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PMID: 15241470 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development.

The EMBO journal ·Vol. 23 ·No. 14 ·2004-07-21 ·Pages 2903-13

Xiao F, Goodwin SM, Xiao Y, Sun Z, Baker D, Tang X, Jenks MA, Zhou JM

Abstract

Pseudomonas syringae relies on type III secretion system to deliver effector proteins into the host cell for parasitism. Type III genes are induced in planta, but host factors affecting the induction are poorly understood. Here we report on the identification of an Arabidopsis mutant, att1 (for aberrant induction of type three genes), that greatly enhances the expression of bacterial type III genes avrPto and hrpL. att1 plants display enhanced disease severity to a virulent strain of P. syringae, suggesting a role of ATT1 in disease resistance. ATT1 encodes CYP86A2, a cytochrome P450 monooxygenase catalyzing fatty acid oxidation. The cutin content is reduced to 30% in att1, indicating that CYP86A2 plays a major role in the biosynthesis of extracellular lipids. att1 has a loose cuticle membrane ultrastructure and shows increased permeability to water vapor, demonstrating the importance of the cuticle membrane in controlling water loss. The enhanced avrPto-luc expression is specific to att1, but not another cuticle mutant, wax2. The results suggest that certain cutin-related fatty acids synthesized by CYP86A2 may repress bacterial type III gene expression in the intercellular spaces.

MeSH Terms
Amino Acid Sequence Arabidopsis/genetics,microbiology Cytochrome P-450 Enzyme System/chemistry,genetics,metabolism Gene Expression Regulation, Bacterial Genes, Bacterial Genes, Plant Membrane Lipids/analysis Molecular Sequence Data Mutation Plant Leaves/ultrastructure Plant Stems/growth & development,ultrastructure Pseudomonas syringae/genetics Sequence Homology, Amino Acid
Chemicals
Membrane Lipids cutin Cytochrome P-450 Enzyme System
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Xiao Fangming
Department of Plant Pathology, Kansas State University, Manhattan, KS, USA.
Goodwin S Mark
Xiao Yanmei
Sun Zhaoyu
Baker Douglas
Tang Xiaoyan
Jenks Matthew A
Zhou Jian-Min
References (40)
40 references, click to expand
  1. Transcriptional organization and expression of the large hrp gene cluster of Pseudomonas solanacearum.
    Mol Plant Microbe Interact. 1992 Mar-Apr;5(2):187-93 PMID: 1617200
  2. Transgenic Arabidopsis plants expressing a fungal cutinase show alterations in the structure and properties of the cuticle and postgenital organ fusions.
    Plant Cell. 2000 May;12(5):721-38 PMID: 10810146
  3. Enhanced green fluorescence by the expression of an Aequorea victoria green fluorescent protein mutant in mono- and dicotyledonous plant cells.
    Proc Natl Acad Sci U S A. 1996 Jun 11;93(12):5888-93 PMID: 8650188
  4. Polyesters in higher plants.
    Adv Biochem Eng Biotechnol. 2001;71:1-49 PMID: 11217409
  5. YscM1 and YscM2, two Yersinia enterocolitica proteins causing downregulation of yop transcription.
    Mol Microbiol. 1997 Nov;26(4):833-43 PMID: 9427412
  6. Use of green fluorescent protein to visualize the early events of symbiosis between Rhizobium meliloti and alfalfa (Medicago sativa).
    J Bacteriol. 1996 Dec;178(24):7159-66 PMID: 8955397
  7. Novel approaches to monitor bacterial gene expression in infected tissue and host.
    Curr Opin Microbiol. 2000 Feb;3(1):97-101 PMID: 10679414
  8. Cloning and characterization of the WAX2 gene of Arabidopsis involved in cuticle membrane and wax production.
    Plant Cell. 2003 May;15(5):1170-85 PMID: 12724542
  9. Type III secretion machines: bacterial devices for protein delivery into host cells.
    Science. 1999 May 21;284(5418):1322-8 PMID: 10334981
  10. Induction of type III secretion in Shigella flexneri is associated with differential control of transcription of genes encoding secreted proteins.
    EMBO J. 1998 May 15;17(10):2894-903 PMID: 9582283
  11. A low-viscosity epoxy resin embedding medium for electron microscopy.
    J Ultrastruct Res. 1969 Jan;26(1):31-43 PMID: 4887011
  12. A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis.
    Nature. 2002 Sep 26;419(6905):399-403 PMID: 12353036
  13. CYP86A1 from Arabidopsis thaliana encodes a cytochrome P450-dependent fatty acid omega-hydroxylase.
    Biochem Biophys Res Commun. 1998 Feb 24;243(3):688-93 PMID: 9500987
  14. Identification of a putative alternate sigma factor and characterization of a multicomponent regulatory cascade controlling the expression of Pseudomonas syringae pv. syringae Pss61 hrp and hrmA genes.
    J Bacteriol. 1994 Feb;176(4):1025-36 PMID: 8106313
  15. The Hrp pilus: learning from flagella.
    Curr Opin Microbiol. 2003 Feb;6(1):15-9 PMID: 12615214
  16. The acyl-CoA synthetase encoded by LACS2 is essential for normal cuticle development in Arabidopsis.
    Plant Cell. 2004 Mar;16(3):629-42 PMID: 14973169
  17. Role of the phytotoxin coronatine in the infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato.
    Mol Plant Microbe Interact. 1995 Jan-Feb;8(1):165-71 PMID: 7539639
  18. prhJ and hrpG, two new components of the plant signal-dependent regulatory cascade controlled by PrhA in Ralstonia solanacearum.
    Mol Microbiol. 1999 Jan;31(1):237-51 PMID: 9987125
  19. Functional expression in yeast and characterization of a clofibrate-inducible plant cytochrome P-450 (CYP94A1) involved in cutin monomers synthesis.
    Biochem J. 1998 Jun 1;332 ( Pt 2):583-9 PMID: 9601090
  20. Mechanism by which contact with plant cuticle triggers cutinase gene expression in the spores of Fusarium solani f. sp. pisi.
    Proc Natl Acad Sci U S A. 1986 Mar;83(6):1704-8 PMID: 16593666
  21. Functional analysis of the LACERATA gene of Arabidopsis provides evidence for different roles of fatty acid omega -hydroxylation in development.
    Proc Natl Acad Sci U S A. 2001 Aug 14;98(17):9694-9 PMID: 11493698
  22. Methyl jasmonate induces lauric acid omega-hydroxylase activity and accumulation of CYP94A1 transcripts but does not affect epoxide hydrolase activities in vicia sativa seedlings
    Plant Physiol. 1998 Dec;118(4):1481-6 PMID: 9847124
  23. Plant and environmental sensory signals control the expression of hrp genes in Pseudomonas syringae pv. phaseolicola.
    J Bacteriol. 1992 Jun;174(11):3499-507 PMID: 1592805
  24. The cloned avirulence gene avrPto induces disease resistance in tomato cultivars containing the Pto resistance gene.
    J Bacteriol. 1992 Mar;174(5):1604-11 PMID: 1537802
  25. Gene cluster of Pseudomonas syringae pv. "phaseolicola" controls pathogenicity of bean plants and hypersensitivity of nonhost plants.
    J Bacteriol. 1986 Nov;168(2):512-22 PMID: 3023280
  26. PrhA controls a novel regulatory pathway required for the specific induction of Ralstonia solanacearum hrp genes in the presence of plant cells.
    Mol Microbiol. 1998 Jan;27(2):437-53 PMID: 9484898
  27. omega-Hydroxylation of Z9-octadecenoic, Z9,10-epoxystearic and 9,10-dihydroxystearic acids by microsomal cytochrome P450 systems from Vicia sativa.
    Biochem Biophys Res Commun. 1992 Apr 15;184(1):183-93 PMID: 1567426
  28. Two simple media for the demonstration of pyocyanin and fluorescin.
    J Lab Clin Med. 1954 Aug;44(2):301-7 PMID: 13184240
  29. Cloning, expression in yeast, and functional characterization of CYP81B1, a plant cytochrome P450 that catalyzes in-chain hydroxylation of fatty acids.
    J Biol Chem. 1998 Mar 27;273(13):7260-7 PMID: 9516419
  30. Regulation of ExoS production and secretion by Pseudomonas aeruginosa in response to tissue culture conditions.
    Infect Immun. 1999 Feb;67(2):914-20 PMID: 9916108
  31. A signal transfer system through three compartments transduces the plant cell contact-dependent signal controlling Ralstonia solanacearum hrp genes.
    Mol Plant Microbe Interact. 2002 Feb;15(2):109-19 PMID: 11876423
  32. Molecular characterization and hrp dependence of the avirulence gene avrPto from Pseudomonas syringae pv. tomato [corrected].
    Mol Gen Genet. 1993 May;239(1-2):6-16 PMID: 8510663
  33. Modulation of virulence factor expression by pathogen target cell contact.
    Science. 1996 Aug 30;273(5279):1231-3 PMID: 8703058
  34. A bacterial sensor of plant cell contact controls the transcriptional induction of Ralstonia solanacearum pathogenicity genes.
    EMBO J. 2000 May 15;19(10):2304-14 PMID: 10811621
  35. Regulation of type III secretion systems.
    Curr Opin Microbiol. 2002 Apr;5(2):166-72 PMID: 11934613
  36. Expression of Erwinia amylovora hrp genes in response to environmental stimuli.
    J Bacteriol. 1992 Mar;174(6):1875-82 PMID: 1372313
  37. CYP94A5, a new cytochrome P450 from Nicotiana tabacum is able to catalyze the oxidation of fatty acids to the omega-alcohol and to the corresponding diacid.
    Eur J Biochem. 2001 May;268(10):3083-90 PMID: 11358528
  38. A protein kinase from Colletotrichum trifolii is induced by plant cutin and is required for appressorium formation.
    Mol Plant Microbe Interact. 2003 May;16(5):411-21 PMID: 12744512
  39. Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity.
    Science. 1989 Sep 22;245(4924):1374-7 PMID: 2781284
  40. Chemically Induced Cuticle Mutation Affecting Epidermal Conductance to Water Vapor and Disease Susceptibility in Sorghum bicolor (L.) Moench.
    Plant Physiol. 1994 Aug;105(4):1239-1245 PMID: 12232280
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2004-07-21
Epub
2004-00-08
Pages
2903-13
Language
English
Region
England
NLM ID
8208664
PMCID
PMC514950
Subset
IM
Grants
NCRR NIH HHS · P20 RR016443 · United States
NCRR NIH HHS · P20 RR16443-01 · United States
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