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PMID: 17322408 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Thioredoxin h5 is required for victorin sensitivity mediated by a CC-NBS-LRR gene in Arabidopsis.

The Plant cell ·Vol. 19 ·No. 2 ·2007-02-00 ·Pages 673-87

Sweat TA, Wolpert TJ

Abstract

The fungus Cochliobolus victoriae causes Victoria blight of oats (Avena sativa) and is pathogenic due to its production of victorin, which induces programmed cell death in sensitive plants. Victorin sensitivity has been identified in Arabidopsis thaliana and is conferred by the dominant gene LOCUS ORCHESTRATING VICTORIN EFFECTS1 (LOV1), which encodes a coiled-coil-nucleotide binding site-leucine-rich repeat protein. We isolated 63 victorin-insensitive mutants, including 59 lov1 mutants and four locus of insensitivity to victorin1 (liv1) mutants. The LIV1 gene encodes thioredoxin h5 (ATTRX5), a member of a large family of disulfide oxidoreductases. To date, very few plant thioredoxins have been assigned specific, nonredundant functions. We found that the victorin response was highly specific to ATTRX5, as the closely related ATTRX3 could only partially compensate for loss of ATTRX5, even when overexpressed. We also created chimeric ATTRX5/ATTRX3 proteins, which identified the central portion of the protein as important for conferring specificity to ATTRX5. Furthermore, we found that ATTRX5, but not ATTRX3, is highly induced in sensitive Arabidopsis following victorin treatment. Finally, we determined that only the first of the two active-site Cys residues in ATTRX5 is required for the response to victorin, suggesting that ATTRX5 function in the victorin pathway involves an atypical mechanism of action.

MeSH Terms
Amino Acid Sequence Arabidopsis/genetics,microbiology,physiology Arabidopsis Proteins/genetics,metabolism Binding Sites Cysteine/metabolism Fungal Proteins/metabolism Gene Expression Regulation, Plant Genetic Complementation Test Leucine-Rich Repeat Proteins Molecular Sequence Data Mutation Mycotoxins/metabolism Phenotype Plant Proteins/genetics,metabolism Plants, Genetically Modified Protein Conformation Proteins/genetics,metabolism Recombinant Fusion Proteins/genetics,metabolism Sequence Alignment Thioredoxin h Thioredoxin-Disulfide Reductase/genetics,metabolism Thioredoxins/genetics,metabolism
Chemicals
ATH5 protein, Arabidopsis ATTRX3 protein, Arabidopsis Arabidopsis Proteins Fungal Proteins Leucine-Rich Repeat Proteins Mycotoxins Plant Proteins Proteins Recombinant Fusion Proteins Thioredoxin h Victorin protein, Cochliobolus victoriae Thioredoxins Thioredoxin-Disulfide Reductase Cysteine
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Sweat Teresa A
Department of Botany and Plant Pathology, Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon 97331-2902, USA.
Wolpert Thomas J
References (59)
59 references, click to expand
  1. Further analysis of the interactions between the Brassica S receptor kinase and three interacting proteins (ARC1, THL1 and THL2) in the yeast two-hybrid system.
    Plant Mol Biol. 2001 Feb;45(3):365-76 PMID: 11292081
  2. Target proteins of the cytosolic thioredoxins in Arabidopsis thaliana.
    Plant Cell Physiol. 2004 Jan;45(1):18-27 PMID: 14749482
  3. Simulation of fungal-mediated cell death by fumonisin B1 and selection of fumonisin B1-resistant (fbr) Arabidopsis mutants.
    Plant Cell. 2000 Oct;12(10):1811-22 PMID: 11041878
  4. An NADP/thioredoxin system in leaves: purification and characterization of NADP-thioredoxin reductase and thioredoxin h from spinach.
    Arch Biochem Biophys. 1988 Nov 1;266(2):496-507 PMID: 3190242
  5. A novel plasma membrane-bound thioredoxin from soybean.
    Plant Mol Biol. 1996 Nov;32(4):653-62 PMID: 8980517
  6. Proteomics gives insight into the regulatory function of chloroplast thioredoxins.
    Proc Natl Acad Sci U S A. 2003 Jan 7;100(1):370-5 PMID: 12509500
  7. Arabidopsis Mutants Selected for Resistance to the Phytotoxin Coronatine Are Male Sterile, Insensitive to Methyl Jasmonate, and Resistant to a Bacterial Pathogen.
    Plant Cell. 1994 May;6(5):751-759 PMID: 12244256
  8. Differential reactivity of the functional sulfhydryl groups of cysteine-32 and cysteine-35 present in the reduced form of thioredoxin from Escherichia coli.
    J Biol Chem. 1980 Nov 10;255(21):10261-5 PMID: 7000775
  9. Thioredoxin catalyzes the S-nitrosation of the caspase-3 active site cysteine.
    Nat Chem Biol. 2005 Aug;1(3):154-8 PMID: 16408020
  10. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  11. Exploiting the triple response of Arabidopsis to identify ethylene-related mutants.
    Plant Cell. 1990 Jun;2(6):513-23 PMID: 2152173
  12. The oat mitochondrial permeability transition and its implication in victorin binding and induced cell death.
    Plant J. 2002 Feb;29(3):295-312 PMID: 11844107
  13. The role and regulation of programmed cell death in plant-pathogen interactions.
    Cell Microbiol. 2004 Mar;6(3):201-11 PMID: 14764104
  14. CITRX thioredoxin is a putative adaptor protein connecting Cf-9 and the ACIK1 protein kinase during the Cf-9/Avr9- induced defence response.
    FEBS Lett. 2006 Jul 24;580(17):4236-41 PMID: 16831430
  15. Cytochrome C-mediated apoptosis.
    Annu Rev Biochem. 2004;73:87-106 PMID: 15189137
  16. Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria.
    Proc Natl Acad Sci U S A. 2004 Feb 24;101(8):2642-7 PMID: 14983062
  17. Characterization of determinants for the specificity of Arabidopsis thioredoxins h in yeast complementation.
    J Biol Chem. 2000 Oct 13;275(41):31641-7 PMID: 10906327
  18. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens.
    Annu Rev Phytopathol. 2005;43:205-27 PMID: 16078883
  19. NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen.
    Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6597-601 PMID: 11607554
  20. Arabidopsis AtSPL14, a plant-specific SBP-domain transcription factor, participates in plant development and sensitivity to fumonisin B1.
    Plant J. 2005 Mar;41(5):744-54 PMID: 15703061
  21. Host-selective toxins and avirulence determinants: what's in a name?
    Annu Rev Phytopathol. 2002;40:251-85 PMID: 12147761
  22. AtNTRB is the major mitochondrial thioredoxin reductase in Arabidopsis thaliana.
    FEBS Lett. 2005 Jan 17;579(2):337-42 PMID: 15642341
  23. Identification and characterization of victorin sensitivity in Arabidopsis thaliana.
    Mol Plant Microbe Interact. 2004 Jun;17(6):577-82 PMID: 15195940
  24. The plant thioredoxin system.
    Cell Mol Life Sci. 2005 Jan;62(1):24-35 PMID: 15619004
  25. The S-locus receptor kinase is inhibited by thioredoxins and activated by pollen coat proteins.
    Nature. 2001 Mar 8;410(6825):220-3 PMID: 11242083
  26. Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa.
    Plant Cell. 2004 Apr;16(4):857-73 PMID: 15020745
  27. Selection and regeneration of toxin-insensitive plants from tissue cultures of oats (Avena sativa) susceptible to Helminthosporium victoriae.
    Theor Appl Genet. 1985 Nov;71(1):16-21 PMID: 24247332
  28. Victorin induction of an apoptotic/senescence-like response in oats.
    Plant Cell. 1999 Feb;11(2):237-49 PMID: 9927641
  29. A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase.
    Proc Natl Acad Sci U S A. 2004 Oct 5;101(40):14545-50 PMID: 15385674
  30. Mitochondrial oxidative burst involved in apoptotic response in oats.
    Plant J. 2002 Jun;30(5):567-79 PMID: 12047631
  31. Gateway-compatible vectors for plant functional genomics and proteomics.
    Plant J. 2006 Feb;45(4):616-29 PMID: 16441352
  32. Redox regulation: a broadening horizon.
    Annu Rev Plant Biol. 2005;56:187-220 PMID: 15862094
  33. Early embryonic lethality caused by targeted disruption of the mouse thioredoxin gene.
    Dev Biol. 1996 Aug 25;178(1):179-85 PMID: 8812119
  34. Identification and characterization of a mitochondrial thioredoxin system in plants.
    Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):14144-9 PMID: 11717467
  35. Plant thioredoxins are key actors in the oxidative stress response.
    Trends Plant Sci. 2006 Jul;11(7):329-34 PMID: 16782394
  36. Comprehensive survey of proteins targeted by chloroplast thioredoxin.
    Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11224-9 PMID: 11553771
  37. Changes in Permeability Induced by Victorin.
    Science. 1962 Sep 21;137(3534):983-4 PMID: 17782735
  38. Two members of the thioredoxin-h family interact with the kinase domain of a Brassica S locus receptor kinase.
    Plant Cell. 1996 Sep;8(9):1641-50 PMID: 8837514
  39. Electrical Membrane Properties of Leaves, Roots, and Single Root Cap Cells of Susceptible Avena sativa: Effect of Victorin C.
    Plant Physiol. 1991 Mar;95(3):675-81 PMID: 16668038
  40. A New Helminthosporium Blight of Oats.
    Science. 1946 Nov 1;104(2705):413-4 PMID: 17814758
  41. The Arabidopsis cytosolic thioredoxin h5 gene induction by oxidative stress and its W-box-mediated response to pathogen elicitor.
    Plant Physiol. 2004 Mar;134(3):1006-16 PMID: 14976236
  42. Novel evidence for apoptotic cell response and differential signals in chromatin condensation and DNA cleavage in victorin-treated oats.
    Plant J. 2001 Oct;28(1):13-26 PMID: 11696183
  43. Plant disease resistance protein signaling: NBS-LRR proteins and their partners.
    Curr Opin Plant Biol. 2004 Aug;7(4):391-9 PMID: 15231261
  44. The absence of mitochondrial thioredoxin 2 causes massive apoptosis, exencephaly, and early embryonic lethality in homozygous mice.
    Mol Cell Biol. 2003 Feb;23(3):916-22 PMID: 12529397
  45. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1.
    EMBO J. 1998 May 1;17(9):2596-606 PMID: 9564042
  46. The victorin-induced mitochondrial permeability transition precedes cell shrinkage and biochemical markers of cell death, and shrinkage occurs without loss of membrane integrity.
    Plant J. 2004 Apr;38(2):244-59 PMID: 15078328
  47. Large-scale structure-function analysis of the Arabidopsis RPM1 disease resistance protein.
    Plant Cell. 2002 Feb;14(2):435-50 PMID: 11884685
  48. Host-selective toxins: agents of compatibility.
    Plant Cell. 1996 Oct;8(10):1723-33 PMID: 8914323
  49. RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes.
    Science. 1994 Sep 23;265(5180):1856-60 PMID: 8091210
  50. Differential Phytotoxicity of Metabolic By-Products of Helminthosporium victoriae.
    Science. 1947 Sep 19;106(2751):270-1 PMID: 17777075
  51. CITRX thioredoxin interacts with the tomato Cf-9 resistance protein and negatively regulates defence.
    EMBO J. 2004 May 19;23(10):2156-65 PMID: 15131698
  52. A central role of salicylic Acid in plant disease resistance.
    Science. 1994 Nov 18;266(5188):1247-50 PMID: 17810266
  53. Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance.
    Plant Cell. 1994 Nov;6(11):1583-1592 PMID: 12244227
  54. Classification of plant thioredoxins by sequence similarity and intron position.
    Methods Enzymol. 2002;347:394-402 PMID: 11898430
  55. Hypersensitive response-related death.
    Plant Mol Biol. 2000 Oct;44(3):321-34 PMID: 11199391
  56. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis.
    Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):10306-11 PMID: 9707643
  57. Evidence for five divergent thioredoxin h sequences in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5620-4 PMID: 7777559
  58. The thioredoxin system in retroviral infection and apoptosis.
    Cell Death Differ. 2005 Aug;12 Suppl 1:991-8 PMID: 15818395
  59. A simple and rapid method for the preparation of plant genomic DNA for PCR analysis.
    Nucleic Acids Res. 1991 Mar 25;19(6):1349 PMID: 2030957
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
DOI
10.1105/tpc.106.047563
Published
2007-02-00
Epub
2007-00-23
Pages
673-87
Language
English
Region
England
NLM ID
9208688
PMCID
PMC1867327
Subset
IM
External Links
PubMed source DOI: 10.1105/tpc.106.047563 PMC Full Text View journal details
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