references.citation: Science. 2011 Dec 9;334(6061):1405-8
references.pmid: 22158819
references.citation: Plant Cell Physiol. 2012 Feb;53(2):e1
references.pmid: 22123792
references.citation: Front Plant Sci. 2013 Feb 22;4:30
references.pmid: 23440336
references.citation: Proc Natl Acad Sci U S A. 2011 Sep 27;108(39):16463-8
references.pmid: 21911370
references.citation: Plant Physiol. 2006 Aug;141(4):1666-75
references.pmid: 16778014
references.citation: Plant J. 2008 Apr;54(1):106-17
references.pmid: 18088304
references.citation: Plant J. 2006 Aug;47(3):445-56
references.pmid: 16790029
references.citation: Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):10306-11
references.pmid: 9707643
references.citation: Science. 2009 Apr 3;324(5923):89-91
references.pmid: 19342588
references.citation: Nature. 2001 Nov 29;414(6863):562-5
references.pmid: 11734859
references.citation: New Phytol. 2011 Jul;191(1):107-119
references.pmid: 21434927
references.citation: Plant Cell. 2006 Apr;18(4):1038-51
references.pmid: 16531493
references.citation: Proc Natl Acad Sci U S A. 2004 Apr 6;101(14):5152-7
references.pmid: 15044700
references.citation: Nature. 2006 Nov 16;444(7117):323-9
references.pmid: 17108957
references.citation: Science. 2007 Oct 5;318(5847):113-6
references.pmid: 17916738
references.citation: PLoS Pathog. 2011 Nov;7(11):e1002318
references.pmid: 22072959
references.citation: Cell Rep. 2014 Apr 24;7(2):348-355
references.pmid: 24726369
references.citation: Plant Cell. 2001 Oct;13(10):2211-24
references.pmid: 11595797
references.citation: PLoS Genet. 2009 Dec;5(12):e1000772
references.pmid: 20011122
references.citation: Plant Physiol. 2014 Apr 22;165(2):791-809
references.pmid: 24755512
references.citation: Annu Rev Phytopathol. 2004;42:185-209
references.pmid: 15283665
references.citation: Annu Rev Plant Biol. 2013;64:839-63
references.pmid: 23373699
references.citation: Mol Plant. 2012 Jul;5(4):914-28
references.pmid: 22199234
references.citation: Plant J. 2010 May 1;62(4):628-40
references.pmid: 20163553
references.citation: Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):3292-7
references.pmid: 10077677