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Role of Ubiquitination in Plant Innate Immunity and Pathogen Virulence

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Abstract

Plant diseases are a major constraint for stable crop production in the world. Plants are constantly threatened by different pathogens and have developed an array of mechanisms to defend themselves. A growing body of evidence indicates that ubiquitination, which is one of the most important cellular processes for protein modification in eukaryotic organisms, is involved in the regulation of host defense signaling. Pathogens also exploit ubiquitination to block or interfere with plant defenses. Recent studies in a few model plants have demonstrated that ubiquitination plays a critical role in plant–pathogen interactions that lead either to plant resistance or to successful pathogen invasion of the plant host. This review discusses recent findings about the functions of ubiquitination in host defense and pathogen invasion.

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References

  • Abramovitch RB, Kim YJ, Chen S, Dickman MB, Martin GB (2003) Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J 22:60–69

    Article  CAS  PubMed  Google Scholar 

  • Angot A, Peeters N, Lechner E, Vailleau F, Baud C, Gentzbittel L, Sartorel E, Genschik P, Boucher C, Genin S (2006) Ralstonia solanacearum requires F-box-like domain-containing type III effectors to promote disease on several host plants. Proc Natl Acad Sci USA 103:14620–14625

    Article  CAS  PubMed  Google Scholar 

  • Armstrong MR, Whisson SC, Pritchard L, Bos JI, Venter E, Avrova AO, Rehmany AP, Bohme U, Brooks K, Cherevach I, Hamlin N, White B, Fraser A, Lord A, Quail MA, Churcher C, Hall N, Berriman M, Huang S, Kamoun S, Beynon JL, Birch PR (2005) An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc Natl Acad Sci USA 102:7766–7771

    Article  CAS  PubMed  Google Scholar 

  • Azevedo C, Santos-Rosa MJ, Shirasu K (2001) The U-box protein family in plants. Trends Plant Sci 6:354–358

    Article  CAS  PubMed  Google Scholar 

  • Azevedo C, Sadanandom A, Kitagawa K, Freialdenhoven A, Shirasu K, Schulze-Lefert P (2002) The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295:2073–2076

    Article  CAS  PubMed  Google Scholar 

  • Birch PR, Armstrong M, Bos J, Boevink P, Gilroy EM, Taylor RM, Wawra S, Pritchard L, Conti L, Ewan R, Whisson SC, van West P, Sadanandom A, Kamoun S (2009) Towards understanding the virulence functions of RXLR effectors of the oomycete plant pathogen Phytophthora infestans. J Exp Bot 60:1133–1140

    Article  CAS  PubMed  Google Scholar 

  • Boutet SC, Disatnik MH, Chan LS, Iori K, Rando TA (2007) Regulation of Pax3 by proteasomal degradation of monoubiquitinated protein in skeletal muscle progenitors. Cell 130:349–362

    Article  CAS  PubMed  Google Scholar 

  • Boyes DC, Nam J, Dangl JL (1998) 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 USA 95:15849–15854

    Article  CAS  PubMed  Google Scholar 

  • Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671

    Article  CAS  PubMed  Google Scholar 

  • Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    Article  CAS  PubMed  Google Scholar 

  • Cunnac S, Occhialini A, Barberis P, Boucher C, Genin S (2004) Inventory and functional analysis of the large Hrp regulon in Ralstonia solanacearum: identification of novel effector proteins translocated to plant host cells through the type III secretion system. Mol Microbiol 53:115–128

    Article  CAS  PubMed  Google Scholar 

  • de Torres M, Mansfield JW, Grabov N, Brown IR, Ammouneh H, Tsiamis G, Forsyth A, Robatzek S, Grant M, Boch J (2006) Pseudomonas syringae effector AvrPtoB suppresses basal defence in Arabidopsis. Plant J 47:368–382

    Article  PubMed  Google Scholar 

  • de Wit PJ (2007) How plants recognize pathogens and defend themselves. Cell Mol Life Sci 64:2726–2732

    Article  PubMed  Google Scholar 

  • Deng L, Wang C, Spencer E, Yang L, Braun A, You J, Slaughter C, Pickart C, Chen ZJ (2000) Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103:351–361

    Article  CAS  PubMed  Google Scholar 

  • Devoto A, Muskett PR, Shirasu K (2003) Role of ubiquitination in the regulation of plant defence against pathogens. Curr Opin Plant Biol 6:307–311

    Article  CAS  PubMed  Google Scholar 

  • Gimenez-Ibanez S, Hann DR, Ntoukakis V, Petutschnig E, Lipka V, Rathjen JP (2009) AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr Biol 19:423–429

    Article  CAS  PubMed  Google Scholar 

  • Glickman MH, Ciechanover A (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82:373–428

    CAS  PubMed  Google Scholar 

  • Gohre V, Spallek T, Haweker H, Mersmann S, Mentzel T, Boller T, de Torres M, Mansfield JW, Robatzek S (2008) Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr Biol 18:1824–1832

    Article  PubMed  Google Scholar 

  • Gonzalez-Lamothe R, Tsitsigiannis DI, Ludwig AA, Panicot M, Shirasu K, Jones JD (2006) The U-box protein CMPG1 is required for efficient activation of defense mechanisms triggered by multiple resistance genes in tobacco and tomato. Plant Cell 18:1067–1083

    Article  CAS  PubMed  Google Scholar 

  • Goritschnig S, Zhang Y, Li X (2007) The ubiquitin pathway is required for innate immunity in Arabidopsis. Plant J 49:540–551

    Article  CAS  PubMed  Google Scholar 

  • Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, Sattler A, Innes RW, Dangl JL (1995) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269:843–846

    Article  CAS  PubMed  Google Scholar 

  • Groll M, Schellenberg B, Bachmann AS, Archer CR, Huber R, Powell TK, Lindow S, Kaiser M, Dudler R (2008) A plant pathogen virulence factor inhibits the eukaryotic proteasome by a novel mechanism. Nature 452:755–758

    Article  CAS  PubMed  Google Scholar 

  • Hatfield PM, Gosink MM, Carpenter TB, Vierstra RD (1997) The ubiquitin-activating enzyme (E1) gene family in Arabidopsis thaliana. Plant J 11:213–226

    Article  CAS  PubMed  Google Scholar 

  • Heath MC (2000) Hypersensitive response-related death. Plant Mol Biol 44:321–334

    Article  CAS  PubMed  Google Scholar 

  • Hicke L, Dunn R (2003) Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 19:141–172

    Article  CAS  PubMed  Google Scholar 

  • Holt BF 3rd, Belkhadir Y, Dangl JL (2005) Antagonistic control of disease resistance protein stability in the plant immune system. Science 309:929–932

    Article  CAS  PubMed  Google Scholar 

  • Janjusevic R, Abramovitch RB, Martin GB, Stebbins CE (2006) A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Science 311:222–226

    Article  CAS  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Kawasaki T, Nam J, Boyes DC, Holt BF 3rd, Hubert DA, Wiig A, Dangl JL (2005) A duplicated pair of Arabidopsis RING-finger E3 ligases contribute to the RPM1- and RPS2-mediated hypersensitive response. Plant J 44:258–270

    Article  CAS  PubMed  Google Scholar 

  • Kim HS, Delaney TP (2002) 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 14:1469–1482

    Article  CAS  PubMed  Google Scholar 

  • Kim HT, Kim KP, Lledias F, Kisselev AF, Scaglione KM, Skowyra D, Gygi SP, Goldberg AL (2007) Certain pairs of ubiquitin-conjugating enzymes (E2s) and ubiquitin-protein ligases (E3s) synthesize nondegradable forked ubiquitin chains containing all possible isopeptide linkages. J Biol Chem 282:17375–17386

    Article  CAS  PubMed  Google Scholar 

  • Lee J, Nam J, Park HC, Na G, Miura K, Jin JB, Yoo CY, Baek D, Kim DH, Jeong JC, Kim D, Lee SY, Salt DE, Mengiste T, Gong Q, Ma S, Bohnert HJ, Kwak SS, Bressan RA, Hasegawa PM, Yun DJ (2007) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49:79–90

    Article  CAS  PubMed  Google Scholar 

  • Li W, Wang B, Wu J, Lu G, Hu Y, Zhang X, Zhang Z, Zhao Q, Feng Q, Zhang H, Wang Z, Wang G, Han B, Wang Z, Zhou B (2009) The Magnaporthe oryzae avirulence gene AvrPiz-t encodes a predicted secreted protein that triggers the immunity in rice mediated by the blast resistance gene Piz-t. Mol Plant Microbe Interact 22:411–420

    Article  CAS  PubMed  Google Scholar 

  • Lin SS, Martin R, Mongrand S, Vandenabeele S, Chen KC, Jang IC, Chua NH (2008) RING1 E3 ligase localizes to plasma membrane lipid rafts to trigger FB1-induced programmed cell death in Arabidopsis. Plant J 56:550–561

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Liu X, Dai L, Wang G (2007) Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants. J Genet Genomics 34:765–776

    Article  PubMed  Google Scholar 

  • Mayo MA, Ziegler-Graff V (1996) Molecular biology of luteoviruses. Adv Virus Res 46:413–460

    Article  CAS  PubMed  Google Scholar 

  • Nomura K, Debroy S, Lee YH, Pumplin N, Jones J, He SY (2006) A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313:220–223

    Article  CAS  PubMed  Google Scholar 

  • Pazhouhandeh M, Dieterle M, Marrocco K, Lechner E, Berry B, Brault V, Hemmer O, Kretsch T, Richards KE, Genschik P, Ziegler-Graff V (2006) F-box-like domain in the polerovirus protein P0 is required for silencing suppressor function. Proc Natl Acad Sci 103(6):1994–1999

    Article  Google Scholar 

  • Rosebrock TR, Zeng L, Brady JJ, Abramovitch RB, Xiao F, Martin GB (2007) A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448:370–374

    Article  CAS  PubMed  Google Scholar 

  • Schwessinger B, Zipfel C (2008) News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr Opin Plant Biol 11:389–395

    Article  CAS  PubMed  Google Scholar 

  • Shirasu K, Lahaye T, Tan MW, Zhou F, Azevedo C, Schulze-Lefert P (1999) A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell 99:355–366

    Article  CAS  PubMed  Google Scholar 

  • Spence J, Sadis S, Haas AL, Finley D (1995) A ubiquitin mutant with specific defects in DNA repair and multiubiquitination. Mol Cell Biol 15:1265–1273

    CAS  PubMed  Google Scholar 

  • Spoel SH, Mou Z, Tada Y, Spivey NW, Genschik P, Dong X (2009) Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137:860–872

    Article  CAS  PubMed  Google Scholar 

  • Sullivan JA, Shirasu K, Deng XW (2003) The diverse roles of ubiquitin and the 26S proteasome in the life of plants. Nat Rev Genet 4:948–958

    Article  CAS  PubMed  Google Scholar 

  • Takai R, Matsuda N, Nakano A, Hasegawa K, Akimoto C, Shibuya N, Minami E (2002) EL5, a rice N-acetylchitooligosaccharide elicitor-responsive RING-H2 finger protein, is a ubiquitin ligase which functions in vitro in co-operation with an elicitor-responsive ubiquitin-conjugating enzyme, OsUBC5b. Plant J 30:447–455

    Article  CAS  PubMed  Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–665

    Article  CAS  PubMed  Google Scholar 

  • Trujillo M, Ichimura K, Casais C, Shirasu K (2008) Negative regulation of PAMP-triggered immunity by an E3 ubiquitin ligase triplet in Arabidopsis. Curr Biol 18:1396–1401

    Article  CAS  PubMed  Google Scholar 

  • van den Burg HA, Tsitsigiannis DI, Rowland O, Lo J, Rallapalli G, Maclean D, Takken FL, Jones JD (2008) The F-box protein ACRE189/ACIF1 regulates cell death and defense responses activated during pathogen recognition in tobacco and tomato. Plant Cell 20:697–719

    Article  PubMed  Google Scholar 

  • Vierstra RD (2003) The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci 8:135–142

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Weaver ND, Kesarwani M, Dong X (2005) Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036–1040

    Article  CAS  PubMed  Google Scholar 

  • Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–1094

    Article  CAS  PubMed  Google Scholar 

  • Yaeno T, Iba K (2008) BAH1/NLA, a RING-type ubiquitin E3 ligase, regulates the accumulation of salicylic acid and immune responses to Pseudomonas syringae DC3000. Plant Physiol 148:1032–1041

    Article  CAS  PubMed  Google Scholar 

  • Ye Y, Meyer HH, Rapoport TA (2003) Function of the p97-Ufd1-Npl4 complex in retrotranslocation from the ER to the cytosol: dual recognition of nonubiquitinated polypeptide segments and polyubiquitin chains. J Cell Biol 162:71–84

    Article  CAS  PubMed  Google Scholar 

  • Zeng LR, Qu S, Bordeos A, Yang C, Baraoidan M, Yan H, Xie Q, Nahm BH, Leung H, Wang GL (2004) 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 16:2795–2808

    Article  CAS  PubMed  Google Scholar 

  • Zhou R, Silverman N, Hong M, Liao DS, Chung Y, Chen ZJ, Maniatis T (2005) The role of ubiquitination in Drosophila innate immunity. J Biol Chem 280:34048–34055

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank the financial support from Natural Science Foundation of China (NSFC, #30828022 and #30871335), the “973” Project (2006CB101904) and U.S. NSF Plant Genome Research Program (#0605017).

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Correspondence to Guo-Liang Wang.

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G. Shirsekar and L. Dai contributed equally to this work.

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Shirsekar, G., Dai, L., Hu, Y. et al. Role of Ubiquitination in Plant Innate Immunity and Pathogen Virulence. J. Plant Biol. 53, 10–18 (2010). https://doi.org/10.1007/s12374-009-9087-x

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  • DOI: https://doi.org/10.1007/s12374-009-9087-x

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