1932

Abstract

Posttranslational modifications add complexity and diversity to cellular proteomes. One of the most prevalent modifications across eukaryotes is ubiquitination, which is orchestrated by E3 ubiquitin ligases. U-box-containing E3 ligases have massively expanded in the plant kingdom and have diversified into plant U-box proteins (PUBs). PUBs likely originated from two or three ancestral forms, fusing with diverse functional subdomains that resulted in neofunctionalization. Their emergence and diversification may reflect adaptations to stress during plant evolution, reflecting changes in the needs of plant proteomes to maintain cellular homeostasis. Through their close association with protein kinases, they are physically linked to cell signaling hubs and activate feedback loops by dynamically pairing with E2-ubiquitin-conjugating enzymes to generate distinct ubiquitin polymers that themselves act as signals. Here, we complement current knowledgewith comparative genomics to gain a deeper understanding of PUB function, focusing on their evolution and structural adaptations of key U-box residues, as well as their various roles in plant cells.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-102720-012310
2022-05-20
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/arplant/73/1/annurev-arplant-102720-012310.html?itemId=/content/journals/10.1146/annurev-arplant-102720-012310&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Andersen P, Kragelund BB, Olsen AN, Larsen FH, Chua N-H et al. 2004. Structure and biochemical function of a prototypical Arabidopsis U-box domain. J. Biol. Chem. 279:40053–61
    [Google Scholar]
  2. 2.
    Antignani V, Klocko AL, Bak G, Chandrasekaran SD, Dunivin T, Nielsen E 2015. Recruitment of PLANT U-BOX13 and the PI4Kβ1/β2 phosphatidylinositol-4 kinases by the small GTPase RabA4B plays important roles during salicylic acid-mediated plant defense signaling in Arabidopsis. Plant Cell 27:243–61
    [Google Scholar]
  3. 3.
    Aravind L, Koonin EV. 2000. The U box is a modified RING finger—a common domain in ubiquitination. Curr. Biol. 10:R132–34
    [Google Scholar]
  4. 4.
    Azevedo C, Santos-Rosa MJ, Shirasu K. 2001. The U-box protein family in plants. Trends Plant Sci 6:354–58
    [Google Scholar]
  5. 5.
    Baek M, DiMaio F, Anishchenko I, Dauparas J, Ovchinnikov S et al. 2021. Accurate prediction of protein structures and interactions using a three-track neural network. Science 373:871–76
    [Google Scholar]
  6. 6.
    Ballinger CA, Connell P, Wu Y, Hu Z, Thompson LJ et al. 1999. Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol. Cell. Biol. 19:4535–45
    [Google Scholar]
  7. 7.
    Benirschke RC, Thompson JR, Nominé Y, Wasielewski E, Juranic N et al. 2010. Molecular basis for the association of human E4B U box ubiquitin ligase with E2-conjugating enzymes UbcH5c and Ubc4. Structure 18:955–65
    [Google Scholar]
  8. 8.
    Bentham AR, De la Concepcion JC, Mukhi N, Zdrzalek R, Draeger M et al. 2020. A molecular roadmap to the plant immune system. J. Biol. Chem. 295:14916–35
    [Google Scholar]
  9. 9.
    Berndsen CE, Wolberger C. 2014. New insights into ubiquitin E3 ligase mechanism. Nat. Struct. Mol. Biol. 21:301–7
    [Google Scholar]
  10. 10.
    Bos JI, 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 107:9909–14
    [Google Scholar]
  11. 11.
    Bürger M, Chory J. 2019. Stressed out about hormones: how plants orchestrate immunity. Cell Host Microbe 26:163–72
    [Google Scholar]
  12. 12.
    Burroughs AM, Iyer LM, Aravind L. 2012. The natural history of ubiquitin and ubiquitin-related domains. Front. Biosci. Landmark 17:1433–60
    [Google Scholar]
  13. 13.
    Chanarat S, Sträßer K. 2013. Splicing and beyond: the many faces of the Prp19 complex. Biochim. Biophys. Acta Mol. Cell Res. 1833:2126–34
    [Google Scholar]
  14. 14.
    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 22:777–88.e7
    [Google Scholar]
  15. 15.
    Chen X, Wang T, Rehman AU, Wang Y, Qi J et al. 2021. Arabidopsis U-box E3 ubiquitin ligase PUB11 negatively regulates drought tolerance by degrading the receptor-like protein kinases LRR1 and KIN7. J. Integr. Plant Biol. 63:494–509
    [Google Scholar]
  16. 16.
    Chen YC, Wong CL, Muzzi F, Vlaardingerbroek I, Kidd BN, Schenk PM. 2014. Root defense analysis against Fusarium oxysporum reveals new regulators to confer resistance. Sci. Rep. 4:5584
    [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 108:14694–99
    [Google Scholar]
  18. 18.
    Chi YH, Koo SS, Oh HT, Lee ES, Park JH et al. 2019. The physiological functions of universal stress proteins and their molecular mechanism to protect plants from environmental stresses. Front. Plant Sci. 10:750
    [Google Scholar]
  19. 19.
    Cho SK, Bae H, Ryu MY, Wook Yang S, Kim WT. 2015. PUB22 and PUB23 U-BOX E3 ligases directly ubiquitinate RPN6, a 26S proteasome lid subunit, for subsequent degradation in Arabidopsis thaliana. Biochem. Biophys. Res. Commun. 464:994–99
    [Google Scholar]
  20. 20.
    Cho SK, Ryu MY, Song C, Kwak JM, Kim WT. 2008. Arabidopsis PUB22 and PUB23 are homologous U-box E3 ubiquitin ligases that play combinatory roles in response to drought stress. Plant Cell 20:1899–914
    [Google Scholar]
  21. 21.
    Christensen DE, Brzovic PS, Klevit RE. 2007. E2-BRCA1 RING interactions dictate synthesis of mono- or specific polyubiquitin chain linkages. Nat. Struct. Mol. Biol. 14:941–48
    [Google Scholar]
  22. 22.
    Copeland C, Woloshen V, Huang Y, Li X. 2016. AtCDC48A is involved in the turnover of an NLR immune receptor. Plant J 88:294–305
    [Google Scholar]
  23. 23.
    de Moura TR, Mozaffari-Jovin S, Szabó CZK, Schmitzová J, Dybkov O et al. 2018. Prp19/Pso4 is an autoinhibited ubiquitin ligase activated by stepwise assembly of three splicing factors. Mol. Cell 69:979–92.e6
    [Google Scholar]
  24. 24.
    Derkacheva M, Yu G, Rufian JS, Jiang S, Derbyshire P et al. 2020. The Arabidopsis E3 ubiquitin ligase PUB4 regulates BIK1 homeostasis and is targeted by a bacterial type-III effector. bioRxiv 2020.10.25.354514. https://doi.org/10.1101/2020.10.25.354514
    [Crossref]
  25. 25.
    Desaki Y, Takahashi S, Sato K, Maeda K, Matsui S et al. 2019. PUB4, a CERK1-interacting ubiquitin ligase, positively regulates MAMP-triggered immunity in Arabidopsis. Plant Cell Physiol 60:2573–83
    [Google Scholar]
  26. 26.
    Dievart A, Gottin C, Perin C, Ranwez V, Chantret N 2020. Origin and diversity of plant receptor-like kinases. Annu. Rev. Plant Biol. 71:131–56
    [Google Scholar]
  27. 27.
    Disch E-M, Tong M, Kotur T, Koch G, Wolf C-A et al. 2016. Membrane-associated ubiquitin ligase SAUL1 suppresses temperature- and humidity-dependent autoimmunity in Arabidopsis. Mol. Plant Microbe Interact. 29:69–80
    [Google Scholar]
  28. 28.
    Doucet J, Lee HK, Goring DR 2016. Pollen acceptance or rejection: a tale of two pathways. Trends Plant Sci 21:1058–67
    [Google Scholar]
  29. 29.
    Edkins AL. 2015. CHIP: a co-chaperone for degradation by the proteasome. Subcell. Biochem. 78:219–42
    [Google Scholar]
  30. 30.
    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 23:498–510.e5Revealed regulatory circuits in rice that include E3s, kinases, and NADPH oxidases.
    [Google Scholar]
  31. 31.
    Furlan G, Klinkenberg J, Trujillo M. 2012. Regulation of plant immune receptors by ubiquitination. Front. Plant Sci. 3:238
    [Google Scholar]
  32. 32.
    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 29:726–45Elucidated the first regulatory mechanism for a PUB E3.
    [Google Scholar]
  33. 33.
    Gilroy EM, Taylor RM, Hein I, Boevink P, Sadanandom A, Birch PRJ. 2011. CMPG1-dependent cell death follows perception of diverse pathogen elicitors at the host plasma membrane and is suppressed by Phytophthora infestans RXLR effector AVR3a. New Phytol 190:653–66
    [Google Scholar]
  34. 34.
    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. 19:423–29
    [Google Scholar]
  35. 35.
    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 18:1067–83
    [Google Scholar]
  36. 36.
    Gonzali S, Loreti E, Cardarelli F, Novi G, Parlanti S et al. 2015. Universal stress protein HRU1 mediates ROS homeostasis under anoxia. Nat. Plants 1:15151
    [Google Scholar]
  37. 37.
    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 69:411–20
    [Google Scholar]
  38. 38.
    Grubb LE, Derbyshire P, Dunning KE, Zipfel C, Menke FLH, Monaghan J. 2021. Large-scale identification of ubiquitination sites on membrane-associated proteins in Arabidopsis thaliana seedlings. Plant Physiol 185:1483–88
    [Google Scholar]
  39. 39.
    Gu T, Mazzurco M, Sulaman W, Matias DD, Goring DR 1998. Binding of an arm repeat protein to the kinase domain of the S-locus receptor kinase. PNAS 95:382–87
    [Google Scholar]
  40. 40.
    Hanzelmann P, Stingele J, Hofmann K, Schindelin H, Raasi S. 2010. The yeast E4 ubiquitin ligase Ufd2 interacts with the ubiquitin-like domains of Rad23 and Dsk2 via a novel and distinct ubiquitin-like binding domain. J. Biol. Chem. 285:20390–98
    [Google Scholar]
  41. 41.
    Hellerschmied D, Roessler M, Lehner A, Gazda L, Stejskal K et al. 2018. UFD-2 is an adaptor-assisted E3 ligase targeting unfolded proteins. Nat. Commun. 9:484
    [Google Scholar]
  42. 42.
    Hu D, Xie Q, Liu Q, Zuo T, Zhang H et al. 2019. Genome-wide distribution, expression and function analysis of the U-box gene family in Brassica oleracea L. Genes 10:1000
    [Google Scholar]
  43. 43.
    Hu H, Dong C, Sun D, Hu Y, Xie J. 2018. Genome-wide identification and analysis of U-box E3 ubiquitin-protein ligase gene family in banana. Int. J. Mol. Sci. 19:3874
    [Google Scholar]
  44. 44.
    Hu X, Qian Q, Xu T, Zhang Y, Dong G et al. 2013. The U-box E3 ubiquitin ligase TUD1 functions with a heterotrimeric G α subunit to regulate Brassinosteroid-mediated growth in rice. PLOS Genet 9:e1003391
    [Google Scholar]
  45. 45.
    Huang Y, Minaker S, Roth C, Huang S, Hieter P et al. 2014. An E4 ligase facilitates polyubiquitination of plant immune receptor resistance proteins in Arabidopsis. Plant Cell 26:485–96Showed that the Arabidopsis UFD2 ortholog contributes to the elongation of ubiquitin chains.
    [Google Scholar]
  46. 46.
    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. 5:5430Identified the rice PUB44 as a direct target of the Xanthomonas effector XopP.
    [Google Scholar]
  47. 47.
    Ivanov R, Gaude T. 2009. Endocytosis and endosomal regulation of the S-receptor kinase during the self-incompatibility response in Brassica oleracea. Plant Cell 21:2107–17
    [Google Scholar]
  48. 48.
    Jacobs S, Zechmann B, Molitor A, Trujillo M, Petutschnig E et al. 2011. Broad-spectrum suppression of innate immunity is required for colonization of Arabidopsis roots by the fungus Piriformospora indica. Plant Physiol 156:726–40
    [Google Scholar]
  49. 49.
    Janjusevic R, Abramovitch RB, Martin GB, Stebbins CE 2006. A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Science 311:222–26
    [Google Scholar]
  50. 50.
    Jia T, Zhang B, You C, Zhang Y, Zeng L et al. 2017. The Arabidopsis MOS4-associated complex promotes microRNA biogenesis and precursor messenger RNA splicing. Plant Cell 29:2626–43
    [Google Scholar]
  51. 51.
    Jing H, Yang X, Zhang J, Liu X, Zheng H et al. 2015. Peptidyl-prolyl isomerization targets rice Aux/IAAs for proteasomal degradation during auxin signalling. Nat. Commun. 6:7395
    [Google Scholar]
  52. 52.
    Johnson ES, Ma PC, Ota IM, Varshavsky A. 1995. A proteolytic pathway that recognizes ubiquitin as a degradation signal. J. Biol. Chem. 270:17442–56
    [Google Scholar]
  53. 53.
    Jung C, Zhao P, Seo JS, Mitsuda N, Deng S, Chua N-H. 2015. PLANT U-BOX PROTEIN10 regulates MYC2 stability in Arabidopsis. Plant Cell 27:2016–31
    [Google Scholar]
  54. 54.
    Jung YJ, Melencion SM, Lee ES, Park JH, Alinapon CV et al. 2015. Universal stress protein exhibits a redox-dependent chaperone function in Arabidopsis and enhances plant tolerance to heat shock and oxidative stress. Front. Plant Sci. 6:1141
    [Google Scholar]
  55. 55.
    Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ. 2015. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10:845–58
    [Google Scholar]
  56. 56.
    Kim DJ, Bitto E, Bingman CA, Kim H-J, Han BW, Phillips GNJr. 2015. Crystal structure of the protein At3g01520, a eukaryotic universal stress protein-like protein from Arabidopsis thaliana in complex with AMP. Proteins 83:1368–73
    [Google Scholar]
  57. 57.
    Kim DY, Lee YJ, Hong MJ, Kim JH, Seo YW. 2021. Genome wide analysis of U-box E3 ubiquitin ligases in wheat (Triticum aestivum L.). Int. J. Mol. Sci. 22:2699
    [Google Scholar]
  58. 58.
    Kim E-J, Lee S-H, Park C-H, Kim S-H, Hsu C-C et al. 2019. Plant U-box40 mediates degradation of the brassinosteroid-responsive transcription factor BZR1 in Arabidopsis roots. Plant Cell 31:791–808
    [Google Scholar]
  59. 59.
    Kim M, Cho HS, Kim D-M, Lee JH, Pai H-S. 2003. CHRK1, a chitinase-related receptor-like kinase, interacts with NtPUB4, an armadillo repeat protein, in tobacco. Biochim. Biophys. Acta Proteins Proteom. 1651:50–59
    [Google Scholar]
  60. 60.
    Kinoshita A, Seo M, Kamiya Y, Sawa S. 2015. Mystery in genetics: PUB4 gives a clue to the complex mechanism of CLV signaling pathway in the shoot apical meristem. Plant Signal. Behav. 10:e1028707
    [Google Scholar]
  61. 61.
    Kinoshita A, ten Hove CA, Tabata R, Yamada M, Shimizu N et al. 2015. A plant U-box protein, PUB4, regulates asymmetric cell division and cell proliferation in the root meristem. Development 142:444–53PUB4 was identified as a component of CLV3/CLE signaling in the root meristem.
    [Google Scholar]
  62. 62.
    Kitashiba H, Liu P, Nishio T, Nasrallah JB, Nasrallah ME. 2011. Functional test of Brassica self-incompatibility modifiers in Arabidopsis thaliana. PNAS 108:18173–78
    [Google Scholar]
  63. 63.
    Koegl M, Hoppe T, Schlenker S, Ulrich HD, Mayer TU, Jentsch S 1999. A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly. Cell 96:635–44
    [Google Scholar]
  64. 64.
    Kong L, Cheng J, Zhu Y, Ding Y, Meng J et al. 2015. Degradation of the ABA co-receptor ABI1 by PUB12/13 U-box E3 ligases. Nat. Commun. 6:8630
    [Google Scholar]
  65. 65.
    Kowarschik K, Hoehenwarter W, Marillonnet S, Trujillo M 2018. UbiGate: a synthetic biology toolbox to analyse ubiquitination. New Phytol 217:1749–63
    [Google Scholar]
  66. 66.
    Kraft E, Stone SL, Ma L, Su N, Gao Y et al. 2005. Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis. Plant Physiol 139:1597–611
    [Google Scholar]
  67. 67.
    Kwon YT, Ciechanover A. 2017. The ubiquitin code in the ubiquitin-proteasome system and autophagy. Trends Biochem. Sci. 42:873–86
    [Google Scholar]
  68. 68.
    Lake MW, Wuebbens MM, Rajagopalan KV, Schindelin H. 2001. Mechanism of ubiquitin activation revealed by the structure of a bacterial MoeB-MoaD complex. Nature 414:325–29
    [Google Scholar]
  69. 69.
    Lee S, Lee DW, Lee Y, Mayer U, Stierhof Y-D et al. 2009. Heat shock protein cognate 70–4 and an E3 ubiquitin ligase, CHIP, mediate plastid-destined precursor degradation through the ubiquitin-26S proteasome system in Arabidopsis. Plant Cell 21:3984–4001
    [Google Scholar]
  70. 70.
    Leidel S, Pedrioli PG, Bucher T, Brost R, Costanzo M et al. 2009. Ubiquitin-related modifier Urm1 acts as a sulphur carrier in thiolation of eukaryotic transfer RNA. Nature 458:228–32
    [Google Scholar]
  71. 71.
    Lewis JD, Lee AH, Hassan JA, Wan J, Hurley B et al. 2013. The Arabidopsis ZED1 pseudokinase is required for ZAR1-mediated immunity induced by the Pseudomonas syringae type III effector HopZ1a. PNAS 110:18722–27
    [Google Scholar]
  72. 72.
    Li J, Zhang Y, Gao Z, Xu X, Wang Y et al. 2021. Plant U-box E3 ligases PUB25 and PUB26 control organ growth in Arabidopsis. New Phytol 229:403–13
    [Google Scholar]
  73. 73.
    Li S, Liu K, Zhou B, Li M, Zhang S et al. 2018. MAC3A and MAC3B, two core subunits of the MOS4-associated complex, positively influence miRNA biogenesis. Plant Cell 30:481–94Prp19a and Prp19b act redundantly in microRNA biogenesis, suggesting a conserved role in plants.
    [Google Scholar]
  74. 74.
    Li W, Ahn IP, Ning Y, Park CH, Zeng L et al. 2012. The U-Box/ARM E3 ligase PUB13 regulates cell death, defense, and flowering time in Arabidopsis. Plant Physiol 159:239–50
    [Google Scholar]
  75. 75.
    Liang X, Ding P, Lian K, Wang J, Ma M et al. 2016. Arabidopsis heterotrimeric G proteins regulate immunity by directly coupling to the FLS2 receptor. eLife 5:e13568
    [Google Scholar]
  76. 76.
    Liao D, Cao Y, Sun X, Espinoza C, Nguyen CT et al. 2017. Arabidopsis E3 ubiquitin ligase PLANT U-BOX13 (PUB13) regulates chitin receptor LYSIN MOTIF RECEPTOR KINASE5 (LYK5) protein abundance. New Phytol. 214:1646–56
    [Google Scholar]
  77. 77.
    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:e2018312118Showed mechanistic and structural basis of PUB13 inhibition by the Avr1D effector in soybean.
    [Google Scholar]
  78. 78.
    Liu C, Liu W, Ye Y, Li W 2017. Ufd2p synthesizes branched ubiquitin chains to promote the degradation of substrates modified with atypical chains. Nat. Commun. 8:14274
    [Google Scholar]
  79. 79.
    Liu J, Deng J, Zhu F, Li Y, Lu Z et al. 2018. The MtDMI2-MtPUB2 negative feedback loop plays a role in nodulation homeostasis. Plant Physiol 176:3003–26
    [Google Scholar]
  80. 80.
    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:e1004629
    [Google Scholar]
  81. 81.
    Liu Y-C, Wu Y-R, Huang X-H, Sun J, Xie Q 2011. AtPUB19, a U-box E3 ubiquitin ligase, negatively regulates abscisic acid and drought responses in Arabidopsis thaliana. Mol. Plant 4:938–46
    [Google Scholar]
  82. 82.
    Lozano-Durán R, Macho AP, Boutrot F, Segonzac C, Somssich IE, Zipfel C. 2013. The transcriptional regulator BZR1 mediates trade-off between plant innate immunity and growth. eLife 2:e00983
    [Google Scholar]
  83. 83.
    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 332:1439–42
    [Google Scholar]
  84. 84.
    Lu X, Shu N, Wang D, Wang J, Chen X et al. 2020. Genome-wide identification and expression analysis of PUB genes in cotton. BMC Genom 21:213
    [Google Scholar]
  85. 85.
    Luo Q, Li Y, Wang W, Fei X, Deng X 2015. Genome-wide survey and expression analysis of Chlamydomonas reinhardtii U-box E3 ubiquitin ligases (CrPUBs) reveal a functional lipid metabolism module. PLOS ONE 10:e0122600
    [Google Scholar]
  86. 86.
    Ma X, Zhang C, Kim DY, Huang Y, Chatt E et al. 2021. Ubiquitylome analysis reveals a central role for the ubiquitin-proteasome system in plant innate immunity. Plant Physiol 185:1943–65
    [Google Scholar]
  87. 87.
    Mahdi LK, Huang M, Zhang X, Nakano RT, Kopp LB et al. 2020. Discovery of a family of mixed lineage kinase domain-like proteins in plants and their role in innate immune signaling. Cell Host Microbe 28:813–24.e6
    [Google Scholar]
  88. 88.
    Marcotrigiano J, Lomakin IB, Sonenberg N, Pestova TV, Hellen CU, Burley SK 2001. A conserved HEAT domain within eIF4G directs assembly of the translation initiation machinery. Mol. Cell 7:193–203
    [Google Scholar]
  89. 89.
    Marin I. 2010. Ancient origin of animal U-box ubiquitin ligases. BMC Evol. Biol. 10:331
    [Google Scholar]
  90. 90.
    Mbengue M, Bourdais G, Gervasi F, Beck M, Zhou J et al. 2016. Clathrin-dependent endocytosis is required for immunity mediated by pattern recognition receptor kinases. PNAS 113:11034–39
    [Google Scholar]
  91. 91.
    Mbengue M, Camut S, de Carvalho-Niebel F, Deslandes L, Froidure S et al. 2010. The Medicago truncatula E3 ubiquitin ligase PUB1 interacts with the LYK3 symbiotic receptor and negatively regulates infection and nodulation. Plant Cell 22:3474–88
    [Google Scholar]
  92. 92.
    Min HJ, Cui LH, Oh TR, Kim JH, Kim T-W, Kim WT. 2019. OsBZR1 turnover mediated by OsSK22-regulated U-box E3 ligase OsPUB24 in rice BR response. Plant J 99:426–38
    [Google Scholar]
  93. 93.
    Miyakawa T, Fujita Y, Yamaguchi-Shinozaki K, Tanokura M. 2013. Structure and function of abscisic acid receptors. Trends Plant Sci 18:259–66
    [Google Scholar]
  94. 94.
    Monaghan J, Xu F, Gao M, Zhao Q, Palma K et al. 2009. Two Prp19-like U-box proteins in the MOS4-associated complex play redundant roles in plant innate immunity. PLOS Pathog 5:e1000526
    [Google Scholar]
  95. 95.
    Mural RV, Liu Y, Rosebrock TR, Brady JJ, Hamera S et al. 2013. The tomato Fni3 lysine-63-specific ubiquitin-conjugating enzyme and Suv ubiquitin E2 variant positively regulate plant immunity. Plant Cell 25:3615–31
    [Google Scholar]
  96. 96.
    Murphy JM. 2020. The killer pseudokinase mixed lineage kinase domain-like protein (MLKL). Cold Spring Harb. Perspect. Biol. 12:a036376
    [Google Scholar]
  97. 97.
    Nakatsukasa K, Huyer G, Michaelis S, Brodsky JL 2008. Dissecting the ER-associated degradation of a misfolded polytopic membrane protein. Cell 132:101–12
    [Google Scholar]
  98. 98.
    Navarro-Quezada A, Schumann N, Quint M. 2013. Plant F-box protein evolution is determined by lineage-specific timing of major gene family expansion waves. PLOS ONE 8:e68672
    [Google Scholar]
  99. 99.
    Nordquist KA, Dimitrova YN, Brzovic PS, Ridenour WB, Munro KA et al. 2010. Structural and functional characterization of the monomeric U-box domain from E4B. Biochemistry 49:347–55
    [Google Scholar]
  100. 100.
    Ohi MD, Vander Kooi CW, Rosenberg JA, Chazin WJ, Gould KL. 2003. Structural insights into the U-box, a domain associated with multi-ubiquitination. Nat. Struct. Biol. 10:250–55
    [Google Scholar]
  101. 101.
    Ohi MD, Vander Kooi CW, Rosenberg JA, Ren L, Hirsch JP et al. 2005. Structural and functional analysis of essential pre-mRNA splicing factor Prp19p. Mol. Cell. Biol. 25:451–60
    [Google Scholar]
  102. 102.
    Petroski MD, Salvesen GS, Wolf DA. 2011. Urm1 couples sulfur transfer to ubiquitin-like protein function in oxidative stress. PNAS 108:1749–50
    [Google Scholar]
  103. 103.
    Planas-Riverola A, Gupta A, Betegón-Putze I, Bosch N, Ibañes M, Caño-Delgado AI. 2019. Brassinosteroid signaling in plant development and adaptation to stress. Development 146:dev151894
    [Google Scholar]
  104. 104.
    Plechanovová A, Jaffray EG, Tatham MH, Naismith JH, Hay RT. 2012. Structure of a RING E3 ligase and ubiquitin-loaded E2 primed for catalysis. Nature 489:115–20
    [Google Scholar]
  105. 105.
    Pruneda JN, Littlefield PJ, Soss SE, Nordquist KA, Chazin WJ et al. 2012. Structure of an E3:E2∼Ub complex reveals an allosteric mechanism shared among RING/U-box ligases. Mol. Cell 47:933–42
    [Google Scholar]
  106. 106.
    Richly H, Rape M, Braun S, Rumpf S, Hoege C, Jentsch S. 2005. A series of ubiquitin binding factors connects CDC48/p97 to substrate multiubiquitylation and proteasomal targeting. Cell 120:73–84
    [Google Scholar]
  107. 107.
    Romero-Barrios N, Monachello D, Dolde U, Wong A, San Clemente H et al. 2020. Advanced cataloging of lysine-63 polyubiquitin networks by genomic, interactome, and sensor-based proteomic analyses. Plant Cell 32:123–38
    [Google Scholar]
  108. 108.
    Rosebrock TR, Zeng LR, Brady JJ, Abramovitch RB, Xiao FM, Martin GB 2007. A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448:370–74
    [Google Scholar]
  109. 109.
    Samuel MA, Chong YT, Haasen KE, Aldea-Brydges MG, Stone SL, Goring DR 2009. Cellular pathways regulating responses to compatible and self-incompatible pollen in Brassica and Arabidopsis stigmas intersect at Exo70A1, a putative component of the exocyst complex. Plant Cell 21:2655–71
    [Google Scholar]
  110. 110.
    Samuel MA, Mudgil Y, Salt JN, Delmas F, Ramachandran S et al. 2008. Interactions between the S-domain receptor kinases and AtPUB-ARM E3 ubiquitin ligases suggest a conserved signaling pathway in Arabidopsis. Plant Physiol 147:2084–95
    [Google Scholar]
  111. 111.
    Senior AW, Evans R, Jumper J, Kirkpatrick J, Sifre L et al. 2020. Improved protein structure prediction using potentials from deep learning. Nature 577:706–10
    [Google Scholar]
  112. 112.
    Seo DH, Ahn MY, Park KY, Kim EY, Kim WT 2016. The N-terminal UND motif of the Arabidopsis U-box E3 Ligase PUB18 is critical for the negative regulation of ABA-mediated stomatal movement and determines its ubiquitination specificity for exocyst subunit Exo70B1. Plant Cell 28:2952–73
    [Google Scholar]
  113. 113.
    Seo DH, Ryu MY, Jammes F, Hwang JH, Turek M et al. 2012. Roles of four Arabidopsis U-box E3 ubiquitin ligases in negative regulation of abscisic acid-mediated drought stress responses. Plant Physiol 160:556–68
    [Google Scholar]
  114. 114.
    Seto D, Laflamme B, Guttman DS, Desveaux D. 2020. The Arabidopsis ZED1-related kinase genomic cluster is specifically required for effector-triggered immunity. Plant Physiol 184:1635–39
    [Google Scholar]
  115. 115.
    Sharma B, Taganna J. 2020. Genome-wide analysis of the U-box E3 ubiquitin ligase enzyme gene family in tomato. Sci. Rep. 10:9581
    [Google Scholar]
  116. 116.
    Shrestha S, Byrne DP, Harris JA, Kannan N, Eyers PA 2020. Cataloguing the dead: breathing new life into pseudokinase research. FEBS J 287:4150–69
    [Google Scholar]
  117. 117.
    Song EJ, Werner SL, Neubauer J, Stegmeier F, Aspden J et al. 2010. The Prp19 complex and the Usp4Sart3 deubiquitinating enzyme control reversible ubiquitination at the spliceosome. Genes Dev 24:1434–47
    [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 24:4703–16
    [Google Scholar]
  119. 119.
    Tang N, Ma S, Zong W, Yang N, Lv Y et al. 2016. MODD mediates deactivation and degradation of OsbZIP46 to negatively regulate ABA signaling and drought resistance in rice. Plant Cell 28:2161–77
    [Google Scholar]
  120. 120.
    Tang X, Ghimire S, Liu W, Fu X, Zhang H et al. 2020. Potato E3 ubiquitin ligase PUB27 negatively regulates drought tolerance by mediating stomatal movement. Plant Physiol. Biochem. 154:557–63
    [Google Scholar]
  121. 121.
    Tong M, Kotur T, Liang W, Vogelmann K, Kleine T et al. 2017. E3 ligase SAUL1 serves as a positive regulator of PAMP-triggered immunity and its homeostasis is monitored by immune receptor SOC3. New Phytol 215:1516–32
    [Google Scholar]
  122. 122.
    Tran JR, Tomsic LR, Brodsky JL. 2011. A Cdc48p-associated factor modulates endoplasmic reticulum-associated degradation, cell stress, and ubiquitinated protein homeostasis. J. Biol. Chem. 286:5744–55
    [Google Scholar]
  123. 123.
    Trujillo M. 2018. News from the PUB: plant U-box type E3 ubiquitin ligases. J. Exp. Bot. 69:371–84
    [Google Scholar]
  124. 124.
    Trujillo M. 2021. Ubiquitin signalling: controlling the message of surface immune receptors. New Phytol 231:47–53
    [Google Scholar]
  125. 125.
    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. 18:1396–401
    [Google Scholar]
  126. 126.
    Tu D, Li W, Ye Y, Brunger AT 2007. Structure and function of the yeast U-box-containing ubiquitin ligase Ufd2p. PNAS 104:15599–606
    [Google Scholar]
  127. 127.
    Turek I, Tischer N, Lassig R, Trujillo M. 2018. Multi-tiered pairing selectivity between E2 ubiquitin-conjugating enzymes and E3 ligases. J. Biol. Chem. 293:16324–36Identified physiological E2-E3 pairs and their regulation by immune responses.
    [Google Scholar]
  128. 128.
    Vander Kooi CW, Ohi MD, Rosenberg JA, Oldham ML, Newcomer ME et al. 2006. The Prp19 U-box crystal structure suggests a common dimeric architecture for a class of oligomeric E3 ubiquitin ligases. Biochemistry 45:121–30
    [Google Scholar]
  129. 129.
    Vasseur F, Exposito-Alonso M, Ayala-Garay OJ, Wang G, Enquist BJ et al. 2018. Adaptive diversification of growth allometry in the plant Arabidopsis thaliana. PNAS 115:3416–21
    [Google Scholar]
  130. 130.
    Vega-Sánchez ME, Zeng L, Chen S, Leung H, Wang G-L 2008. SPIN1, a K homology domain protein negatively regulated and ubiquitinated by the E3 ubiquitin ligase SPL11, is involved in flowering time control in rice. Plant Cell 20:1456–69
    [Google Scholar]
  131. 131.
    Vierstra RD. 2009. The ubiquitin-26S proteasome system at the nexus of plant biology. Nat Rev. Mol. Cell. Biol. 10:385–97
    [Google Scholar]
  132. 132.
    Wang H, Lu Y, Jiang T, Berg H, Li C, Xia Y 2013. The Arabidopsis U-box/ARM repeat E3 ligase AtPUB4 influences growth and degeneration of tapetal cells, and its mutation leads to conditional male sterility. Plant J 74:511–23
    [Google Scholar]
  133. 133.
    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 69:493–504.e6Showed the regulatory interplay between E3s, large G proteins, and kinases during the immune response.
    [Google Scholar]
  134. 134.
    Wang J, Qu B, Dou S, Li L, Yin D et al. 2015. The E3 ligase OsPUB15 interacts with the receptor-like kinase PID2 and regulates plant cell death and innate immunity. BMC Plant Biol 15:49
    [Google Scholar]
  135. 135.
    Wang L, Wen R, Wang J, Xiang D, Wang Q et al. 2019. Arabidopsis UBC13 differentially regulates two programmed cell death pathways in responses to pathogen and low-temperature stress. New Phytol 221:919–34
    [Google Scholar]
  136. 136.
    Wang N, Liu Y, Cai Y, Tang J, Li Y, Gai J 2020. The soybean U-box gene GmPUB6 regulates drought tolerance in Arabidopsis thaliana. Plant Physiol. Biochem. 155:284–96
    [Google Scholar]
  137. 137.
    Wang N, Liu Y, Cong Y, Wang T, Zhong X et al. 2016. Genome-wide identification of soybean U-box E3 ubiquitin ligases and roles of GmPUB8 in negative regulation of drought stress response in Arabidopsis. Plant Cell Physiol 57:1189–209
    [Google Scholar]
  138. 138.
    Wang W, Liu N, Gao C, Cai H, Romeis T, Tang D 2020. The Arabidopsis exocyst subunits EXO70B1 and EXO70B2 regulate FLS2 homeostasis at the plasma membrane. New Phytol 227:529–44
    [Google Scholar]
  139. 139.
    Wang W, Liu N, Gao C, Rui L, Tang D 2019. The Pseudomonas syringae effector AvrPtoB associates with and ubiquitinates Arabidopsis exocyst subunit EXO70B1. Front. Plant Sci. 10:1027
    [Google Scholar]
  140. 140.
    Wang X, Chory J 2006. Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 313:1118–22
    [Google Scholar]
  141. 141.
    Wang X, Ding Y, Li Z, Shi Y, Wang J et al. 2019. PUB25 and PUB26 promote plant freezing tolerance by degrading the cold signaling negative regulator MYB15. Dev. Cell 51:222–35.e5
    [Google Scholar]
  142. 142.
    Wang Y, Wu Y, Yu B, Yin Z, Xia Y 2017. EXTRA-LARGE G PROTEINs interact with E3 ligases PUB4 and PUB2 and function in cytokinin and developmental processes. Plant Physiol 173:1235–46
    [Google Scholar]
  143. 143.
    Wawra S, Trusch F, Matena A, Apostolakis K, Linne U et al. 2017. The RxLR motif of the host targeting effector AVR3a of Phytophthora infestans is cleaved before secretion. Plant Cell 29:1184–95
    [Google Scholar]
  144. 144.
    Whisson SC, Boevink PC, Wang S, Birch PR 2016. The cell biology of late blight disease. Curr. Opin. Microbiol. 34:127–35
    [Google Scholar]
  145. 145.
    Wiborg J, O'Shea C, Skriver K. 2008. Biochemical function of typical and variant Arabidopsis thaliana U-box E3 ubiquitin-protein ligases. Biochem. J. 413:447–57
    [Google Scholar]
  146. 146.
    Wu Z, Tong M, Tian L, Zhu C, Liu X et al. 2020. Plant E3 ligases SNIPER1 and SNIPER2 broadly regulate the homeostasis of sensor NLR immune receptors. EMBO J 39:e104915
    [Google Scholar]
  147. 147.
    Xi J, Ge Y, Kinsland C, McLafferty FW, Begley TP. 2001. Biosynthesis of the thiazole moiety of thiamin in Escherichia coli: identification of an acyldisulfide-linked protein–protein conjugate that is functionally analogous to the ubiquitin/E1 complex. PNAS 98:8513–18
    [Google Scholar]
  148. 148.
    Yang C-W, 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 18:1084–98
    [Google Scholar]
  149. 149.
    Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y. 2015. The I-TASSER Suite: protein structure and function prediction. Nat. Methods 12:7–8
    [Google Scholar]
  150. 150.
    Yang Q, Guo J, Zeng H, Xu L, Xue J et al. 2021. The receptor-like cytoplasmic kinase CDG1 negatively regulates Arabidopsis pattern-triggered immunity and is involved in AvrRpm1-induced RIN4 phosphorylation. Plant Cell 33:1341–60
    [Google Scholar]
  151. 151.
    Yee D, Goring DR 2009. The diversity of plant U-box E3 ubiquitin ligases: from upstream activators to downstream target substrates. J. Exp. Bot. 60:1109–21
    [Google Scholar]
  152. 152.
    Zeng L-R, Qu S, Bordeos A, Yang C, Baraoidan M et al. 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 16:2795–808
    [Google Scholar]
  153. 153.
    Zhang C, Song L, Choudhary MK, Zhou B, Sun G et al. 2018. Genome-wide analysis of genes encoding core components of the ubiquitin system in soybean (Glycine max) reveals a potential role for ubiquitination in host immunity against soybean cyst nematode. BMC Plant Biol 18:149
    [Google Scholar]
  154. 154.
    Zhang M, Windheim M, Roe SM, Peggie M, Cohen P et al. 2005. Chaperoned ubiquitylation—crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex. Mol. Cell 20:525–38
    [Google Scholar]
  155. 155.
    Zhang M, Zhao J, Li L, Gao Y, Zhao L et al. 2017. The Arabidopsis U-box E3 ubiquitin ligase PUB30 negatively regulates salt tolerance by facilitating BRI1 kinase inhibitor 1 (BKI1) degradation. Plant Cell Environ 40:2831–43
    [Google Scholar]
  156. 156.
    Zhao T, Rui L, Li J, Nishimura MT, Vogel JP et al. 2015. A truncated NLR protein, TIR-NBS2, is required for activated defense responses in the exo70B1 mutant. PLOS Genet 11:e1004945
    [Google Scholar]
  157. 157.
    Zhou J, Liu D, Wang P, Ma X, Lin W et al. 2018. Regulation of Arabidopsis brassinosteroid receptor BRI1 endocytosis and degradation by plant U-box PUB12/PUB13-mediated ubiquitination. PNAS 115:E1906–15Revealed that PUB12 and PUB13 mediate BRI1 endocytosis in addition to degradation of FLS2.
    [Google Scholar]
  158. 158.
    Zhou J, Lu D, Xu G, Finlayson SA, He P, Shan L. 2015. The dominant negative ARM domain uncovers multiple functions of PUB13 in Arabidopsis immunity, flowering, and senescence. J. Exp. Bot. 66:3353–66
    [Google Scholar]
  159. 159.
    Zhou J, Zhang Y, Qi J, Chi Y, Fan B et al. 2014. E3 ubiquitin ligase CHIP and NBR1-mediated selective autophagy protect additively against proteotoxicity in plant stress responses. PLOS Genet. 10:e1004116Shows that CHIP cooperates with the autophagy receptor NBR1 to maintain proteostasis via distinct pathways.
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-102720-012310
Loading
/content/journals/10.1146/annurev-arplant-102720-012310
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
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