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PMID: 21487047 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Intronic T-DNA insertion renders Arabidopsis opr3 a conditional jasmonic acid-producing mutant.

Plant physiology ·Vol. 156 ·No. 2 ·2011-06-00 ·Pages 770-8

Chehab EW, Kim S, Savchenko T, Kliebenstein D, Dehesh K, Braam J

Abstract

Jasmonic acid and its derived metabolites (JAs) orchestrate plant defense against insects and fungi. 12-Oxo-phytodienoic acid (OPDA), a JA precursor, has also been implicated in plant defense. We sought to define JAs and OPDA functions through comparative defense susceptibility characteristics of three Arabidopsis (Arabidopsis thaliana) genotypes: aos, lacking JAs and OPDA; opda reductase3 (opr3), deficient in JA production but can accumulate OPDA; and transgenics that overexpress OPR3. opr3, like aos, is susceptible to cabbage loopers (Trichoplusia ni) but, relative to aos, opr3 has enhanced resistance to a necrotrophic fungus. Gas chromatography-mass spectrometry reveals that opr3 produces OPDA but no detectable JAs following wounding and looper infestation; unexpectedly, substantial levels of JAs accumulate in opr3 upon fungal infection. Full-length OPR3 transcripts accumulate in fungal-infected opr3, potentially through splicing of the T-DNA containing intron. Fungal resistance correlates with levels of JAs not OPDA; therefore, opr3 resistance to some pests is likely due to JA accumulation, and signaling activities ascribed to OPDA should be reassessed because opr3 can produce JAs. Together these data (1) reinforce the primary role JAs play in plant defense against insects and necrotrophic fungi, (2) argue for a reassessment of signaling activities ascribed to OPDA, and (3) provide evidence that mutants with intron insertions can retain gene function.

MeSH Terms
Animals Arabidopsis/genetics,immunology,microbiology,parasitology Arabidopsis Proteins/genetics,metabolism Botrytis/drug effects,physiology Brassica/parasitology Cyclopentanes/metabolism,pharmacology DNA, Bacterial/genetics Fatty Acids, Unsaturated/metabolism Fertility/drug effects Gene Expression Regulation, Plant/drug effects Immunity, Innate/drug effects,immunology Indoles/metabolism Introns/genetics Molecular Sequence Data Moths/drug effects,physiology Mutagenesis, Insertional/drug effects,genetics Mutation/genetics Oxidoreductases/genetics,metabolism Oxylipins/metabolism,pharmacology Plant Diseases/immunology,microbiology,parasitology Thiazoles/metabolism
Chemicals
Arabidopsis Proteins Cyclopentanes DNA, Bacterial Fatty Acids, Unsaturated Indoles Oxylipins T-DNA Thiazoles camalexin 12-oxophytodienoic acid jasmonic acid OPR3 protein, Arabidopsis Oxidoreductases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Chehab E Wassim
Rice University, Houston, Texas 77005, USA.
Kim Se
Savchenko Tatyana
Kliebenstein Daniel
Dehesh Katayoon
Braam Janet
References (47)
47 references, click to expand
  1. Comparative analysis of quantitative trait loci controlling glucosinolates, myrosinase and insect resistance in Arabidopsis thaliana.
    Genetics. 2002 May;161(1):325-32 PMID: 12019246
  2. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  3. An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack.
    Plant Cell. 1996 Nov;8(11):2067-77 PMID: 8953771
  4. Crystal structure of 12-oxophytodienoate reductase 3 from tomato: self-inhibition by dimerization.
    Proc Natl Acad Sci U S A. 2006 Sep 26;103(39):14337-42 PMID: 16983071
  5. The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis.
    Proc Natl Acad Sci U S A. 2000 Sep 12;97(19):10625-30 PMID: 10973494
  6. Tissue-specific oxylipin signature of tomato flowers: allene oxide cyclase is highly expressed in distinct flower organs and vascular bundles.
    Plant J. 2000 Oct;24(1):113-26 PMID: 11029709
  7. Asymmetric bioreduction of activated alkenes using cloned 12-oxophytodienoate reductase isoenzymes OPR-1 and OPR-3 from Lycopersicon esculentum (tomato): a striking change of stereoselectivity.
    Angew Chem Int Ed Engl. 2007;46(21):3934-7 PMID: 17431865
  8. BIOSYNTHESIS AND ACTION OF JASMONATES IN PLANTS.
    Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:355-381 PMID: 15012267
  9. Identification of Botrytis cinerea susceptibility loci in Arabidopsis thaliana.
    Plant J. 2004 May;38(3):473-86 PMID: 15086796
  10. Enzymes in jasmonate biosynthesis - structure, function, regulation.
    Phytochemistry. 2009 Sep;70(13-14):1532-8 PMID: 19703696
  11. Simultaneous quantification of jasmonic acid and salicylic acid in plants by vapor-phase extraction and gas chromatography-chemical ionization-mass spectrometry.
    Anal Biochem. 2003 Jan 15;312(2):242-50 PMID: 12531212
  12. The role of oxophytodienoate reductases in the detoxification of the explosive 2,4,6-trinitrotoluene by Arabidopsis.
    Plant Physiol. 2009 Sep;151(1):253-61 PMID: 19605548
  13. Transcriptional responses to exposure to the brassicaceous defence metabolites camalexin and allyl-isothiocyanate in the necrotrophic fungus Alternaria brassicicola.
    Mol Plant Pathol. 2007 Mar;8(2):195-208 PMID: 20507491
  14. Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress.
    Proc Natl Acad Sci U S A. 1995 May 9;92(10):4114-9 PMID: 11607536
  15. A critical role of two positively charged amino acids in the Jas motif of Arabidopsis JAZ proteins in mediating coronatine- and jasmonoyl isoleucine-dependent interactions with the COI1 F-box protein.
    Plant J. 2008 Sep;55(6):979-88 PMID: 18547396
  16. COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine.
    Proc Natl Acad Sci U S A. 2008 May 13;105(19):7100-5 PMID: 18458331
  17. The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis.
    Plant Cell. 2004 Aug;16(8):2117-27 PMID: 15258265
  18. Distinct roles of jasmonates and aldehydes in plant-defense responses.
    PLoS One. 2008 Apr 02;3(4):e1904 PMID: 18382679
  19. Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid-isoleucine-mediated defenses against Manduca sexta.
    Plant Cell. 2006 Nov;18(11):3303-20 PMID: 17085687
  20. 12-oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis.
    Plant Cell. 2011 Feb;23(2):583-99 PMID: 21335376
  21. Role of beta-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato.
    Plant Cell. 2005 Mar;17(3):971-86 PMID: 15722469
  22. Secondary metabolites influence Arabidopsis/Botrytis interactions: variation in host production and pathogen sensitivity.
    Plant J. 2005 Oct;44(1):25-36 PMID: 16167893
  23. Plant defense in the absence of jasmonic acid: the role of cyclopentenones.
    Proc Natl Acad Sci U S A. 2001 Oct 23;98(22):12837-42 PMID: 11592974
  24. A downstream mediator in the growth repression limb of the jasmonate pathway.
    Plant Cell. 2007 Aug;19(8):2470-83 PMID: 17675405
  25. 12-oxo-phytodienoic acid triggers expression of a distinct set of genes and plays a role in wound-induced gene expression in Arabidopsis.
    Plant Physiol. 2005 Nov;139(3):1268-83 PMID: 16258017
  26. Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare.
    Plant J. 1998 Sep;15(6):747-54 PMID: 9807813
  27. Deficiencies in jasmonate-mediated plant defense reveal quantitative variation in Botrytis cinerea pathogenesis.
    PLoS Pathog. 2010 Apr 15;6(4):e1000861 PMID: 20419157
  28. The Critical Requirement for Linolenic Acid Is Pollen Development, Not Photosynthesis, in an Arabidopsis Mutant.
    Plant Cell. 1996 Mar;8(3):403-416 PMID: 12239389
  29. The role of JAR1 in Jasmonoyl-L: -isoleucine production during Arabidopsis wound response.
    Planta. 2008 May;227(6):1221-32 PMID: 18247047
  30. A role for jasmonate in pathogen defense of Arabidopsis.
    Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):7209-14 PMID: 9618564
  31. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling.
    Nature. 2007 Aug 9;448(7154):661-5 PMID: 17637677
  32. Arabidopsis potential calcium sensors regulate nitric oxide levels and the transition to flowering.
    Plant Signal Behav. 2007 Nov;2(6):446-54 PMID: 19517005
  33. Induction of the Arabidopsis PHO1;H10 gene by 12-oxo-phytodienoic acid but not jasmonic acid via a CORONATINE INSENSITIVE1-dependent pathway.
    Plant Physiol. 2008 Jun;147(2):696-706 PMID: 18434606
  34. Functional diversification of acyl-coenzyme A oxidases in jasmonic acid biosynthesis and action.
    Plant Physiol. 2007 Feb;143(2):812-24 PMID: 17172287
  35. 12-Oxophytodienoate reductase 3 (OPR3) is the isoenzyme involved in jasmonate biosynthesis.
    Planta. 2000 May;210(6):979-84 PMID: 10872231
  36. X-ray structure of Arabidopsis At2g06050, 12-oxophytodienoate reductase isoform 3.
    Proteins. 2005 Jan 1;58(1):243-5 PMID: 15468319
  37. The DEFECTIVE IN ANTHER DEHISCIENCE gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis.
    Plant Cell. 2001 Oct;13(10):2191-209 PMID: 11595796
  38. The JAZ family of repressors is the missing link in jasmonate signalling.
    Nature. 2007 Aug 9;448(7154):666-71 PMID: 17637675
  39. GATEWAY vectors for Agrobacterium-mediated plant transformation.
    Trends Plant Sci. 2002 May;7(5):193-5 PMID: 11992820
  40. The Arabidopsis epithiospecifier protein promotes the hydrolysis of glucosinolates to nitriles and influences Trichoplusia ni herbivory.
    Plant Cell. 2001 Dec;13(12):2793-807 PMID: 11752388
  41. Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut.
    Proc Natl Acad Sci U S A. 2005 Dec 27;102(52):19237-42 PMID: 16357201
  42. Wound-induced endogenous jasmonates stunt plant growth by inhibiting mitosis.
    PLoS One. 2008;3(11):e3699 PMID: 19002244
  43. A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis.
    Plant J. 2002 Jul;31(1):1-12 PMID: 12100478
  44. Rice HYDROPEROXIDE LYASES with unique expression patterns generate distinct aldehyde signatures in Arabidopsis.
    Plant Physiol. 2006 May;141(1):121-34 PMID: 16531481
  45. X-ray structure of 12-oxophytodienoate reductase 1 provides structural insight into substrate binding and specificity within the family of OYE.
    Structure. 2001 May 9;9(5):419-29 PMID: 11377202
  46. Methyljasmonate and α-linolenic acid are potent inducers of tendril coiling.
    Planta. 1991 Oct;185(3):316-22 PMID: 24186412
  47. The TASTY locus on chromosome 1 of Arabidopsis affects feeding of the insect herbivore Trichoplusia ni.
    Plant Physiol. 2001 Jun;126(2):890-8 PMID: 11402216
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
Published
2011-06-00
Epub
2011-00-12
Pages
770-8
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC3177274
Subset
IM
Databases
GENBANK
AF293653, AF344314
RefSeq
NM_100810, NM_106319, NM_179352, NM_201702, NM_202428
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