1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Phytopathology
  4. Volume 61, 2023
  5. Article

Annual Review of Phytopathology

Volume 61, 2023

The Plant Ubiquitin–Proteasome System as a Target for Microbial Manipulation

Abstract

The plant immune system perceives pathogens to trigger defense responses. In turn, pathogens secrete effector molecules to subvert these defense responses. The initiation and maintenance of defense responses involve not only de novo synthesis of regulatory proteins and enzymes but also their regulated degradation. The latter is achieved through protein degradation pathways such as the ubiquitin–proteasome system (UPS). The UPS regulates all stages of immunity, from the perception of the pathogen to the execution of the response, and, therefore, constitutes an ideal candidate for microbial manipulation of the host. Pathogen effector molecules interfere with the plant UPS through several mechanisms. This includes hijacking general UPS functions or perturbing its ability to degrade specific targets. In this review, we describe how the UPS regulates different immunity-related processes and how pathogens subvert this to promote disease.

Keyword(s): effectors, pathogens, plant immunity, proteostasis, ubiquitination, ubiquitin–proteasome system
Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-021622-110443
2023-09-05
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/phyto/61/1/annurev-phyto-021622-110443.html?itemId=/content/journals/10.1146/annurev-phyto-021622-110443&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Abramovitch RB, Janjusevic R, Stebbins CE, Martin GB, Lindow SE. 2006. Type III effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity. PNAS 103:82851–56
     [Google Scholar]
  2. 2.
    Angot A, Peeters N, Lechner E, Vailleau F, Baud C et al. 2006. Ralstonia solanacearum requires F-box-like domain-containing type III effectors to promote disease on several host plants. PNAS 103:3914620–25
     [Google Scholar]
  3. 3.
    Ballut L, Petit F, Le Gall O, Candresse T, Schmid P et al. 2003. Biochemical identification of proteasome-associated endonuclease activity in sunflower. Biochim. Biophys. Acta 1645:130–39
     [Google Scholar]
  4. 4.
    Baltrus DA, Nishimura MT, Romanchuk A, Chang JH, Mukhtar MS et al. 2011. Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLOS Pathog 7:7e1002132
     [Google Scholar]
  5. 5.
    Becker F, Buschfeld E, Schell J, Bachmair A. 1993. Altered response to viral infection by tobacco plants perturbed in ubiquitin system. Plant J. 3:6875–81
     [Google Scholar]
  6. 6.
    Bos JIB, Armstrong MR, Gilroy EM, Boevink PC, Hein I et al. 2010. Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. PNAS 107:219909–14
     [Google Scholar]
  7. 7.
    Bullones-Bolaños A, Bernal-Bayard J, Ramos-Morales F. 2022. The NEL family of bacterial E3 ubiquitin ligases. Int. J. Mol. Sci. 23:147725
     [Google Scholar]
  8. 8.
    Bürger M, Chory J. 2019. Stressed out about hormones: how plants orchestrate immunity. Cell Host Microbe 26:2163–72
     [Google Scholar]
  9. 9.
    Caillaud MC, Asai S, Rallapalli G, Piquerez S, Fabro G, Jones JDG. 2013. A downy mildew effector attenuates salicylic acid-triggered immunity in Arabidopsis by interacting with the host mediator complex. PLOS Biol 11:12e1001732
     [Google Scholar]
  10. 10.
    Chen B, Lin L, Lu Y, Peng J, Zheng H et al. 2020. Ubiquitin-like protein 5 interacts with the silencing suppressor p3 of rice stripe virus and mediates its degradation through the 26S proteasome pathway. PLOS Pathog. 16:8e1008780
     [Google Scholar]
  11. 11.
    Chen H, Chen J, Li M, Chang M, Xu K et al. 2017. A bacterial type III effector targets the master regulator of salicylic acid signaling, NPR1, to subvert plant immunity. Cell Host Microbe 22:6777–88.e7
     [Google Scholar]
  12. 12.
    Chen L, Hellmann H. 2013. Plant E3 ligases: flexible enzymes in a sessile world. Mol. Plant 6:51388–404
     [Google Scholar]
  13. 13.
    Chen Q, Zhong Y, Wu Y, Liu L, Wang P et al. 2016. HRD1-mediated ERAD tuning of ER-bound E2 is conserved between plants and mammals. Nat. Plants 2:16094
     [Google Scholar]
  14. 14.
    Chen ZQ, Zhao JH, Chen Q, Zhang ZH, Li J et al. 2020. DNA geminivirus infection induces an imprinted E3 ligase gene to epigenetically activate viral gene transcription. Plant Cell 32:103256–72
     [Google Scholar]
  15. 15.
    Cheng D, Zhou D, Wang Y, Wang B, He Q et al. 2021. Ralstonia solanacearum type III effector RipV2 encoding a novel E3 ubiquitin ligase (NEL) is required for full virulence by suppressing plant PAMP-triggered immunity. Biochem. Biophys. Res. Commun. 550:120–26
     [Google Scholar]
  16. 16.
    Cheng W, Munkvold KR, Gao H, Mathieu J, Schwizer S et al. 2011. Structural analysis of Pseudomonas syringae AvrPtoB bound to host BAK1 reveals two similar kinase-interacting domains in a type III effector. Cell Host Microbe 10:6616–26
     [Google Scholar]
  17. 17.
    Cheng YT, Li Y, Huang S, Huang Y, Dong X et al. 2011. Stability of plant immune-receptor resistance proteins is controlled by SKP1-CULLIN1-F-box (SCF)-mediated protein degradation. PNAS 108:3514694–99
     [Google Scholar]
  18. 18.
    Choi C, Im JH, Lee J, Il Kwon S, Kim W-Y et al. 2022. OsDWD1 E3 ligase-mediated OsNPR1 degradation suppresses basal defense in rice. Plant J. 112:4966–81
     [Google Scholar]
  19. 19.
    Chronis D, Chen S, Lu S, Hewezi T, Carpenter SCD et al. 2013. A ubiquitin carboxyl extension protein secreted from a plant-parasitic nematode Globodera rostochiensis is cleaved in planta to promote plant parasitism. Plant J 74:2185–96
     [Google Scholar]
  20. 20.
    Chung K, Tasaka M. 2011. RPT2a, a 26S proteasome AAA-ATPase, is directly involved in Arabidopsis CC-NBS-LRR protein uni-1D-induced signaling pathways. Plant Cell Physiol 52:91657–64
     [Google Scholar]
  21. 21.
    Coll NS, Epple P, Dangl JL. 2011. Programmed cell death in the plant immune system. Cell Death Differ. 18:81247–56
     [Google Scholar]
  22. 22.
    Collins GA, Goldberg AL. 2017. The logic of the 26S proteasome. Cell 169:5792–806
     [Google Scholar]
  23. 23.
    Copeland C, Woloshen V, Huang Y, Li X. 2016. AtCDC48A is involved in the turnover of an NLR immune receptor. Plant J 88:2294–305
     [Google Scholar]
  24. 24.
    Couto D, Zipfel C. 2016. Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 16:9537–52
     [Google Scholar]
  25. 25.
    Craig A, Ewan R, Mesmar J, Gudipati V, Sadanandom A. 2009. E3 ubiquitin ligases and plant innate immunity. J. Exp. Bot. 60:41123–32
     [Google Scholar]
  26. 26.
    Dallery JF, Zimmer M, Halder V, Suliman M, Pigné S et al. 2020. Inhibition of jasmonate-mediated plant defences by the fungal metabolite higginsianin B. J. Exp. Bot. 71:102910–21
     [Google Scholar]
  27. 27.
    de Marchi R, Sorel M, Mooney B, Fudal I, Goslin K et al. 2016. The N-end rule pathway regulates pathogen responses in plants. Sci. Rep. 6:126020
     [Google Scholar]
  28. 28.
    Diaz-Granados A, Sterken MG, Overmars H, Ariaans R, Holterman M et al. 2020. The effector GpRbp-1 of Globodera pallida targets a nuclear HECT E3 ubiquitin ligase to modulate gene expression in the host. Mol. Plant Pathol. 21:166–82
     [Google Scholar]
  29. 29.
    Dissmeyer N. 2019. Conditional protein function via N-degron pathway-mediated proteostasis in stress physiology. Annu. Rev. Plant. Biol. 70:83–117
     [Google Scholar]
  30. 30.
    Dong OX, Ao K, Xu F, Johnson KCM, Wu Y et al. 2018. Individual components of paired typical NLR immune receptors are regulated by distinct E3 ligases. Nat Plants 4:9699–710
     [Google Scholar]
  31. 31.
    Dubiella U, Serrano I. 2021. The ubiquitin proteasome system as a double agent in plant-virus interactions. Plants 10:54–7
     [Google Scholar]
  32. 32.
    Fan J, Bai P, Ning Y, Wang J, Shi X et al. 2018. The monocot-specific receptor-like kinase SDS2 controls cell death and immunity in rice. Cell Host Microbe 23:4498–510.e5
     [Google Scholar]
  33. 33.
    Fernández-Calvo P, Chini A, Fernández-Barbero G, Chico JM, Gimenez-Ibanez S et al. 2011. The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23:2701–15
     [Google Scholar]
  34. 34.
    Fu ZQ, Yan S, Saleh A, Wang W, Ruble J et al. 2012. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486:7402228–32
     [Google Scholar]
  35. 35.
    Furlan G, Nakagami H, Eschen-Lippold L, Jiang X, Majovsky P et al. 2017. Changes in PUB22 ubiquitination modes triggered by MITOGEN-ACTIVATED PROTEIN KINASE3 dampen the immune response. Plant Cell 29:4726–45
     [Google Scholar]
  36. 36.
    Furniss JJ, Grey H, Wang Z, Nomoto M, Jackson L et al. 2018. Proteasome-associated HECT-type ubiquitin ligase activity is required for plant immunity. PLOS Pathog 14:11e1007447
     [Google Scholar]
  37. 37.
    Gao C, Sun P, Wang W, Tang D. 2021. Arabidopsis E3 ligase KEG associates with and ubiquitinates MKK4 and MKK5 to regulate plant immunity. J Integr. Plant Biol. 63:2327–39
     [Google Scholar]
  38. 38.
    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. 19:5423–29
     [Google Scholar]
  39. 39.
    Göhre V, Spallek T, Häweker H, Mersmann S, Mentzel T et al. 2008. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 18:231824–32
     [Google Scholar]
  40. 40.
    Goritschnig S, Zhang Y, Li X. 2007. The ubiquitin pathway is required for innate immunity in Arabidopsis. Plant J 49:3540–51
     [Google Scholar]
  41. 41.
    Goslin K, Eschen-Lippold L, Naumann C, Linster E, Sorel M et al. 2019. Differential N-end rule degradation of RIN4/NOI fragments generated by the AvrRpt2 effector protease. Plant Physiol 180:42272–89
     [Google Scholar]
  42. 42.
    Gou M, Shi Z, Zhu Y, Bao Z, Wang G, Hua J. 2012. The F-box protein CPR1/CPR30 negatively regulates R protein SNC1 accumulation. Plant J 69:3411–20
     [Google Scholar]
  43. 43.
    Gravot A, Richard G, Lime T, Lemarié S, Jubault M et al. 2016. Hypoxia response in Arabidopsis roots infected by Plasmodiophora brassicae supports the development of clubroot. BMC Plant Biol 16:1251
     [Google Scholar]
  44. 44.
    Groll M, Schellenberg B, Bachmann AS, Archer CR, Huber R et al. 2008. A plant pathogen virulence factor inhibits the eukaryotic proteasome by a novel mechanism. Nature 452:7188755–58
     [Google Scholar]
  45. 45.
    Gu Y, Innes RW. 2012. The KEEP ON GOING protein of Arabidopsis regulates intracellular protein trafficking and is degraded during fungal infection. Plant Cell 24:114717–30
     [Google Scholar]
  46. 46.
    He Q, McLellan H, Boevink PC, Sadanandom A, Xie C et al. 2015. U-box E3 ubiquitin ligase PUB17 acts in the nucleus to promote specific immune pathways triggered by Phytophthora infestans. J. Exp. Bot. 66:113189–99
     [Google Scholar]
  47. 47.
    Hu X-H, Fan J, Wu J-L, Shen S, He J-X et al. 2021. Proteasome maturation factor UMP1 confers broad-spectrum disease resistance by modulating H2O2 accumulation in rice. bioRxiv 433750: https://doi.org/10.1101/2021.03.03.433750
    [Google Scholar]
  48. 48.
    Huang J, Wu X, Gao Z. 2021. The RING-type protein BOI negatively regulates the protein level of a CC-NBS-LRR in Arabidopsis. Biochem. Biophys. Res. Commun. 578:104–9
     [Google Scholar]
  49. 49.
    Huang W, MacLean AM, Sugio A, Maqbool A, Busscher M et al. 2021. Parasitic modulation of host development by ubiquitin-independent protein degradation. Cell 184:205201–14.e12
     [Google Scholar]
  50. 50.
    Ishikawa K, Yamaguchi K, Sakamoto K, Yoshimura S, Inoue K et al. 2014. Bacterial effector modulation of host E3 ligase activity suppresses PAMP-triggered immunity in rice. Nat. Commun. 5:5430
     [Google Scholar]
  51. 51.
    Ji H, Liu D, Zhang Z, Sun J, Han B, Li Z. 2020. A bacterial F-box effector suppresses SAR immunity through mediating the proteasomal degradation of OsTrxh2 in rice. Plant J 104:41054–72
     [Google Scholar]
  52. 52.
    Jiang C, Hei R, Yang Y, Zhang S, Wang Q et al. 2020. An orphan protein of Fusarium graminearum modulates host immunity by mediating proteasomal degradation of TaSnRK1α. Nat. Commun. 11:14382
     [Google Scholar]
  53. 53.
    Jiang S, Yao J, Ma KW, Zhou H, Song J et al. 2013. Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors. PLOS Pathog 9:10e1003715
     [Google Scholar]
  54. 54.
    Jin L, Qin Q, Wang Y, Pu Y, Liu L et al. 2016. Rice dwarf virus P2 protein hijacks auxin signaling by directly targeting the rice OsIAA10 protein, enhancing viral infection and disease development. PLOS Pathog 12:9e1005847
     [Google Scholar]
  55. 55.
    Jin Y, Ma D, Dong J, Jin J, Li D et al. 2007. HC-Pro protein of Potato virus Y can interact with three Arabidopsis 20S proteasome subunits in planta. J. Virol. 81:2312881–88
     [Google Scholar]
  56. 56.
    Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:7117323–29
     [Google Scholar]
  57. 57.
    Kamal H, Minhas F, Tripathi D, Abbasi WA, Hamza M et al. 2019. βC1, pathogenicity determinant encoded by Cotton leaf curl Multan betasatellite, interacts with calmodulin-like protein 11 (Gh-CML11) in Gossypium hirsutum. PLOS ONE 14:12e0225876
     [Google Scholar]
  58. 58.
    Karki SJ, Reilly A, Zhou B, Mascarello M, Burke J et al. 2021. A small secreted protein from Zymoseptoria tritici interacts with a wheat E3 ubiquitin ligase to promote disease. J. Exp. Bot. 72:2733–46
     [Google Scholar]
  59. 59.
    Kawasaki T, Nam J, Boyes DC, Holt BF, Hubert DA et al. 2005. A duplicated pair of Arabidopsis RING-finger E3 ligases contribute to the RPM1- and RPS2-mediated hypersensitive response. Plant J 44:2258–70
     [Google Scholar]
  60. 60.
    Khan M, Subramaniam R, Desveaux D. 2016. Of guards, decoys, baits and traps: pathogen perception in plants by type III effector sensors. Curr. Opin. Microbiol. 29:49–55
     [Google Scholar]
  61. 61.
    Kitazawa Y, Iwabuchi N, Maejima K, Sasano M, Matsumoto O et al. 2022. A phytoplasma effector acts as a ubiquitin-like mediator between floral MADS-box proteins and proteasome shuttle proteins. Plant Cell 34:51709–23
     [Google Scholar]
  62. 62.
    Kreitman M, Noronha A, Yarden Y. 2018. Irreversible modifications of receptor tyrosine kinases. FEBS Lett 592:132199–212
     [Google Scholar]
  63. 63.
    Kud J, Wang W, Gross R, Fan Y, Huang L et al. 2019. The potato cyst nematode effector RHA1B is a ubiquitin ligase and uses two distinct mechanisms to suppress plant immune signaling. PLOS Pathog 15:4e1007720
     [Google Scholar]
  64. 64.
    Lacroix B, Citovsky V 2015. Nopaline-type Ti plasmid of Agrobacterium encodes a VirF-like functional F-box protein. Sci Rep 5:16610
     [Google Scholar]
  65. 65.
    Lai J, Chen H, Teng K, Zhao Q, Zhang Z et al. 2009. RKP, a RING finger E3 ligase induced by BSCTV C4 protein, affects geminivirus infection by regulation of the plant cell cycle. Plant J 57:5905–17
     [Google Scholar]
  66. 66.
    Langin G, Gouguet P, Üstün S. 2020. Microbial effector proteins: a journey through the proteolytic landscape. Trends Microbiol 28:7523–35
     [Google Scholar]
  67. 67.
    Lee BJ, Kwon SJ, Kim SK, Kim KJ, Park CJ et al. 2006. Functional study of hot pepper 26S proteasome subunit RPN7 induced by Tobacco mosaic virus from nuclear proteome analysis. Biochem. Biophys. Res. Commun. 351:2405–11
     [Google Scholar]
  68. 68.
    Leong JX, Raffeiner M, Spinti D, Langin G, Franz-Wachtel M et al. 2022. A bacterial effector counteracts host autophagy by promoting degradation of an autophagy component. EMBO J 41:13e110352
     [Google Scholar]
  69. 69.
    Lequeu J, Simon-Plas F, Fromentin J, Etienne P, Petitot AS et al. 2005. Proteasome comprising a β1 inducible subunit acts as a negative regulator of NADPH oxidase during elicitation of plant defense reactions. FEBS Lett 579:214879–86
     [Google Scholar]
  70. 70.
    Li J, Chu ZH, Batoux M, Nekrasov V, Roux M et al. 2009. Specific ER quality control components required for biogenesis of the plant innate immune receptor EFR. PNAS 106:3715973–78
     [Google Scholar]
  71. 71.
    Lim G-H, Hoey T, Zhu S, Clavel M, Yu K et al. 2018. COP1, a negative regulator of photomorphogenesis, positively regulates plant disease resistance via double-stranded RNA binding proteins. PLOS Pathog. 14:3e1006894
     [Google Scholar]
  72. 72.
    Lin Y, Hu Q, Zhou J, Yin W, Yao D et al. 2021. Phytophthora sojae effector Avr1d functions as an E2 competitor and inhibits ubiquitination activity of GmPUB13 to facilitate infection. PNAS 118:10e2018312118
     [Google Scholar]
  73. 73.
    Liu J, Huang Y, Kong L, Yu X, Feng B et al. 2020. The malectin-like receptor-like kinase LETUM1 modulates NLR protein SUMM2 activation via MEKK2 scaffolding. Nat. Plants 6:91106–15
     [Google Scholar]
  74. 74.
    Liu J, Park CH, He F, Nagano M, Wang M et al. 2015. The RhoGAP SPIN6 associates with SPL11 and OsRac1 and negatively regulates programmed cell death and innate immunity in rice. PLOS Pathog 11:2e1004629
     [Google Scholar]
  75. 75.
    Liu X, Zhou Y, Du M, Liang X, Fan F et al. 2022. The calcium-dependent protein kinase CPK28 is targeted by the ubiquitin ligases ATL31 and ATL6 for proteasome-mediated degradation to fine-tune immune signaling in Arabidopsis. Plant Cell 34:1679–97
     [Google Scholar]
  76. 76.
    Lozano-Durán R, Rosas-Díaz T, Gusmaroli G, Luna AP, Taconnat L et al. 2011. Geminiviruses subvert ubiquitination by altering CSN-mediated derubylation of SCF E3 ligase complexes and inhibit jasmonate signaling in Arabidopsis thaliana. Plant Cell 23:31014–32
     [Google Scholar]
  77. 77.
    Lu D, Lin W, Gao X, Wu S, Cheng C et al. 2011. Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332:60361439–42
     [Google Scholar]
  78. 78.
    Ma A, Zhang D, Wang G, Wang K, Li Z et al. 2021. Verticillium dahliae effector VDAL protects MYB6 from degradation by interacting with PUB25 and PUB26 E3 ligases to enhance Verticillium wilt resistance. Plant Cell 33:123675–99
     [Google Scholar]
  79. 79.
    Ma W, Xu X, Cai L, Cao Y, Haq F et al. 2020. A Xanthomonas oryzae type III effector XopL causes cell death through mediating ferredoxin degradation in Nicotiana benthamiana. Phytopathol. Res. 2:16
     [Google Scholar]
  80. 80.
    Mackey D, Yun D, Nam J. 2021. Proteasome-dependent degradation of RPM1 desensitizes the RPM1-mediated hypersensitive response. J. Plant Biol. 64:3217–25
     [Google Scholar]
  81. 81.
    MacLean AM, Orlovskis Z, Kowitwanich K, Zdziarska AM, Angenent GC et al. 2014. Phytoplasma effector SAP54 hijacks plant reproduction by degrading MADS-box proteins and promotes insect colonization in a RAD23-dependent manner. PLOS Biol 12:4e1001835
     [Google Scholar]
  82. 82.
    Maejima K, Kitazawa Y, Tomomitsu T, Yusa A, Neriya Y et al. 2015. Degradation of class E MADS-domain transcription factors in Arabidopsis by a phytoplasmal effector, phyllogen. Plant Signal. Behav. 10:8e1042635
     [Google Scholar]
  83. 83.
    Marshall RS, Vierstra RD. 2019. Dynamic regulation of the 26S proteasome: from synthesis to degradation. Front. Mol. Biosci. 6:40
     [Google Scholar]
  84. 84.
    Matsushita A, Inoue H, Goto S, Nakayama A, Sugano S et al. 2013. Nuclear ubiquitin proteasome degradation affects WRKY45 function in the rice defense program. Plant J 73:2302–13
     [Google Scholar]
  85. 85.
    McLellan H, Chen K, He Q, Wu X, Boevink PC et al. 2020. The ubiquitin E3 ligase PUB17 positively regulates immunity by targeting a negative regulator, KH17, for degradation. Plant Commun 1:4100020
     [Google Scholar]
  86. 86.
    Miao M, Niu X, Kud J, Du X, Avila J et al. 2016. The ubiquitin ligase SEVEN IN ABSENTIA (SINA) ubiquitinates a defense-related NAC transcription factor and is involved in defense signaling. New Phytol 211:1138–48
     [Google Scholar]
  87. 87.
    Millyard L, Lee J, Zhang C, Yates G, Sadanandom A. 2016. The ubiquitin conjugating enzyme, TaU4 regulates wheat defence against the phytopathogen Zymoseptoria tritici. Sci. Rep. 6:35683
     [Google Scholar]
  88. 88.
    Misas-Villamil JC, Kolodziejek I, Crabill E, Kaschani F, Niessen S et al. 2013. Pseudomonas syringae pv. syringae uses proteasome inhibitor syringolin A to colonize from wound infection sites. PLOS Pathog 9:310–16
     [Google Scholar]
  89. 89.
    Mithoe SC, Menke FL. 2018. Regulation of pattern recognition receptor signalling by phosphorylation and ubiquitination. Curr. Opin. Plant Biol. 45:Pt. A162–70
     [Google Scholar]
  90. 90.
    Müller J, Piffanelli P, Devoto A, Miklis M, Elliott C et al. 2005. Conserved ERAD-like quality control of a plant polytopic membrane protein. Plant Cell 17:1149–63
     [Google Scholar]
  91. 91.
    Nakano M, Oda K, Mukaihara T. 2017. Ralstonia solanacearum novel E3 ubiquitin ligase (NEL) effectors RipAW and RipAR suppress pattern-triggered immunity in plants. Microbiology 163:7992–1002
     [Google Scholar]
  92. 92.
    Ngou BPM, Ding P, Jones JDG. 2022. Thirty years of resistance: zig-zag through the plant immune system. Plant Cell 34:51447–78
     [Google Scholar]
  93. 93.
    Ngou BPM, Heal R, Wyler M, Schmid MW, Jones JDG. 2022. Concerted expansion and contraction of immune receptor gene repertoires in plant genomes. Nat. Plants 8:101146–52
     [Google Scholar]
  94. 94.
    Ning Y, Shi X, Wang R, Fan J, Park CH et al. 2015. OsELF3-2, an ortholog of Arabidopsis ELF3, interacts with the E3 ligase APIP6 and negatively regulates immunity against Magnaporthe oryzae in rice. Mol. Plant 8:111679–82
     [Google Scholar]
  95. 95.
    Nirmala J, Dahl S, Steffenson BJ, Kannangara CG, von Wettstein D et al. 2007. Proteolysis of the barley receptor-like protein kinase RPG1 by a proteasome pathway is correlated with Rpg1-mediated stem rust resistance. PNAS 104:2410276–81
     [Google Scholar]
  96. 96.
    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 313:5784220–23
     [Google Scholar]
  97. 97.
    Orosa B, He Q, Mesmar J, Gilroy EM, McLellan H et al. 2017. BTB-BACK domain protein POB1 suppresses immune cell death by targeting ubiquitin E3 ligase PUB17 for degradation. PLOS Genet 13:1e1006540
     [Google Scholar]
  98. 98.
    Orosa B, Üstün S, Calderón Villalobos LIA, Genschik P, Gibbs D et al. 2020. Plant proteostasis—shaping the proteome: a research community aiming to understand molecular mechanisms that control protein abundance. New Phytol 227:41028–33
     [Google Scholar]
  99. 99.
    Pant BD, Oh S, Lee HK, Nandety RS, Mysore KS. 2020. Antagonistic regulation by CPN60A and CLPC1 of TRXL1 that regulates MDH activity leading to plant disease resistance and thermotolerance. Cell Rep 33:11108515
     [Google Scholar]
  100. 100.
    Park CH, Shirsekar G, Bellizzi M, Chen S, Songkumarn P et al. 2016. The E3 ligase APIP10 connects the effector AvrPiz-t to the NLR receptor Piz-t in rice. PLOS Pathog 12:3e1005529
     [Google Scholar]
  101. 101.
    Petutschnig EK, Stolze M, Lipka U, Kopischke M, Horlacher J et al. 2014. A novel Arabidopsis CHITIN ELICITOR RECEPTOR KINASE 1 (CERK1) mutant with enhanced pathogen-induced cell death and altered receptor processing. New Phytol 204:4955–67
     [Google Scholar]
  102. 102.
    Qin J, Zhou X, Sun L, Wang K, Yang F et al. 2018. The Xanthomonas effector XopK harbours E3 ubiquitin-ligase activity that is required for virulence. New Phytol 220:1219–31
     [Google Scholar]
  103. 103.
    Qin T, Liu S, Zhang Z, Sun L, He X et al. 2019. GhCyP3 improves the resistance of cotton to Verticillium dahliae by inhibiting the E3 ubiquitin ligase activity of GhPUB17. Plant Mol. Biol. 99:4–5379–93
     [Google Scholar]
  104. 104.
    Raffeiner M, Üstün S, Guerra T, Spinti D, Fitzner M et al. 2022. The Xanthomonas type-III effector XopS stabilizes CaWRKY40a to regulate defense responses and stomatal immunity in pepper (Capsicum annuum). Plant Cell 34:51684–708
     [Google Scholar]
  105. 105.
    Ramachandran P, Joshi JB, Maupin-Furlow JA, Uthandi S. 2021. Bacterial effectors mimicking ubiquitin-proteasome pathway tweak plant immunity. Microbiol. Res. 250:126810
     [Google Scholar]
  106. 106.
    Roussin-Léveillée C, Lajeunesse G, St-Amand M, Veerapen VP, Silva-Martins G et al. 2022. Evolutionarily conserved bacterial effectors hijack abscisic acid signaling to induce an aqueous environment in the apoplast. Cell Host Microbe 30:4489–501.e4
     [Google Scholar]
  107. 107.
    Sahana N, Kaur H, Basavaraj, Tena F, Jain RK et al. 2012. Inhibition of the host proteasome facilitates Papaya ringspot virus accumulation and proteosomal catalytic activity is modulated by viral factor HcPro. PLOS ONE 7:12e52546
     [Google Scholar]
  108. 108.
    Sahu PP, Sharma N, Puranik S, Chakraborty S, Prasad M. 2016. Tomato 26S proteasome subunit RPT4a regulates ToLCNDV transcription and activates hypersensitive response in tomato. Sci. Rep 6:27078
     [Google Scholar]
  109. 109.
    Saile SC, Ackermann FM, Sunil S, Keicher J, Bayless A et al. 2021. Arabidopsis ADR1 helper NLR immune receptors localize and function at the plasma membrane in a phospholipid dependent manner. New Phytol 232:62440–56
     [Google Scholar]
  110. 110.
    Shimono M, Koga H, Akagi A, Hayashi N, Goto S et al. 2012. Rice WRKY45 plays important roles in fungal and bacterial disease resistance. Mol. Plant Pathol. 13:183–94
     [Google Scholar]
  111. 111.
    Shimono M, Sugano S, Nakayama A, Jiang CJ, Ono K et al. 2007. Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19:62064–76
     [Google Scholar]
  112. 112.
    Shu K, Yang W. 2017. E3 ubiquitin ligases: ubiquitous actors in plant development and abiotic stress responses. Plant Cell Physiol. 58:91461–76
     [Google Scholar]
  113. 113.
    Shukla A, Üstün S, Hafrén A 2021. Proteasome homeostasis is essential for a robust cauliflower mosaic virus infection. bioRxiv 436740. https://doi.org/10.1101/2021.03.24.436740
  114. 114.
    Singer AU, Schulze S, Skarina T, Xu X, Cui H et al. 2013. A pathogen type III effector with a novel E3 ubiquitin ligase architecture. PLOS Pathog 9:1e1003121
     [Google Scholar]
  115. 115.
    Skelly MJ, Furniss JJ, Grey H, Wong K-W, Spoel SH 2019. Dynamic ubiquitination determines transcriptional activity of the plant immune coactivator NPR1. eLife 8:e47005
     [Google Scholar]
  116. 116.
    Soni M, Mondal KK. 2018. Xanthomonas axonopodis pv. punicae uses XopL effector to suppress pomegranate immunity. J. Integr. Plant Biol. 60:4341–57
     [Google Scholar]
  117. 117.
    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 137:5860–72
     [Google Scholar]
  118. 118.
    Stegmann M, Anderson RG, Ichimura K, Pecenkova T, Reuter P et al. 2012. The ubiquitin ligase PUB22 targets a subunit of the exocyst complex required for PAMP-triggered responses in Arabidopsis. Plant Cell 24:114703–16
     [Google Scholar]
  119. 119.
    Su W, Liu Y, Xia Y, Hong Z, Li J. 2011. Conserved endoplasmic reticulum-associated degradation system to eliminate mutated receptor-like kinases in Arabidopsis. PNAS 108:2870–75
     [Google Scholar]
  120. 120.
    Tan L, Rong W, Luo H, Chen Y, He C. 2014. The Xanthomonas campestris effector protein XopD Xcc 8004 triggers plant disease tolerance by targeting DELLA proteins. New Phytol. 204:3595–608
     [Google Scholar]
  121. 121.
    Tanaka H, Kitakura S, De Rycke R, De Groodt R, Friml J. 2009. Fluorescence imaging-based screen identifies ARF GEF component of early endosomal trafficking. Curr. Biol. 19:5391–97
     [Google Scholar]
  122. 122.
    Tanaka S, Brefort T, Neidig N, Djamei A, Kahnt J et al. 2014. A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize. eLife 3:e01355
     [Google Scholar]
  123. 123.
    Tao T, Zhou CJ, Wang Q, Chen XR, Sun Q et al. 2017. Rice black streaked dwarf virus P7-2 forms a SCF complex through binding to Oryza sativa SKP1-like proteins, and interacts with GID2 involved in the gibberellin pathway. PLOS ONE 12:5e0177518
     [Google Scholar]
  124. 124.
    Thiel H, Hleibieh K, Gilmer D, Varrelmann M. 2012. The P25 pathogenicity factor of Beet necrotic yellow vein virus targets the sugar beet 26s proteasome involved in the induction of a hypersensitive resistance response via interaction with an F-box protein. Mol. Plant-Microbe Interact. 25:81058–72
     [Google Scholar]
  125. 125.
    Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A et al. 2007. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448:7154661–65
     [Google Scholar]
  126. 126.
    Thulasi Devendrakumar K, Copeland C, Li X 2019. The proteasome regulator PTRE1 contributes to the turnover of SNC1 immune receptor. Mol. Plant Pathol. 20:111566–73
     [Google Scholar]
  127. 127.
    Till CJ, Vicente J, Zhang H, Oszvald M, Deery MJ et al. 2019. The Arabidopsis thaliana N-recognin E3 ligase PROTEOLYSIS1 influences the immune response. Plant Dir 3:12e00194
     [Google Scholar]
  128. 128.
    Üstün S, Bartetzko V, Börnke F. 2013. The Xanthomonas campestris type III effector XopJ targets the host cell proteasome to suppress salicylic-acid mediated plant defence. PLOS Pathog 9:6e1003427
     [Google Scholar]
  129. 129.
    Üstün S, Bartetzko V, Börnke F. 2015. The Xanthomonas effector XopJ triggers a conditional hypersensitive response upon treatment of N. benthamiana leaves with salicylic acid. Front. Plant Sci. 6:599
     [Google Scholar]
  130. 130.
    Üstün S, Börnke F. 2015. The Xanthomonas campestris type III effector XopJ proteolytically degrades proteasome subunit RPT6. Plant Physiol 168:1107–19
     [Google Scholar]
  131. 131.
    Üstün S, Hafrén A, Liu Q, Marshall RS, Minina EA et al. 2018. Bacteria exploit autophagy for proteasome degradation and enhanced virulence in plants. Plant Cell 30:3668–85
     [Google Scholar]
  132. 132.
    Üstün S, König P, Guttman DS, Börnke F. 2014. HopZ4 from Pseudomonas syringae, a member of the HopZ Type III effector family from the YopJ superfamily, inhibits the proteasome in plants. Mol. Plant-Microbe Interact. 27:7611–23
     [Google Scholar]
  133. 133.
    Üstün S, Sheikh A, Gimenez-Ibanez S, Jones A, Ntoukakis V, Börnke F. 2016. The proteasome acts as a hub for plant immunity and is targeted by Pseudomonas type III effectors. Plant Physiol 172:31941–58
     [Google Scholar]
  134. 134.
    Vicente J, Mendiondo GM, Pauwels J, Pastor V, Izquierdo Y et al. 2019. Distinct branches of the N-end rule pathway modulate the plant immune response. New Phytol 221:2988–1000
     [Google Scholar]
  135. 135.
    Vierstra RD. 2009. The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 10:6385–97
     [Google Scholar]
  136. 136.
    Wang J, Grubb LE, Wang J, Liang X, Li L et al. 2018. A regulatory module controlling homeostasis of a plant immune kinase. Mol. Cell 69:3493–504.e6
     [Google Scholar]
  137. 137.
    Wang J, Wang R, Fang H, Zhang C, Zhang F et al. 2021. Two VOZ transcription factors link an E3 ligase and an NLR immune receptor to modulate immunity in rice. Mol. Plant 14:2253–66
     [Google Scholar]
  138. 138.
    Wang S, Li Q, Zhao L, Fu S, Qin L et al. 2020. Arabidopsis UBC22, an E2 able to catalyze lysine-11 specific ubiquitin linkage formation, has multiple functions in plant growth and immunity. Plant Sci 297:110520
     [Google Scholar]
  139. 139.
    Wang T, Chang C, Gu C, Tang S, Xie Q, Shen Q-H. 2016. An E3 ligase affects the NLR receptor stability and immunity to powdery mildew. Plant Physiol 172:42504–15
     [Google Scholar]
  140. 140.
    Wang Z, Orosa-Puente B, Nomoto M, Grey H, Potuschak T et al. 2022. Proteasome-associated ubiquitin ligase relays target plant hormone-specific transcriptional activators. Sci. Adv. 8:424466
     [Google Scholar]
  141. 141.
    Wu Z, Tong M, Tian L, Zhu C, Liu X et al. 2020. Plant E3 ligases SNIPER 1 and SNIPER 2 broadly regulate the homeostasis of sensor NLR immune receptors. EMBO J 39:15e104915
     [Google Scholar]
  142. 142.
    Xu CC, Zhang D, Hann DR, Xie ZP, Staehelin C. 2018. Biochemical properties and in planta effects of NopM, a rhizobial E3 ubiquitin ligase. J. Biol. Chem. 293:3915304–15
     [Google Scholar]
  143. 143.
    Xu F, Huang Y, Li L, Gannon P, Linster E et al. 2015. Two N-terminal acetyltransferases antagonistically regulate the stability of a nod-like receptor in Arabidopsis. Plant Cell 27:51547–62
     [Google Scholar]
  144. 144.
    Xu FQ, Xue HW. 2019. The ubiquitin-proteasome system in plant responses to environments. Plant Cell Environ 42:102931–44
     [Google Scholar]
  145. 145.
    Yamaguchi K, Mezaki H, Fujiwara M, Hara Y, Kawasaki T. 2017. Arabidopsis ubiquitin ligase PUB12 interacts with and negatively regulates chitin elicitor receptor kinase 1 (CERK1). PLOS ONE 12:11e0188886
     [Google Scholar]
  146. 146.
    Yan J, Li H, Li S, Yao R, Deng H et al. 2013. The Arabidopsis F-box protein CORONATINE INSENSITIVE1 is stabilized by SCFCOI1 and degraded via the 26S proteasome pathway. Plant Cell 25:2486–98
     [Google Scholar]
  147. 147.
    Yan J, Yao R, Chen L, Li S, Gu M et al. 2018. Dynamic perception of jasmonates by the F-box protein COI1. Mol. Plant 11:101237–47
     [Google Scholar]
  148. 148.
    Yan X, Tao J, Luo HL, Tan LT, Rong W et al. 2019. A type III effector XopLXcc8004 is vital for Xanthomonas campestris pathovar campestris to regulate plant immunity. Res. Microbiol. 170:3138–46
     [Google Scholar]
  149. 149.
    Yang CW, González-Lamothe R, Ewan RA, Rowland O, Yoshioka H et al. 2006. 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 18:41084–98
     [Google Scholar]
  150. 150.
    Yang L, Teixeira PJPL, Biswas S, Finkel OM, He Y et al. 2017. Pseudomonas syringae type III effector HopBB1 promotes host transcriptional repressor degradation to regulate phytohormone responses and virulence. Cell Host Microbe 21:2156–68
     [Google Scholar]
  151. 151.
    Yao C, Wu Y, Nie H, Tang D. 2012. RPN1a, a 26S proteasome subunit, is required for innate immunity in Arabidopsis. Plant J 71:61015–28
     [Google Scholar]
  152. 152.
    You Q, Zhai K, Yang D, Yang W, Wu J et al. 2016. An E3 ubiquitin ligase-BAG protein module controls plant innate immunity and broad-spectrum disease resistance. Cell Host Microbe 20:6758–69
     [Google Scholar]
  153. 153.
    Yu G, Derkacheva M, Rufian JS, Brillada C, Kowarschik K et al. 2022. The Arabidopsis E3 ubiquitin ligase PUB4 regulates BIK1 and is targeted by a bacterial type-III effector. EMBO J. 41:23e107257
     [Google Scholar]
  154. 154.
    Yu Y, Xu W, Wang J, Wang L, Yao W et al. 2013. The Chinese wild grapevine (Vitis pseudoreticulata) E3 ubiquitin ligase Erysiphe necator-induced RING finger protein 1 (EIRP1) activates plant defense responses by inducing proteolysis of the VpWRKY11 transcription factor. New Phytol. 200:3834–46
     [Google Scholar]
  155. 155.
    Zhang C, Wei Y, Xu L, Wu KC, Yang L et al. 2020. A bunyavirus-inducible ubiquitin ligase targets RNA polymerase IV for degradation during viral pathogenesis in rice. Mol. Plant 13:6836–50
     [Google Scholar]
  156. 156.
    Zhang Y, Song G, Lal NK, Nagalakshmi U, Li Y et al. 2019. TurboID-based proximity labeling reveals that UBR7 is a regulator of N NLR immune receptor-mediated immunity. Nat Commun 10:13252
     [Google Scholar]
  157. 157.
    Zhao C, Rispe C, Nabity PD. 2019. Secretory RING finger proteins function as effectors in a grapevine galling insect. BMC Genom 20:1923
     [Google Scholar]
  158. 158.
    Zhou B, Mural RV, Chen X, Oates ME, Connor RA et al. 2017. A subset of ubiquitin-conjugating enzymes is essential for plant immunity. Plant Physiol 173:21371–90
     [Google Scholar]
  159. 159.
    Zhou B, Wang C, Chen X, Zhang Y, Zeng L 2021. Two ubiquitin-activating systems occur in plants with one playing a major role in plant immunity. bioRxiv 458739 https://doi.org/10.1101/2021.09.02.458739
    [Crossref]
  160. 160.
    Ziebell H, Murphy AM, Groen SC, Tungadi T, Westwood JH et al. 2011. Cucumber mosaic virus and its 2b RNA silencing suppressor modify plant-aphid interactions in tobacco. Sci. Rep. 1:187
     [Google Scholar]
  161. 161.
    Zipfel C. 2014. Plant pattern-recognition receptors. Trends Immunol 35:7345–51
     [Google Scholar]
/content/journals/10.1146/annurev-phyto-021622-110443
Loading
The Plant Ubiquitin–Proteasome System as a Target for Microbial Manipulation
Annual Review of Phytopathology 61, 351 (2023); https://doi.org/10.1146/annurev-phyto-021622-110443
/content/journals/10.1146/annurev-phyto-021622-110443
/content/journals/10.1146/annurev-phyto-021622-110443
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error