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The Function of Deubiquitinating Enzymes in Arabidopsis: Recent Progress of Ubiquitin-Specific Proteases (UBPs)

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Abstract

Compared to transcriptional regulation, post-translational modification is more efficient for eliciting rapid responses to external stimuli in plants. Ubiquitination, as a representative post-translational modification in eukaryotes, regulates the half-life and activity of target proteins. Although studies on the ubiquitination process have been intensively conducted, focusing on the function of E3 ubiquitin ligases, the deubiquitination process mediated by deubiquitinases (DUBs) remains relatively poorly understood. DUBs, which counteract the actions of E3 ubiquitin ligases, are categorized into five families based on their catalytic domains. Among DUB families, the ubiquitin-binding protease (UBP) is the largest in plants. The UBP family in Arabidopsis (AtUBP) comprises 27 members, many of which have been implicated in cellular events. In this study, we summarized the most recent knowledge related to the structure and biological functions of AtUBP members. A detailed understanding of their biological roles and modes of action will provide new insights into the mechanisms regulating protein stability and activity via ubiquitination/deubiquitination in Arabidopsis.

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References

  • Abdul Rehman SA, Kristariyanto YA, Choi SY, Nkosi PJ, Weidlich S, Labib K, Hofmann K, Kulathu Y (2016) MINDY-1 is a member of an evolutionarily conserved and structurally distinct new family of deubiquitinating enzymes. Mol Cell 63:146–155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Al Khateeb WM, Sher AA, Marcus JM, Schroeder DF (2019) UVSSA, UBP12, and RDO2/TFIIS contribute to Arabidopsis UV tolerance. Front Plant Sci 10:516

    Article  PubMed  PubMed Central  Google Scholar 

  • Al-Saharin R, Hellmann H, Mooney S (2022) Plant E3 ligases and their role in abiotic stress response. Cells 11:890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amerik AY, Hochstrasser M (2004) Mechanism and function of deubiquitinating enzymes. Biochim Biophys Acta Mol Cell Res 1695:189–207

    Article  CAS  Google Scholar 

  • An Z, Liu Y, Ou Y, Li J, Zhang B, Sun D, Sun Y, Tang W (2018) Regulation of the stability of RGF1 receptor by the ubiquitin-specific proteases UBP12/UBP13 is critical for root meristem maintenance. Proc Natl Acad Sci USA 115:1123–1128

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonnet J, Romier C, Tora L, Devys D (2008) Zinc-finger UBPs: regulators of deubiquitylation. Trends Biochem Sci 33:369–375

    Article  CAS  PubMed  Google Scholar 

  • Carroll EC, Marqusee S (2022) Site-specific ubiquitination: deconstructing the degradation tag. Curr Opin Struct Biol 73:102345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chandler JS, McArdle B, Callis J (1997) AtUBP3 and AtUBP4 are two closely related Arabidopsis thaliana ubiquitin-specific proteases present in the nucleus. Mol Gen Genet 255:302–310

    Article  CAS  PubMed  Google Scholar 

  • Cui X, Lu F, Li Y, Xue Y, Kang Y, Zhang S, Qiu Q, Cui X, Zheng S, Liu B, Xu X, Cao X (2013) Ubiquitin-specific proteases UBP12 and UBP13 act in circadian clock and photoperiodic flowering regulation in Arabidopsis. Plant Physiol 162:897–906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Derkacheva M, Liu S, Figueiredo DD, Gentry M, Mozgova I, Nanni P, Tang M, Mannervik M, Köhler C, Hennig L (2016) H2A deubiquitinases UBP12/13 are part of the Arabidopsis polycomb group protein system. Nat Plants 2:16126

    Article  CAS  PubMed  Google Scholar 

  • Doelling JH, Yan N, Kurepa J, Walker J, Vierstra RD (2001) The ubiquitin-specific protease UBP14 is essential for early embryo development in Arabidopsis thaliana. Plant J 27:393–405

    Article  CAS  PubMed  Google Scholar 

  • Doelling JH, Phillips AR, Soyler-Ogretim G, Wise J, Chandler J, Callis J, Otegui MS, Vierstra RD (2007) The ubiquitin-specific protease subfamily UBP3/UBP4 is essential for pollen development and transmission in Arabidopsis. Plant Physiol 145:801–813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du L, Li N, Chen L, Xu Y, Li Y, Zhang Y, Li C, Li Y (2014) The ubiquitin receptor DA1 regulates seed and organ size by modulating the stability of the ubiquitin-specific protease UBP15/SOD2 in Arabidopsis. Plant Cell 26:665–677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ewan R, Pangestuti R, Thornber S, Craig A, Carr C, O’Donnell L, Zhang C, Sadanandom A (2011) Deubiquitinating enzymes AtUBP12 and AtUBP13 and their tobacco homologue NtUBP12 are negative regulators of plant immunity. New Phytol 191:92–106

    Article  CAS  PubMed  Google Scholar 

  • Fu H, Lin YL, Fatimababy AS (2010) Proteasomal recognition of ubiquitylated substrates. Trends Plant Sci 15:375–386

    Article  CAS  PubMed  Google Scholar 

  • Husnjak K, Dikic I (2012) Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu Rev Biochem 81:291–322

    Article  CAS  PubMed  Google Scholar 

  • Jeong JS, Jung C, Seo JS, Kim JK, Chua NH (2017) The deubiquitinating enzymes UBP12 and UBP13 positively regulate MYC2 levels in jasmonate responses. Plant Cell 29:1406–1424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Komander D, Clague MJ, Urbé S (2009) Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol 10:550–563

    Article  CAS  PubMed  Google Scholar 

  • Kralemann LEM, Liu S, Trejo-Arellano MS, Muñoz-Viana R, Köhler C, Hennig L (2020) Removal of H2Aub1 by ubiquitin-specific proteases 12 and 13 is required for stable Polycomb-mediated gene repression in Arabidopsis. Genome Biol 21:144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwasna D, Abdul Rehman SA, Natarajan J, Matthews S, Madden R, De Cesare V, Weidlich S, Virdee S, Ahel I, Gibbs-Seymour I, Kulathu Y (2018) Discovery and characterization of ZUFSP/ZUP1, a distinct deubiquitinase class important for genome stability. Mol Cell 70:150-164.e6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee CM, Li MW, Feke A, Liu W, Saffer AM, Gendron JM (2019) GIGANTEA recruits the UBP12 and UBP13 deubiquitylases to regulate accumulation of the ZTL photoreceptor complex. Nat Commun 10:3750

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Li M, Chen D, Shiloh A, Luo J, Nikolaev AY, Qin J, Gu W (2002) Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 416:648–653

    Article  ADS  CAS  PubMed  Google Scholar 

  • Li Y, Zheng L, Corke F, Smith C, Bevan MW (2008) Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev 22:1331–1336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li WF, Perry PJ, Prafulla NN, Schmidt W (2010) Ubiquitin-specific protease 14 (UBP14) is involved in root responses to phosphate deficiency in Arabidopsis. Mol Plant 3:212–223

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Xia T, Gao F, Li Y (2020) Control of plant branching by the CUC2/CUC3-DA1-UBP15 regulatory module. Plant Cell 32:1919–1932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindbäck LN, Hu Y, Ackermann A, Artz O, Pedmale UV (2022) UBP12 and UBP13 deubiquitinases destabilize the CRY2 blue light receptor to regulate Arabidopsis growth. Curr Biol 32:3221-3231.e6

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Wang F, Zhang H, He H, Ma L, Deng XW (2008) Functional characterization of the Arabidopsis ubiquitin-specific protease gene family reveals specific role and redundancy of individual members in development. Plant J 55:844–856

    Article  CAS  PubMed  Google Scholar 

  • Liu G, Liang J, Lou L, Tian M, Zhang X, Liu L, Zhao Q, Xia R, Wu Y, Xie Q, Yu F (2022) The deubiquitinases UBP12 and UBP13 integrate with the E3 ubiquitin ligase XBAT35.2 to modulate VPS23A stability in ABA signaling. Sci Adv 8:eabl5765

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo M, Luo MZ, Buzas D, Finnegan J, Helliwell C, Dennis ES, Peacock WJ, Chaudhury A (2008) UBIQUITIN-SPECIFIC PROTEASE 26 is required for seed development and the repression of PHERES1 in Arabidopsis. Genetics 180:229–236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo Y, Takagi J, Claus LAN, Zhang C, Yasuda S, Hasegawa Y, Yamaguchi J, Shan L, Russinova E, Sato T (2022a) Deubiquitinating enzymes UBP12 and UBP13 stabilize the brassinosteroid receptor BRI1. EMBO Rep 23:e53354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo Y, Yasuda S, Takagi J, Hasegawa Y, Chiba Y, Yamaguchi J, Sato T (2022b) Deubiquitinating enzymes UBP12 and UBP13 regulate carbon/nitrogen-nutrient stress responses by interacting with the membrane-localized ubiquitin ligase ATL31 in Arabidopsis. Biochem Biophys Res Commun 636:55–61

    Article  CAS  PubMed  Google Scholar 

  • Majumdar P, Nath U (2020) De-ubiquitinases on the move: an emerging field in plant biology. Plant Biol 22:563–572

    Article  CAS  PubMed  Google Scholar 

  • March E, Farrona S (2018) Plant deubiquitinases and their role in the control of gene expression through modification of histones. Front Plant Sci 8:2274

    Article  PubMed  PubMed Central  Google Scholar 

  • Masselink H, Bernards R (2000) The adenovirus E1A binding protein BS69 is a corepressor of transcription through recruitment of N-CoR. Oncogene 19:1538–1546

    Article  CAS  PubMed  Google Scholar 

  • Miricescu A, Goslin K, Graciet E (2018) Ubiquitylation in plants: signaling hub for the integration of environmental signals. J Exp Bot 69:4511–4527

    Article  CAS  PubMed  Google Scholar 

  • Moon BC, Choi MS, Kang YH, Kim MC, Cheong MS, Park CY, Yoo JH, Koo SC, Lee SM, Lim CO, Cho MJ, Chung WS (2005) Arabidopsis ubiquitin-specific protease 6 (AtUBP6) interacts with calmodulin. FEBS Lett 579:3885–3890

    Article  CAS  PubMed  Google Scholar 

  • Nassrallah A, Rougée M, Bourbousse C, Drevensek S, Fonseca S, Iniesto E, Ait-Mohamed O, Deton-Cabanillas AF, Zabulon G, Ahmed I, Stroebel D, Masson V, Lombard B, Eeckhout D, Gevaert K, Loew D, Genovesio A, Breyton C, De Jaeger G, Bowler C, Rubio V, Barneche F (2018) DET1-mediated degradation of a SAGA-like deubiquitination module controls H2Bub homeostasis. Elife 7:e37892

    Article  PubMed  PubMed Central  Google Scholar 

  • Neutzner M, Neutzner A (2012) Enzymes of ubiquitination and deubiquitination. Essays Biochem 52:37–50

    Article  CAS  PubMed  Google Scholar 

  • Ohtake F, Saeki Y, Ishido S, Kanno J, Tanaka K (2016) The K48–K63 branched ubiquitin chain regulates NF-κB signaling. Mol Cell 64:251–266

    Article  CAS  PubMed  Google Scholar 

  • Pan R, Kaur N, Hu J (2014) The Arabidopsis mitochondrial membrane-bound ubiquitin protease UBP27 contributes to mitochondrial morphogenesis. Plant J 78:1047–1059

    Article  CAS  PubMed  Google Scholar 

  • Park SH, Jeong JS, Seo JS, Park BS, Chua NH (2019) Arabidopsis ubiquitin-specific proteases UBP12 and UBP13 shape ORE1 levels during leaf senescence induced by nitrogen deficiency. New Phytol 223:1447–1460

    Article  CAS  PubMed  Google Scholar 

  • Park SH, Jeong JS, Zhou Y, Binte Mustafa NF, Chua NH (2022) Deubiquitination of BES1 by UBP12/UBP13 promotes brassinosteroid signaling and plant growth. Plant Commun 3:100348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romero-Barrios N, Vert G (2018) Proteasome-independent functions of lysine-63 polyubiquitination in plants. New Phytol 217:995–1011

    Article  PubMed  Google Scholar 

  • Scaglione KM, Basrur V, Ashraf NS, Konen JR, Elenitoba-Johnson KS, Todi SV, Paulson HL (2013) The ubiquitin-conjugating enzyme (E2) Ube2w ubiquitinates the N terminus of substrates. J Biol Chem 288:18784–18788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmitz RJ, Tamada Y, Doyle MR, Zhang X, Amasino RM (2009) Histone H2B deubiquitination is required for transcriptional activation of FLOWERING LOCUS C and for proper control of flowering in Arabidopsis. Plant Physiol 149:1196–1204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seo KI, Song E, Chung S, Lee JH (2012) Roles of various cullin-RING E3 ligases involved in hormonal and stress responses in plants. J Plant Biol 55:421–428

    Article  CAS  Google Scholar 

  • Skelly MJ (2022) The emerging roles of deubiquitinases in plant proteostasis. Essays Biochem 66:147–154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skelly MJ, Furniss JJ, Grey H, Wong KW, Spoel SH (2019) Dynamic ubiquitination determines transcriptional activity of the plant immune coactivator NPR1. Elife 8:e47005

    Article  PubMed  PubMed Central  Google Scholar 

  • Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Physiol Plant Mol Biol 55:555–590

    Article  CAS  Google Scholar 

  • Sridhar VV, Kapoor A, Zhang K, Zhu J, Zhou T, Hasegawa PM, Bressan RA, Zhu JK (2007) Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature 447:735–738

    Article  ADS  CAS  PubMed  Google Scholar 

  • Tracz M, Bialek W (2021) Beyond K48 and K63: non-canonical protein ubiquitination. Cell Mol Biol Lett 26:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Biol 10:385–397

    Article  CAS  PubMed  Google Scholar 

  • Woo OG, Kim H, Lee JH (2021) Current understanding of the CRL1 complex in Arabidopsis. J Plant Biol 64:1–12

    Article  CAS  Google Scholar 

  • Wu R, Zheng W, Tan J, Sammer R, Du L, Lu C (2019) Protein partners of plant ubiquitin-specific proteases (UBPs). Plant Physiol Biochem 145:227–236

    Article  PubMed  Google Scholar 

  • Wu X, Cai X, Zhang B, Wu S, Wang R, Li N, Li Y, Sun Y, Tang W (2022) ERECTA regulates seed size independently of its intracellular domain via MAPK-DA1-UBP15 signaling. Plant Cell 34:3773–3789

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie DL, Huang HM, Zhou CY, Liu CX, Kanwar MK, Qi ZY, Zhou J (2022) HsfA1a confers pollen thermotolerance through upregulating antioxidant capacity, protein repair, and degradation in Solanum lycopersicum L. Hortic Res 9:uhac163

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiong J, Yang F, Yao X, Zhao Y, Wen Y, Lin H, Guo H, Yin Y, Zhang D (2022) The deubiquitinating enzymes UBP12 and UBP13 positively regulate recovery after carbon starvation by modulating BES1 stability in Arabidopsis thaliana. Plant Cell 34:4516–4530

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Jin W, Li N, Zhang W, Liu C, Li C, Li Y (2016) Ubiquitin-specific protease14 interacts with ultraviolet-B insensitive4 to regulate endoreduplication and cell and organ growth in Arabidopsis. Plant Cell 28:1200–1214

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yan N, Doelling JH, Falbel TG, Durski AM, Vierstra RD (2000) The ubiquitin-specific protease family from Arabidopsis. AtUBP1 and 2 are required for the resistance to the amino acid analog canavanine. Plant Physiol 124:1828–1843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Zhou H, Zhang M, Gao Y, Li L, Gao Y, Li M, Yang Y, Guo Y, Li X (2016) Ubiquitin-specific protease 24 negatively regulates abscisic acid signalling in Arabidopsis thaliana. Plant Cell Environ 39:427–440

    Article  CAS  PubMed  Google Scholar 

  • Zhou H, Zhao J, Yang Y, Chen C, Liu Y, Jin X, Chen L, Li X, Deng XW, Schumaker KS, Guo Y (2012) Ubiquitin-specific protease16 modulates salt tolerance in Arabidopsis by regulating Na+/H+ antiport activity and serine hydroxymethyltransferase stability. Plant Cell 24:5106–5122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Y, Park SH, Soh MY, Chua NH (2021) Ubiquitin-specific proteases UBP12 and UBP13 promote shade avoidance response by enhancing PIF7 stability. Proc Natl Acad Sci U S A 118:e2103633118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou H, Zhao J, Cai J, Patil SB (2017) UBIQUITIN-SPECIFIC PROTEASES function in plant development and stress responses. Plant Mol Biol 94:565–576

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Park SH, Chua NH (2023) UBP12/UBP13-mediated deubiquitination of salicylic acid receptor NPR3 suppresses plant immunity. Mol Plant 16:232–244

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by a 2 years Research Grant of Pusan National University (J-H Lee).

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Authors and Affiliations

  1. Underwood International College, Yonsei University, Seoul, 03722, Korea

    Sunglan Chung

  2. Department of Biology Education, Pusan National University, Busan, 46241, Korea

    Hye-Lim Kwon & Jae-Hoon Lee

  3. Department of Biological Sciences, Konkuk University, Seoul, 05029, Korea

    Hye Sup Yun

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  1. Sunglan Chung
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  2. Hye-Lim Kwon
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  4. Jae-Hoon Lee
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JHL conceived the study. SC and JHL wrote the manuscript with contributions of authors HLK and HSY. All authors have approved the manuscript and declare no conflicts of interest.

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Correspondence to Jae-Hoon Lee.

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Chung, S., Kwon, HL., Yun, H.S. et al. The Function of Deubiquitinating Enzymes in Arabidopsis: Recent Progress of Ubiquitin-Specific Proteases (UBPs). J. Plant Biol. 67, 1–9 (2024). https://doi.org/10.1007/s12374-023-09408-2

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