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PMID: 16531490 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The U-box protein CMPG1 is required for efficient activation of defense mechanisms triggered by multiple resistance genes in tobacco and tomato.

The Plant cell ·Vol. 18 ·No. 4 ·2006-04-00 ·Pages 1067-83

González-Lamothe R, Tsitsigiannis DI, Ludwig AA, Panicot M, Shirasu K, Jones JD

Abstract

We previously identified three Avr9/Cf-9 Rapidly Elicited (ACRE) genes essential for Cf-9- and Cf-4-dependent hypersensitive response (HR) production in Nicotiana benthamiana. Two of them encode putative E3 ubiquitin ligase components. This led us to investigate other ACRE genes associated with the ubiquitination pathway. ACRE74 encodes a U-box E3 ligase homolog, highly related to parsley (Petroselinum crispum) CMPG1 and Arabidopsis thaliana PLANT U-BOX20 (PUB20) and PUB21 proteins, and was called Nt CMPG1. Transcript levels of Nt CMPG1 and the homologous tomato (Solanum lycopersicum) Cmpg1 are induced in Cf9 tobacco (Nicotiana tabacum) and Cf9 tomato after Avr9 elicitation. Tobacco CMPG1 possesses in vitro E3 ligase activity. N. benthamiana plants silenced for Nt CMPG1 show reduced HR after Cf-9/Avr9 elicitation, while overexpression of Nt CMPG1 induces a stronger HR in Cf9 tobacco plants after Avr9 infiltration. In tomato, silencing of Cmpg1 decreased resistance to Cladosporium fulvum. Overexpression of epitope-tagged tobacco CMPG1 mutated in the U-box domain confers a dominant-negative phenotype. We also show that Nt CMPG1 is involved in the Pto/AvrPto and Inf1 responses. In summary, we show that the E3 ligase Nt CMPG1 is essential for plant defense and disease resistance.

MeSH Terms
Amino Acid Sequence Base Sequence Consensus Sequence DNA Primers Genes, Dominant Immunity, Innate/genetics Lycopersicon esculentum/enzymology,genetics,physiology Molecular Sequence Data Mutation Plant Diseases Plant Proteins/metabolism Sequence Alignment Sequence Homology, Amino Acid Tobacco/enzymology,genetics,physiology Ubiquitin/metabolism Ubiquitin-Protein Ligases/genetics,metabolism
Chemicals
DNA Primers Plant Proteins Ubiquitin Ubiquitin-Protein Ligases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
González-Lamothe Rocío
Sainsbury Laboratory, John Ines Centre, Norwich NR4 7UH, UK.
Tsitsigiannis Dimitrios I
Ludwig Andrea A
Panicot Mireia
Shirasu Ken
Jones Jonathan D G
References (79)
79 references, click to expand
  1. U box proteins as a new family of ubiquitin-protein ligases.
    J Biol Chem. 2001 Aug 31;276(35):33111-20 PMID: 11435423
  2. The PSIPRED protein structure prediction server.
    Bioinformatics. 2000 Apr;16(4):404-5 PMID: 10869041
  3. SCF and Cullin/Ring H2-based ubiquitin ligases.
    Annu Rev Cell Dev Biol. 1999;15:435-67 PMID: 10611969
  4. Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato.
    Annu Rev Phytopathol. 2003;41:215-43 PMID: 14527329
  5. Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants.
    Proc Natl Acad Sci U S A. 2002 Aug 6;99(16):10865-9 PMID: 12119413
  6. CHRK1, a chitinase-related receptor-like kinase, interacts with NtPUB4, an armadillo repeat protein, in tobacco.
    Biochim Biophys Acta. 2003 Sep 23;1651(1-2):50-9 PMID: 14499588
  7. PLANT DISEASE RESISTANCE GENES.
    Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:575-607 PMID: 15012275
  8. Rapid Avr9- and Cf-9 -dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses.
    Plant Cell. 1999 Feb;11(2):273-87 PMID: 9927644
  9. Protein secondary structure prediction based on position-specific scoring matrices.
    J Mol Biol. 1999 Sep 17;292(2):195-202 PMID: 10493868
  10. Virus-induced gene silencing in tomato.
    Plant J. 2002 Sep;31(6):777-86 PMID: 12220268
  11. Molecular interactions between tomato and the leaf mold pathogen Cladosporium fulvum.
    Annu Rev Phytopathol. 2005;43:395-436 PMID: 16078890
  12. The Rx gene from potato controls separate virus resistance and cell death responses.
    Plant Cell. 1999 May;11(5):781-92 PMID: 10330465
  13. Two antifungal thaumatin-like proteins from barley grain.
    FEBS Lett. 1991 Oct 7;291(1):127-31 PMID: 1936240
  14. Constructs and methods for high-throughput gene silencing in plants.
    Methods. 2003 Aug;30(4):289-95 PMID: 12828942
  15. The tomato Cf-9 disease resistance gene functions in tobacco and potato to confer responsiveness to the fungal avirulence gene product avr 9
    Plant Cell. 1998 Aug;10(8):1251-66 PMID: 9707527
  16. Developmental control of promoter activity is not responsible for mature onset of Cf-9B-mediated resistance to leaf mold in tomato.
    Mol Plant Microbe Interact. 2002 Nov;15(11):1099-107 PMID: 12423015
  17. AtCHIP, a U-box-containing E3 ubiquitin ligase, plays a critical role in temperature stress tolerance in Arabidopsis.
    Plant Physiol. 2003 Jun;132(2):861-9 PMID: 12805616
  18. A generic protein purification method for protein complex characterization and proteome exploration.
    Nat Biotechnol. 1999 Oct;17(10):1030-2 PMID: 10504710
  19. Modulation of sensitivity and selectivity in plant signaling by proteasomal destabilization.
    Curr Opin Plant Biol. 2003 Oct;6(5):453-62 PMID: 12972046
  20. Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown.
    J Biol Chem. 1983 Jul 10;258(13):8206-14 PMID: 6305978
  21. The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes.
    Proc Natl Acad Sci U S A. 2005 Sep 27;102(39):14046-51 PMID: 16162672
  22. ProDom: automated clustering of homologous domains.
    Brief Bioinform. 2002 Sep;3(3):246-51 PMID: 12230033
  23. Virus-induced gene silencing in Solanum species.
    Plant J. 2004 Jul;39(2):264-72 PMID: 15225290
  24. Role of ubiquitination in the regulation of plant defence against pathogens.
    Curr Opin Plant Biol. 2003 Aug;6(4):307-11 PMID: 12873523
  25. Structure and biochemical function of a prototypical Arabidopsis U-box domain.
    J Biol Chem. 2004 Sep 17;279(38):40053-61 PMID: 15231834
  26. Comparison of the hypersensitive response induced by the tomato Cf-4 and Cf-9 genes in Nicotiana spp.
    Mol Plant Microbe Interact. 2000 Apr;13(4):465-9 PMID: 10755310
  27. Bre1 is required for Notch signaling and histone modification.
    Dev Cell. 2005 Feb;8(2):279-86 PMID: 15691768
  28. SMART, a simple modular architecture research tool: identification of signaling domains.
    Proc Natl Acad Sci U S A. 1998 May 26;95(11):5857-64 PMID: 9600884
  29. cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles.
    Plant Cell. 2000 Jun;12(6):963-77 PMID: 10852940
  30. The Cf-9 disease resistance protein is present in an approximately 420-kilodalton heteromultimeric membrane-associated complex at one molecule per complex.
    Plant Cell. 2002 Mar;14(3):689-702 PMID: 11910014
  31. Genetic and molecular analysis of tomato Cf genes for resistance to Cladosporium fulvum.
    Philos Trans R Soc Lond B Biol Sci. 1998 Sep 29;353(1374):1413-24 PMID: 9800204
  32. Phylogenomic analysis of the receptor-like proteins of rice and Arabidopsis.
    Plant Physiol. 2005 Jun;138(2):611-23 PMID: 15955925
  33. JPred: a consensus secondary structure prediction server.
    Bioinformatics. 1998;14(10):892-3 PMID: 9927721
  34. Plant pathogens and integrated defence responses to infection.
    Nature. 2001 Jun 14;411(6839):826-33 PMID: 11459065
  35. The SCF(COI1) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis.
    Plant Cell. 2002 Aug;14(8):1919-35 PMID: 12172031
  36. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato.
    Cell. 1997 Dec 12;91(6):821-32 PMID: 9413991
  37. The ubiquitin-proteasome pathway and plant development.
    Plant Cell. 2004 Dec;16(12):3181-95 PMID: 15579807
  38. The U box is a modified RING finger - a common domain in ubiquitination.
    Curr Biol. 2000 Feb 24;10(4):R132-4 PMID: 10704423
  39. The U-box protein family in plants.
    Trends Plant Sci. 2001 Aug;6(8):354-8 PMID: 11495788
  40. Resistance of nicotiana benthamiana to phytophthora infestans is mediated by the recognition of the elicitor protein INF1
    Plant Cell. 1998 Sep;10(9):1413-26 PMID: 9724689
  41. Evolving disease resistance genes.
    Curr Opin Plant Biol. 2005 Apr;8(2):129-34 PMID: 15752991
  42. Construct design for efficient, effective and high-throughput gene silencing in plants.
    Plant J. 2001 Sep;27(6):581-90 PMID: 11576441
  43. The E3 ubiquitin ligase activity of arabidopsis PLANT U-BOX17 and its functional tobacco homolog ACRE276 are required for cell death and defense.
    Plant Cell. 2006 Apr;18(4):1084-98 PMID: 16531496
  44. How the ubiquitin-proteasome system controls transcription.
    Nat Rev Mol Cell Biol. 2003 Mar;4(3):192-201 PMID: 12612638
  45. The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase.
    Science. 1999 Oct 8;286(5438):309-12 PMID: 10514377
  46. A large complement of the predicted Arabidopsis ARM repeat proteins are members of the U-box E3 ubiquitin ligase family.
    Plant Physiol. 2004 Jan;134(1):59-66 PMID: 14657406
  47. ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen.
    Plant Cell. 2003 Apr;15(4):885-98 PMID: 12671085
  48. Resistance gene-dependent activation of a calcium-dependent protein kinase in the plant defense response.
    Plant Cell. 2000 May;12(5):803-16 PMID: 10810151
  49. Two immediate-early pathogen-responsive members of the AtCMPG gene family in Arabidopsis thaliana and the W-box-containing elicitor-response element of AtCMPG1.
    Proc Natl Acad Sci U S A. 2002 Jun 25;99(13):9049-54 PMID: 12084942
  50. Post-translational regulation in plants employing a diverse set of polypeptide tags.
    Biochem Soc Trans. 2005 Apr;33(Pt 2):393-9 PMID: 15787614
  51. The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis.
    Plant Physiol. 2004 Jun;135(2):1113-28 PMID: 15181213
  52. Gibberellins signal nuclear import of PHOR1, a photoperiod-responsive protein with homology to Drosophila armadillo.
    Cell. 2001 Aug 10;106(3):343-54 PMID: 11509183
  53. Interaction of the ring finger-related U-box motif of a nuclear dot protein with ubiquitin-conjugating enzymes.
    J Biol Chem. 2001 Jun 1;276(22):19617-23 PMID: 11274149
  54. The RING finger of c-Cbl mediates desensitization of the epidermal growth factor receptor.
    J Biol Chem. 1999 Aug 6;274(32):22151-4 PMID: 10428778
  55. Structure of a c-Cbl-UbcH7 complex: RING domain function in ubiquitin-protein ligases.
    Cell. 2000 Aug 18;102(4):533-9 PMID: 10966114
  56. SGT1 encodes an essential component of the yeast kinetochore assembly pathway and a novel subunit of the SCF ubiquitin ligase complex.
    Mol Cell. 1999 Jul;4(1):21-33 PMID: 10445024
  57. Functional analysis of Avr9/Cf-9 rapidly elicited genes identifies a protein kinase, ACIK1, that is essential for full Cf-9-dependent disease resistance in tomato.
    Plant Cell. 2005 Jan;17(1):295-310 PMID: 15598806
  58. Toll-like receptor signalling.
    Nat Rev Immunol. 2004 Jul;4(7):499-511 PMID: 15229469
  59. Non-traditional functions of ubiquitin and ubiquitin-binding proteins.
    J Biol Chem. 2003 Sep 19;278(38):35857-60 PMID: 12860974
  60. A tobacco mosaic virus-induced tobacco protein is homologous to the sweet-tasting protein thaumatin.
    Nature. 1986 May 29-Jun 4;321(6069):531-2 PMID: 3713832
  61. Technical Advance. Tobacco rattle virus as a vector for analysis of gene function by silencing.
    Plant J. 2001 Jan;25(2):237-45 PMID: 11169199
  62. A highly specific pathogen-responsive promoter element from the immediate-early activated CMPG1 gene in Petroselinum crispum.
    Plant J. 2001 Apr;26(2):217-27 PMID: 11389762
  63. A duplicated pair of Arabidopsis RING-finger E3 ligases contribute to the RPM1- and RPS2-mediated hypersensitive response.
    Plant J. 2005 Oct;44(2):258-70 PMID: 16212605
  64. Role of SCF ubiquitin-ligase and the COP9 signalosome in the N gene-mediated resistance response to Tobacco mosaic virus.
    Plant Cell. 2002 Jul;14(7):1483-96 PMID: 12119369
  65. Extracellular signal-regulated kinase 1c (ERK1c), a novel 42-kilodalton ERK, demonstrates unique modes of regulation, localization, and function.
    Mol Cell Biol. 2004 Nov;24(22):10000-15 PMID: 15509801
  66. The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance.
    Science. 2002 Mar 15;295(5562):2073-6 PMID: 11847307
  67. Ubiquitin as a central cellular regulator.
    Cell. 2004 Jan 23;116(2 Suppl):S29-32, 2 p following S32 PMID: 15055578
  68. Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis.
    Plant Physiol. 2005 Dec;139(4):1597-611 PMID: 16339806
  69. pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation.
    Plant Mol Biol. 2000 Apr;42(6):819-32 PMID: 10890530
  70. 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
  71. Structural insights into the U-box, a domain associated with multi-ubiquitination.
    Nat Struct Biol. 2003 Apr;10(4):250-5 PMID: 12627222
  72. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  73. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction.
    Physiol Rev. 2002 Apr;82(2):373-428 PMID: 11917093
  74. Virus-induced silencing of WIPK and SIPK genes reduces resistance to a bacterial pathogen, but has no effect on the INF1-induced hypersensitive response (HR) in Nicotiana benthamiana.
    Mol Genet Genomics. 2003 Aug;269(5):583-91 PMID: 12838412
  75. K+ channels of Cf-9 transgenic tobacco guard cells as targets for Cladosporium fulvum Avr9 elicitor-dependent signal transduction.
    Plant J. 1999 Aug;19(4):453-62 PMID: 10504567
  76. SMART 4.0: towards genomic data integration.
    Nucleic Acids Res. 2004 Jan 1;32(Database issue):D142-4 PMID: 14681379
  77. Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity.
    Plant Cell. 2004 Oct;16(10):2795-808 PMID: 15377756
  78. Calcium-dependent protein kinases play an essential role in a plant defence response.
    EMBO J. 2001 Oct 15;20(20):5556-67 PMID: 11597999
  79. Triad3A, an E3 ubiquitin-protein ligase regulating Toll-like receptors.
    Nat Immunol. 2004 May;5(5):495-502 PMID: 15107846
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2006-04-00
Epub
2006-00-10
Pages
1067-83
Language
English
Region
England
NLM ID
9208688
PMCID
PMC1425846
Subset
IM
Databases
GENBANK
AAG51307, AAK69402, AAP03884, DQ118759
RefSeq
NP_198565
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