Home LiteratureArticle Details
PMID: 23757404 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Export of salicylic acid from the chloroplast requires the multidrug and toxin extrusion-like transporter EDS5.

Plant physiology ·Vol. 162 ·No. 4 ·2013-08-00 ·Pages 1815-21

Serrano M, Wang B, Aryal B, Garcion C, Abou-Mansour E, Heck S, Geisler M, Mauch F, Nawrath C, Métraux JP

Abstract

Salicylic acid (SA) is central for the defense of plants to pathogens and abiotic stress. SA is synthesized in chloroplasts from chorismic acid by an isochorismate synthase (ICS1); SA biosynthesis is negatively regulated by autoinhibitory feedback at ICS1. Genetic studies indicated that the multidrug and toxin extrusion transporter ENHANCED DISEASE SUSCEPTIBILITY5 (EDS5) of Arabidopsis (Arabidopsis thaliana) is necessary for SA accumulation after biotic and abiotic stress, but so far it is not understood how EDS5 controls the biosynthesis of SA. Here, we show that EDS5 colocalizes with a marker of the chloroplast envelope and that EDS5 functions as a multidrug and toxin extrusion-like transporter in the export of SA from the chloroplast to the cytoplasm in Arabidopsis, where it controls the innate immune response. The location at the chloroplast envelope supports a model of the effect of EDS5 on SA biosynthesis: in the eds5 mutant, stress-induced SA is trapped in the chloroplast and inhibits its own accumulation by autoinhibitory feedback.

MeSH Terms
Arabidopsis/drug effects,physiology,radiation effects Arabidopsis Proteins/genetics,metabolism Biological Transport Carbonyl Cyanide m-Chlorophenyl Hydrazone/pharmacology Chloroplasts/genetics,metabolism Cytoplasm/genetics,metabolism Immunity, Innate Membrane Transport Proteins/genetics,metabolism Molecular Sequence Data Mutation Nigericin/pharmacology Plants, Genetically Modified Protoplasts/metabolism Salicylic Acid/metabolism Ultraviolet Rays
Chemicals
Arabidopsis Proteins EDS5 protein, Arabidopsis Membrane Transport Proteins Carbonyl Cyanide m-Chlorophenyl Hydrazone Salicylic Acid Nigericin
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Serrano Mario
Department of Biology, University of Fribourg, 1700 Fribourg, Switzerland.
Wang Bangjun
Aryal Bibek
Garcion Christophe
Abou-Mansour Eliane
Heck Silvia
Geisler Markus
Mauch Felix
Nawrath Christiane
Métraux Jean-Pierre
References (31)
31 references, click to expand
  1. Defining the core proteome of the chloroplast envelope membranes.
    Front Plant Sci. 2013 Feb 06;4:11 PMID: 23390424
  2. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  3. Manipulation of salicylate content in Arabidopsis thaliana by the expression of an engineered bacterial salicylate synthase.
    Plant J. 2001 Jan;25(1):67-77 PMID: 11169183
  4. Salicylic Acid, a multifaceted hormone to combat disease.
    Annu Rev Phytopathol. 2009;47:177-206 PMID: 19400653
  5. Vitamin K1 accumulation in tobacco plants overexpressing bacterial genes involved in the biosynthesis of salicylic acid.
    J Biotechnol. 2007 Jan 30;128(1):72-9 PMID: 17084477
  6. Tic21 is an essential translocon component for protein translocation across the chloroplast inner envelope membrane.
    Plant Cell. 2006 Sep;18(9):2247-57 PMID: 16891400
  7. Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1.
    Plant J. 2005 Oct;44(2):179-94 PMID: 16212599
  8. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants.
    Nature. 2012 May 16;486(7402):228-32 PMID: 22699612
  9. The MATE proteins as fundamental transporters of metabolic and xenobiotic organic cations.
    Trends Pharmacol Sci. 2006 Nov;27(11):587-93 PMID: 16996621
  10. On the origin of family 1 plant glycosyltransferases.
    Phytochemistry. 2003 Feb;62(3):399-413 PMID: 12620353
  11. Requirement of salicylic Acid for the induction of systemic acquired resistance.
    Science. 1993 Aug 6;261(5122):754-6 PMID: 17757215
  12. A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum.
    Nat Genet. 2007 Sep;39(9):1156-61 PMID: 17721535
  13. A homolog of Escherichia coli RecA protein in plastids of higher plants.
    Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):8068-72 PMID: 1518831
  14. EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family.
    Plant Cell. 2002 Jan;14(1):275-86 PMID: 11826312
  15. Arabidopsis isochorismate synthase functional in pathogen-induced salicylate biosynthesis exhibits properties consistent with a role in diverse stress responses.
    J Biol Chem. 2007 Feb 23;282(8):5919-33 PMID: 17190832
  16. Salicylic acid production in response to biotic and abiotic stress depends on isochorismate in Nicotiana benthamiana.
    FEBS Lett. 2008 Feb 20;582(4):473-8 PMID: 18201575
  17. The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+ -antiporter active in proanthocyanidin-accumulating cells of the seed coat.
    Plant Cell. 2007 Jun;19(6):2023-38 PMID: 17601828
  18. Salicylic Acid Is Not the Translocated Signal Responsible for Inducing Systemic Acquired Resistance but Is Required in Signal Transduction.
    Plant Cell. 1994 Jul;6(7):959-965 PMID: 12244262
  19. The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium.
    Plant Cell. 2001 Apr;13(4):853-71 PMID: 11283341
  20. Two functionally distinct members of the MATE (multi-drug and toxic compound extrusion) family of transporters potentially underlie two major aluminum tolerance QTLs in maize.
    Plant J. 2010 Mar;61(5):728-40 PMID: 20003133
  21. Vacuolar transport of nicotine is mediated by a multidrug and toxic compound extrusion (MATE) transporter in Nicotiana tabacum.
    Proc Natl Acad Sci U S A. 2009 Feb 17;106(7):2447-52 PMID: 19168636
  22. Arabidopsis ABCB21 is a facultative auxin importer/exporter regulated by cytoplasmic auxin concentration.
    Plant Cell Physiol. 2012 Dec;53(12):2090-100 PMID: 23147222
  23. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis.
    Nat Protoc. 2007;2(7):1565-72 PMID: 17585298
  24. Multidrug and toxic compound extrusion-type transporters implicated in vacuolar sequestration of nicotine in tobacco roots.
    Plant Physiol. 2009 Feb;149(2):708-18 PMID: 19098091
  25. Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins.
    J Biol Chem. 2008 Aug 1;283(31):21817-26 PMID: 18499676
  26. OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice.
    Plant Physiol. 2009 Jan;149(1):297-305 PMID: 19011004
  27. Isolation and preparation of chloroplasts from Arabidopsis thaliana plants.
    Methods Mol Biol. 2008;425:171-86 PMID: 18369897
  28. Isochorismate synthase is required to synthesize salicylic acid for plant defence.
    Nature. 2001 Nov 29;414(6863):562-5 PMID: 11734859
  29. ADP-D-glucose-alpha-i,4-glucan alpha-4-glucosyltransferase in spinach chloroplasts. Partial purification and some properties of the enzyme.
    Biochim Biophys Acta. 1966 Feb 14;113(2):312-20 PMID: 5942432
  30. Salicylic acid and its location in response to biotic and abiotic stress.
    FEBS Lett. 2011 Jun 23;585(12):1847-52 PMID: 21530511
  31. Multidrug efflux transporters in the MATE family.
    Biochim Biophys Acta. 2009 May;1794(5):763-8 PMID: 19100867
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
Published
2013-08-00
Epub
2013-00-11
Pages
1815-21
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC3729763
Subset
IM
Databases
GENBANK
AF416569
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com