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PMID: 20447278 Published · ppublish English Journal Article Review

The ubiquitin/26S proteasome system in plant-pathogen interactions: a never-ending hide-and-seek game.

Molecular plant pathology ·Vol. 11 ·No. 2 ·2010-03-00 ·Pages 293-308

Dielen AS, Badaoui S, Candresse T, German-Retana S

Abstract

The ubiquitin/26S proteasome system (UPS) plays a central role in plant protein degradation. Over the past few years, the importance of this pathway in plant-pathogen interactions has been increasingly highlighted. UPS is involved in almost every step of the defence mechanisms in plants, regardless of the type of pathogen. In addition to its proteolytic activities, UPS, through its 20S RNase activity, may be part of a still unknown antiviral defence pathway. Strikingly, UPS is not only a weapon used by plants to defend themselves, but also a target for some pathogens that have evolved mechanisms to inhibit and/or use this system for their own purposes. This article attempts to summarize the current knowledge on UPS involvement in plant-microbe interactions, a complex scheme that illustrates the never-ending arms race between hosts and microbes.

MeSH Terms
Biocatalysis Host-Pathogen Interactions Plant Diseases/microbiology,virology Proteasome Endopeptidase Complex/metabolism Protein Stability Ubiquitin/metabolism
Chemicals
Ubiquitin Proteasome Endopeptidase Complex ATP dependent 26S protease
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Dielen Anne-Sophie
Interactions Plante-Virus, UMR GDPP 1090, INRA Université de Bordeaux 2, BP 81, F-33883 Villenave d'Ornon Cedex, France.
Badaoui Saloua
Candresse Thierry
German-Retana Sylvie
References (145)
145 references, click to expand
  1. GmRAR1 and GmSGT1 are required for basal, R gene-mediated and systemic acquired resistance in soybean.
    Mol Plant Microbe Interact. 2009 Jan;22(1):86-95 PMID: 19061405
  2. The ubiquitin-26S proteasome system at the nexus of plant biology.
    Nat Rev Mol Cell Biol. 2009 Jun;10(6):385-97 PMID: 19424292
  3. HcPro, a multifunctional protein encoded by a plant RNA virus, targets the 20S proteasome and affects its enzymic activities.
    J Gen Virol. 2005 Sep;86(Pt 9):2595-2603 PMID: 16099919
  4. Ubiquitin ligases mediate growth and development by promoting protein death.
    Curr Opin Plant Biol. 2007 Dec;10(6):624-32 PMID: 17851112
  5. HC-Pro protein of Potato virus Y can interact with three Arabidopsis 20S proteasome subunits in planta.
    J Virol. 2007 Dec;81(23):12881-8 PMID: 17898064
  6. p53's double life: transactivation-independent repression of homologous recombination.
    Trends Genet. 2004 Jun;20(6):235-43 PMID: 15145576
  7. Ubiquitination-mediated protein degradation and modification: an emerging theme in plant-microbe interactions.
    Cell Res. 2006 May;16(5):413-26 PMID: 16699537
  8. 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
  9. Structure, function and regulation of plant proteasomes.
    Biochimie. 2008 Feb;90(2):324-35 PMID: 17825468
  10. Proteasome plasticity.
    FEBS Lett. 2005 Jun 13;579(15):3214-23 PMID: 15890341
  11. The Polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing.
    Curr Biol. 2007 Sep 18;17(18):1615-21 PMID: 17869109
  12. Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein.
    EMBO J. 2003 Nov 3;22(21):5679-89 PMID: 14592967
  13. Inhibition of proteasome activity by the TED4 protein in extracellular space: a novel mechanism for protection of living cells from injury caused by dying cells.
    Plant Cell Physiol. 2001 Jan;42(1):9-19 PMID: 11158439
  14. Ubiquitin, hormones and biotic stress in plants.
    Ann Bot. 2007 May;99(5):787-822 PMID: 17220175
  15. The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins.
    Trends Plant Sci. 2003 Mar;8(3):135-42 PMID: 12663224
  16. Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance.
    Plant Cell. 2002 Mar;14(3):629-39 PMID: 11910010
  17. The Arabidopsis EIN3 binding F-Box proteins EBF1 and EBF2 have distinct but overlapping roles in ethylene signaling.
    Plant Cell. 2007 Feb;19(2):509-23 PMID: 17307926
  18. The proteasome and MHC class I antigen processing.
    Biochim Biophys Acta. 2004 Nov 29;1695(1-3):225-33 PMID: 15571818
  19. Plant CULLIN-based E3s: phytohormones come first.
    FEBS Lett. 2005 Jun 13;579(15):3239-45 PMID: 15943967
  20. 20S proteasome and accumulation of oxidized and ubiquitinated proteins in maize leaves subjected to cadmium stress.
    Phytochemistry. 2007 Apr;68(8):1139-46 PMID: 17399749
  21. The ubiquitin system for protein degradation and some of its roles in the control of the cell division cycle.
    Cell Death Differ. 2005 Sep;12(9):1191-7 PMID: 16094395
  22. The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance.
    Science. 2002 Mar 15;295(5562):2073-6 PMID: 11847307
  23. The nanovirus-encoded Clink protein affects plant cell cycle regulation through interaction with the retinoblastoma-related protein.
    J Virol. 2007 Apr;81(8):4177-85 PMID: 17267511
  24. Overexpression of OgPAE1 from wild rice confers fungal resistance against Botrytis cinerea.
    J Plant Res. 2008 Jul;121(4):435-40 PMID: 18463946
  25. Evolution of the type III secretion system and its effectors in plant-microbe interactions.
    New Phytol. 2008;177(1):33-47 PMID: 18078471
  26. F-box proteins everywhere.
    Curr Opin Plant Biol. 2006 Dec;9(6):631-8 PMID: 17005440
  27. Intracellular trafficking of Potato leafroll virus movement protein in transgenic Arabidopsis.
    Traffic. 2007 Sep;8(9):1205-14 PMID: 17631001
  28. Syringolin A, a new plant elicitor from the phytopathogenic bacterium Pseudomonas syringae pv. syringae, inhibits the proliferation of neuroblastoma and ovarian cancer cells and induces apoptosis.
    Cell Prolif. 2006 Dec;39(6):599-609 PMID: 17109642
  29. Stability in vitro of the 69K movement protein of Turnip yellow mosaic virus is regulated by the ubiquitin-mediated proteasome pathway.
    J Gen Virol. 2002 Dec;83(Pt 12):3187-3197 PMID: 12466497
  30. RNA degrading activity is tightly associated with the multicatalytic proteinase, ingensin.
    FEBS Lett. 1989 Sep 11;255(1):179-83 PMID: 2477278
  31. The LeATL6-associated ubiquitin/proteasome system may contribute to fungal elicitor-activated defense response via the jasmonic acid-dependent signaling pathway in tomato.
    Mol Plant Microbe Interact. 2007 Jan;20(1):72-81 PMID: 17249424
  32. ARGONAUTE4 is required for resistance to Pseudomonas syringae in Arabidopsis.
    Plant Cell. 2007 Nov;19(11):3778-90 PMID: 17993621
  33. Related to ubiquitin 1 and 2 are redundant and essential and regulate vegetative growth, auxin signaling, and ethylene production in Arabidopsis.
    Plant Cell. 2004 Sep;16(9):2418-32 PMID: 15319484
  34. Involvement of targeted proteolysis in plant genetic transformation by Agrobacterium.
    Nature. 2004 Sep 2;431(7004):87-92 PMID: 15343337
  35. A proteasome for all occasions.
    FEBS Lett. 2007 Jun 19;581(15):2854-61 PMID: 17418826
  36. SKP2A, an F-box protein that regulates cell division, is degraded via the ubiquitin pathway.
    Plant J. 2008 Mar;53(5):828-41 PMID: 18036202
  37. The RPN1 subunit of the 26S proteasome in Arabidopsis is essential for embryogenesis.
    Plant Cell. 2005 Oct;17(10):2723-37 PMID: 16169895
  38. Arabidopsis SGT1b is required for defense signaling conferred by several downy mildew resistance genes.
    Plant Cell. 2002 May;14(5):993-1003 PMID: 12034892
  39. 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
  40. Partners in dicing.
    Genome Biol. 2006;7(3):210 PMID: 16584538
  41. Cryptogein affects expression of alpha3, alpha6 and beta1 20S proteasome subunits encoding genes in tobacco.
    J Exp Bot. 2001 Sep;52(362):1947-8 PMID: 11520884
  42. The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis.
    Proc Natl Acad Sci U S A. 2002 Aug 20;99(17):11519-24 PMID: 12169662
  43. Non-traditional functions of ubiquitin and ubiquitin-binding proteins.
    J Biol Chem. 2003 Sep 19;278(38):35857-60 PMID: 12860974
  44. Regulated proteolysis in light signaling.
    Curr Opin Plant Biol. 2005 Oct;8(5):469-76 PMID: 16039154
  45. Proteasome comprising a beta1 inducible subunit acts as a negative regulator of NADPH oxidase during elicitation of plant defense reactions.
    FEBS Lett. 2005 Aug 29;579(21):4879-86 PMID: 16111682
  46. Human immunodeficiency virus-1 Tat protein interacts with distinct proteasomal alpha and beta subunits.
    FEBS Lett. 2003 Oct 9;553(1-2):200-4 PMID: 14550573
  47. Misfolded plant virus proteins: elicitors and targets of ubiquitylation.
    FEBS Lett. 2003 Jun 19;545(2-3):229-32 PMID: 12804781
  48. Interaction of the virulence protein VirF of Agrobacterium tumefaciens with plant homologs of the yeast Skp1 protein.
    Curr Biol. 2001 Feb 20;11(4):258-62 PMID: 11250154
  49. Regulatory role of SGT1 in early R gene-mediated plant defenses.
    Science. 2002 Mar 15;295(5562):2077-80 PMID: 11847308
  50. Point mutation of the proteasome beta5 subunit gene is an important mechanism of bortezomib resistance in bortezomib-selected variants of Jurkat T cell lymphoblastic lymphoma/leukemia line.
    J Pharmacol Exp Ther. 2008 Aug;326(2):423-31 PMID: 18502982
  51. Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis.
    Plant Physiol. 2005 Jan;137(1):13-30 PMID: 15644464
  52. BAH1/NLA, a RING-type ubiquitin E3 ligase, regulates the accumulation of salicylic acid and immune responses to Pseudomonas syringae DC3000.
    Plant Physiol. 2008 Oct;148(2):1032-41 PMID: 18753285
  53. The parallel and convergent universes of polyketide synthases and nonribosomal peptide synthetases.
    Chem Biol. 1999 Dec;6(12):R319-25 PMID: 10631508
  54. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB.
    Curr Biol. 2008 Dec 9;18(23):1824-32 PMID: 19062288
  55. Type IV secretion systems: tools of bacterial horizontal gene transfer and virulence.
    Cell Microbiol. 2008 Dec;10(12):2377-86 PMID: 18549454
  56. RAR1 and NDR1 contribute quantitatively to disease resistance in Arabidopsis, and their relative contributions are dependent on the R gene assayed.
    Plant Cell. 2002 May;14(5):1005-15 PMID: 12034893
  57. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling.
    Nature. 2007 Aug 9;448(7154):661-5 PMID: 17637677
  58. Enhanced defense responses in Arabidopsis induced by the cell wall protein fractions from Pythium oligandrum require SGT1, RAR1, NPR1 and JAR1.
    Plant Cell Physiol. 2009 May;50(5):924-34 PMID: 19304739
  59. Biochemical identification of proteasome-associated endonuclease activity in sunflower.
    Biochim Biophys Acta. 2003 Jan 31;1645(1):30-9 PMID: 12535608
  60. 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
  61. Expression of a RING-HC protein from rice improves resistance to Pseudomonas syringae pv. tomato DC3000 in transgenic Arabidopsis thaliana.
    J Exp Bot. 2007;58(15-16):4147-59 PMID: 18182423
  62. Ethylene receptor degradation controls the timing of ripening in tomato fruit.
    Plant J. 2007 Aug;51(3):458-67 PMID: 17655616
  63. Post-translational regulation in plants employing a diverse set of polypeptide tags.
    Biochem Soc Trans. 2005 Apr;33(Pt 2):393-9 PMID: 15787614
  64. 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
  65. A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase.
    Science. 2006 Jan 13;311(5758):222-6 PMID: 16373536
  66. The ubiquitin pathway is required for innate immunity in Arabidopsis.
    Plant J. 2007 Feb;49(3):540-51 PMID: 17217463
  67. A bacterial virulence protein suppresses host innate immunity to cause plant disease.
    Science. 2006 Jul 14;313(5784):220-3 PMID: 16840699
  68. The balance between cell division and endoreplication depends on E2FC-DPB, transcription factors regulated by the ubiquitin-SCFSKP2A pathway in Arabidopsis.
    Plant Cell. 2006 Sep;18(9):2224-35 PMID: 16920782
  69. The tyrphostin adaphostin interacts synergistically with proteasome inhibitors to induce apoptosis in human leukemia cells through a reactive oxygen species (ROS)-dependent mechanism.
    Blood. 2006 Jan 1;107(1):232-40 PMID: 16166589
  70. The targeting of the proteasomal regulatory subunit S2 by adenovirus E1A causes inhibition of proteasomal activity and increased p53 expression.
    J Biol Chem. 2004 Jun 11;279(24):25122-33 PMID: 15056666
  71. Host inhibition of a bacterial virulence effector triggers immunity to infection.
    Science. 2009 May 8;324(5928):784-7 PMID: 19423826
  72. Identification of genes involved in the biosynthesis of the cytotoxic compound glidobactin from a soil bacterium.
    Environ Microbiol. 2007 Jul;9(7):1640-50 PMID: 17564599
  73. A new CULLIN 1 mutant has altered responses to hormones and light in Arabidopsis.
    Plant Physiol. 2007 Feb;143(2):684-96 PMID: 17158585
  74. Arabidopsis SON1 is an F-box protein that regulates a novel induced defense response independent of both salicylic acid and systemic acquired resistance.
    Plant Cell. 2002 Jul;14(7):1469-82 PMID: 12119368
  75. 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
  76. The HECT ubiquitin-protein ligase (UPL) family in Arabidopsis: UPL3 has a specific role in trichome development.
    Plant J. 2003 Sep;35(6):729-42 PMID: 12969426
  77. The Polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation.
    Curr Biol. 2007 Sep 18;17(18):1609-14 PMID: 17869110
  78. Role of SGT1 in resistance protein accumulation in plant immunity.
    EMBO J. 2006 May 3;25(9):2007-16 PMID: 16619029
  79. Joining the army of proteasome inhibitors.
    Chem Biol. 2008 May;15(5):419-21 PMID: 18482693
  80. Sgt1, but not Rar1, is essential for the RB-mediated broad-spectrum resistance to potato late blight.
    BMC Plant Biol. 2008 Jan 23;8:8 PMID: 18215301
  81. Negative regulation of PAMP-triggered immunity by an E3 ubiquitin ligase triplet in Arabidopsis.
    Curr Biol. 2008 Sep 23;18(18):1396-401 PMID: 18771922
  82. Functional study of hot pepper 26S proteasome subunit RPN7 induced by Tobacco mosaic virus from nuclear proteome analysis.
    Biochem Biophys Res Commun. 2006 Dec 15;351(2):405-11 PMID: 17070775
  83. The exosome and the proteasome: nano-compartments for degradation.
    Cell. 2006 May 19;125(4):651-4 PMID: 16713559
  84. Substrate affinity and substrate specificity of proteasomes with RNase activity.
    Mol Biol Rep. 2003 Mar;30(1):1-7 PMID: 12688529
  85. Protein polyubiquitination plays a role in basal host resistance of barley.
    Plant Cell. 2006 Nov;18(11):3321-31 PMID: 17114351
  86. Type III effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity.
    Proc Natl Acad Sci U S A. 2006 Feb 21;103(8):2851-6 PMID: 16477026
  87. RNA interference: the story of gene silencing in plants and humans.
    Biotechnol Adv. 2008 May-Jun;26(3):202-9 PMID: 18221853
  88. RAR1 positively controls steady state levels of barley MLA resistance proteins and enables sufficient MLA6 accumulation for effective resistance.
    Plant Cell. 2004 Dec;16(12):3480-95 PMID: 15548741
  89. Ubiquitin-independent proteolytic functions of the proteasome.
    Arch Biochem Biophys. 2003 Jul 1;415(1):1-5 PMID: 12801506
  90. Preferential induction of 20S proteasome subunits during elicitation of plant defense reactions: towards the characterization of "plant defense proteasomes".
    Int J Biochem Cell Biol. 2003 May;35(5):637-50 PMID: 12672456
  91. Double-stranded RNA binding may be a general plant RNA viral strategy to suppress RNA silencing.
    J Virol. 2006 Jun;80(12):5747-56 PMID: 16731914
  92. COI1 links jasmonate signalling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis.
    Plant J. 2002 Nov;32(4):457-66 PMID: 12445118
  93. F-box-like domain in the polerovirus protein P0 is required for silencing suppressor function.
    Proc Natl Acad Sci U S A. 2006 Feb 7;103(6):1994-9 PMID: 16446454
  94. The F-box protein ACRE189/ACIF1 regulates cell death and defense responses activated during pathogen recognition in tobacco and tomato.
    Plant Cell. 2008 Mar;20(3):697-719 PMID: 18375657
  95. RNA interference.
    Nature. 2002 Jul 11;418(6894):244-51 PMID: 12110901
  96. Marine actinomycetes: a new source of compounds against the human malaria parasite.
    PLoS One. 2008 Jun 04;3(6):e2335 PMID: 18523554
  97. Secreted proteins from Ralstonia solanacearum: a hundred tricks to kill a plant.
    Curr Opin Microbiol. 2009 Feb;12(1):44-52 PMID: 19144559
  98. Metal resistance in yeast mediated by the expression of a maize 20S proteasome alpha subunit.
    Gene. 2002 Jun 26;293(1-2):199-204 PMID: 12137958
  99. Down-regulation of the 26S proteasome subunit RPN9 inhibits viral systemic transport and alters plant vascular development.
    Plant Physiol. 2006 Oct;142(2):651-61 PMID: 16905670
  100. KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling.
    Plant Cell. 2006 Dec;18(12):3415-28 PMID: 17194765
  101. Identification of ubiquitinated proteins in Arabidopsis.
    Plant Mol Biol. 2008 Sep;68(1-2):145-58 PMID: 18535787
  102. Roles of the ubiquitin/proteasome pathway in pollen tube growth with emphasis on MG132-induced alterations in ultrastructure, cytoskeleton, and cell wall components.
    Plant Physiol. 2006 Aug;141(4):1578-90 PMID: 16778013
  103. Antagonistic control of disease resistance protein stability in the plant immune system.
    Science. 2005 Aug 5;309(5736):929-32 PMID: 15976272
  104. Role of ubiquitination in the regulation of plant defence against pathogens.
    Curr Opin Plant Biol. 2003 Aug;6(4):307-11 PMID: 12873523
  105. Identification of major lysine residues of S(3)-RNase of Petunia inflata involved in ubiquitin-26S proteasome-mediated degradation in vitro.
    Plant J. 2008 Jun;54(6):1094-104 PMID: 18346191
  106. Partners-in-infection: host proteins involved in the transformation of plant cells by Agrobacterium.
    Trends Cell Biol. 2002 Mar;12(3):121-9 PMID: 11859024
  107. A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans.
    Cell. 1999 Nov 12;99(4):355-66 PMID: 10571178
  108. Overexpression of a rice defense-related F-box protein gene OsDRF1 in tobacco improves disease resistance through potentiation of defense gene expression.
    Physiol Plant. 2008 Nov;134(3):440-52 PMID: 18573188
  109. Post-transcriptional RNA silencing in plant-microbe interactions: a touch of robustness and versatility.
    Curr Opin Plant Biol. 2008 Aug;11(4):464-70 PMID: 18583181
  110. HIV-1 tat inhibits the 20 S proteasome and its 11 S regulator-mediated activation.
    J Biol Chem. 1997 Mar 28;272(13):8145-8 PMID: 9079628
  111. Functional analysis of a DNA-shuffled movement protein reveals that microtubules are dispensable for the cell-to-cell movement of tobacco mosaic virus.
    Plant Cell. 2002 Jun;14(6):1207-22 PMID: 12084822
  112. Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors.
    EMBO J. 2006 Jun 21;25(12):2768-80 PMID: 16724105
  113. The tobacco ubiquitin-activating enzymes NtE1A and NtE1B are induced by tobacco mosaic virus, wounding and stress hormones.
    Mol Cells. 2005 Apr 30;19(2):228-31 PMID: 15879707
  114. Phytopathogen type III effector weaponry and their plant targets.
    Curr Opin Plant Biol. 2008 Aug;11(4):396-403 PMID: 18657470
  115. RKP, a RING finger E3 ligase induced by BSCTV C4 protein, affects geminivirus infection by regulation of the plant cell cycle.
    Plant J. 2009 Mar;57(5):905-17 PMID: 19000158
  116. Proteasome function is required for activation of programmed cell death in heat shocked tobacco Bright-Yellow 2 cells.
    FEBS Lett. 2007 Mar 6;581(5):917-22 PMID: 17303129
  117. The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity.
    Plant Cell. 2006 Oct;18(10):2792-806 PMID: 17028203
  118. E3 ubiquitin ligases and plant innate immunity.
    J Exp Bot. 2009;60(4):1123-32 PMID: 19276192
  119. A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity.
    Nature. 2007 Jul 19;448(7151):370-4 PMID: 17637671
  120. Characterization of the VIER F-BOX PROTEINE genes from Arabidopsis reveals their importance for plant growth and development.
    Plant Cell. 2007 Apr;19(4):1163-78 PMID: 17435085
  121. Antiviral immunity directed by small RNAs.
    Cell. 2007 Aug 10;130(3):413-26 PMID: 17693253
  122. HISTONE MONOUBIQUITINATION1 interacts with a subunit of the mediator complex and regulates defense against necrotrophic fungal pathogens in Arabidopsis.
    Plant Cell. 2009 Mar;21(3):1000-19 PMID: 19286969
  123. Ralstonia solanacearum requires F-box-like domain-containing type III effectors to promote disease on several host plants.
    Proc Natl Acad Sci U S A. 2006 Sep 26;103(39):14620-5 PMID: 16983093
  124. Recognition of the polyubiquitin proteolytic signal.
    EMBO J. 2000 Jan 4;19(1):94-102 PMID: 10619848
  125. Plant immunity: AvrPto targets the frontline.
    Curr Biol. 2008 Mar 11;18(5):R218-20 PMID: 18334200
  126. Role of proteasomes in disease.
    BMC Biochem. 2007 Nov 22;8 Suppl 1:S3 PMID: 18047740
  127. Mutational analysis of PVX TGBp3 links subcellular accumulation and protein turnover.
    Virology. 2008 May 25;375(1):103-17 PMID: 18289625
  128. Plant ARGONAUTES.
    Trends Plant Sci. 2008 Jul;13(7):350-8 PMID: 18508405
  129. Clink, a nanovirus-encoded protein, binds both pRB and SKP1.
    J Virol. 2000 Apr;74(7):2967-72 PMID: 10708410
  130. Heterologous expression and molecular and cellular characterization of CaPUB1 encoding a hot pepper U-Box E3 ubiquitin ligase homolog.
    Plant Physiol. 2006 Dec;142(4):1664-82 PMID: 17041029
  131. Tobacco mosaic virus particles contain ubiquitinated coat protein subunits.
    Virology. 1988 Jul;165(1):310-2 PMID: 2838968
  132. Protein degradation and protection against misfolded or damaged proteins.
    Nature. 2003 Dec 18;426(6968):895-9 PMID: 14685250
  133. VIP1, an Arabidopsis protein that interacts with Agrobacterium VirE2, is involved in VirE2 nuclear import and Agrobacterium infectivity.
    EMBO J. 2001 Jul 2;20(13):3596-607 PMID: 11432846
  134. Protein complexes mediate signalling in plant responses to hormones, light, sucrose and pathogens.
    Plant Mol Biol. 2002 Dec;50(6):971-80 PMID: 12516865
  135. Involvement of proteasomal subunits zeta and iota in RNA degradation.
    Biochem J. 1997 Aug 15;326 ( Pt 1):93-8 PMID: 9337855
  136. F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress.
    Plant Physiol. 2007 Apr;143(4):1467-83 PMID: 17293439
  137. Degradation of tobacco mosaic virus movement protein by the 26S proteasome.
    J Virol. 2000 Apr;74(7):3330-7 PMID: 10708450
  138. Exploitation of eukaryotic ubiquitin signaling pathways by effectors translocated by bacterial type III and type IV secretion systems.
    PLoS Pathog. 2007 Jan;3(1):e3 PMID: 17257058
  139. Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain.
    Cell. 2000 Oct 13;103(2):351-61 PMID: 11057907
  140. Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity.
    Cell. 2009 May 29;137(5):860-72 PMID: 19490895
  141. The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response.
    Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15849-54 PMID: 9861059
  142. Plant pathogens and integrated defence responses to infection.
    Nature. 2001 Jun 14;411(6839):826-33 PMID: 11459065
  143. Identification and initial characterization of a specific proteasome (prosome) associated RNase activity.
    J Biol Chem. 1995 Sep 15;270(37):22023-8 PMID: 7545175
  144. A plant pathogen virulence factor inhibits the eukaryotic proteasome by a novel mechanism.
    Nature. 2008 Apr 10;452(7188):755-8 PMID: 18401409
  145. Structural characterization of HC-Pro, a plant virus multifunctional protein.
    J Biol Chem. 2003 Jun 27;278(26):23753-61 PMID: 12684502
Article Info
Journal
Molecular plant pathology
Abbr.
Mol Plant Pathol
ISSN
1364-3703
Published
2010-03-00
Pages
293-308
Language
English
Region
England
NLM ID
100954969
PMCID
PMC6640532
Subset
IM
Corrections
ErratumIn
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