Skip to main content
Log in

Roles of various cullin-RING E3 ligases involved in hormonal and stress responses in plants

  • Review Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Post-translational modification plays an important role in the regulation of protein stability, enzyme activity, and the cellular localization of proteins. Ubiquitination is a representative post-translational modification in eukaryotes that is mainly responsible for protein degradation. There have been a number of reports on the role of ubiquitination in various cellular responses in plants, such as regulation of the cell division cycle, stress responses and hormonal signaling. Among the three types of ubiquitination-related enzymes, E3 ubiquitin ligase is critical in determining substrate specificity. The importance of cullin-RING E3 ligase (CRL), a type of E3 ligase, has been emphasized during the recent decade due to its large number and its involvement in various plant cellular processes. Here, we describe how CRL E3 ligase complexes are involved in cellular events mediated by plant hormones and during plant stress adaptation while focusing on their substrate receptors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of Arabidopsis MYC and MYB homologs in drought- and abscisic-acid-regulated gene expression. Plant Cell 9:1859–1868

    PubMed  CAS  Google Scholar 

  • Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274

    Article  PubMed  CAS  Google Scholar 

  • Ariizumi T, Lawrence PK, Steber CM (2011) The role of two f-box proteins, SLEEPY1 and SNEEZY, in Arabidopsis gibberellin signaling. Plant Physiol 155:765–775

    Article  PubMed  CAS  Google Scholar 

  • Barlow PN, Luisi B, Milner A, Elliott M, Everett R (1994) Structure of the C3HC4 domain by 1H-nuclear magnetic resonance spectroscopy: a new structural class of zinc-finger. J Mol Biol 237:201–211

    Article  PubMed  CAS  Google Scholar 

  • Biedermann S, Hellmann H (2010) The DDB1a interacting proteins ATCSA-1 and DDB2 are critical factors for UV-B tolerance and genomic integrity in Arabidopsis thaliana. Plant J 62:404–415

    Article  PubMed  CAS  Google Scholar 

  • Cao Y, Yang Y, Zhang H, Li D, Zheng Z, Song F (2008) Overexpression of a rice defense-related F-box protein gene OsDRF1 in tobacco improves disease resistance through potentiation of defense gene expression. Physiol Plant 134:440–452

    Article  PubMed  CAS  Google Scholar 

  • Chen H, Shen Y, Tang X, Yu L, Wang J, Guo L, Zhang Y, Zhang H, Feng S, Strickland E, Zheng N, Deng XW (2006) Arabidopsis CULLIN4 forms an E3 ubiquitin ligase with RBX1 and the CDD complex in mediating light control of development. Plant Cell 18:1991–2004

    Article  PubMed  CAS  Google Scholar 

  • Christians MJ, Gingerich DJ, Hansen M, Binder BM, Kieber JJ, Vierstra RD (2009) The BTB ubiquitin ligases ETO1, EOL1 and EOL2 act collectively to regulate ethylene biosynthesis in Arabidopsis by controlling type-2 ACC synthase levels. Plant J 57:332–345

    Article  PubMed  CAS  Google Scholar 

  • Craig A, Ewan R, Mesmar J, Gudipati V, Sadanandom A (2009) E3 ubiquitin ligases and plant innate immunity. J Exp Bot 60:1123–1132

    Article  PubMed  CAS  Google Scholar 

  • del Pozo JC, Diaz-Trivino S, Cisneros N, Gutierrez C (2006) The balance between cell division and endoreplication depends on E2FC-DPB, transcription factors regulated by the ubiquitin-SCFSKP2A pathway in Arabidopsis. Plant Cell 18:2224–2235

    Article  PubMed  Google Scholar 

  • Deveraux Q, Ustrell V, Pickart C, Rechsteiner MA (1994) 26S protease subunit that binds ubiquitin conjugates. J Biol Chem 269:7059–7061

    PubMed  CAS  Google Scholar 

  • Deshaies RJ, Joazeiro CA (2009) RING domain E3 ubiquitin ligases. Annu Rev Biochem 78:399–434

    Article  PubMed  CAS  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    Article  PubMed  CAS  Google Scholar 

  • Dill A, Thomas SG, Hu JH, Steber CM, Suna TP (2004) The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell 16:1392–1405

    Article  PubMed  CAS  Google Scholar 

  • Downes BP, Stupar RM, Gingerich DJ, Vierstra RD (2003) HECT ubiquitin-protein ligase (UPL) family in Arabidopsis: UPL3 has a specific role in trichome development. Plant J 35:729–742

    Article  PubMed  CAS  Google Scholar 

  • Farmer LM, Book AJ, Lee KH, Lin YL, Fu H, Vierstra RD (2010) The RAD23 family provides an essential connection between the 26S proteasome and ubiquitylated proteins in Arabidopsis. Plant Cell 22:124–142

    Article  PubMed  CAS  Google Scholar 

  • Feng S, Ma L, Wang X, Xie D, Dinesh-Kumar SP, Wei N, Deng XW (2003) The COP9 signalosome interacts physically with SCFCOI1 and modulates jasmonate responses. Plant Cell 15:1083–1094

    Article  PubMed  CAS  Google Scholar 

  • Feng S, Shen Y, Sullivan JA, Rubio V, Xiong Y, Sun TP, Deng XW (2004) Arabidopsis CAND1, an unmodified CUL1-interacting protein, is involved in multiple developmental pathways controlled by ubiquitin/proteasome-mediated protein degradation. Plant Cell 16:1870–1882

    Article  PubMed  CAS  Google Scholar 

  • Finley D (2009) Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem 78:477–513

    Article  PubMed  CAS  Google Scholar 

  • Funakoshi M, Sasaki T, Nishimoto T, Kobayashi H (2002) Budding yeast Dsk2p is a polyubiquitin-binding protein that can interact with the proteasome. Proc Natl Acad Sci USA 99:745–750

    Article  PubMed  CAS  Google Scholar 

  • Gabriely G, Kama R, Gelin-Licht R, Gerst JE (2008) Different domains of the UBL-UBA ubiquitin receptor, Ddi1/Vsm1, are involved in its multiple cellular roles. Mol Biol Cell 19:3625–3637

    Article  PubMed  CAS  Google Scholar 

  • Greenham K, Santner A, Castillejo C, Mooney S, Sairanen I, Ljung K, Estelle M (2011) The AFB4 auxin receptor is a negative regulator of auxin signaling in seedlings. Curr Biol 21:520–525

    Article  PubMed  CAS  Google Scholar 

  • Gruber H, Heijde M, Heller W, Albert A, Seidlitz HK, Ulm R (2010) Negative feedback regulation of UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. Proc Natl Acad Sci USA 107:20132–20137

    Article  PubMed  CAS  Google Scholar 

  • Gou M, Su N, Zheng J, Huai J, Wu G, Zhao J, He J, Tang D, Yang S, Wang G (2009) An F-box gene, CPR30, functions as a negative regulator of the defense response in Arabidopsis. Plant J 60:757–770

    Article  PubMed  CAS  Google Scholar 

  • Guo H, Ecker JR (2003) Plant responses to ethylene gas are mediated by SCFEBF1/EBF2-dependent proteolysis of EIN3 transcription factor. Cell 115:667–677

    Article  PubMed  CAS  Google Scholar 

  • Haglund K, Di Fiore PP, Dikic I (2003) Distinct monoubiquitin signals in receptor endocytosis. Trends Biochem Sci 28:598–603

    Article  PubMed  CAS  Google Scholar 

  • Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–479

    Article  PubMed  CAS  Google Scholar 

  • Hotton SK, Callis J (2008) Regulation of cullin RING ligases. Annu Rev Plant Biol 59:467–489

    Article  PubMed  CAS  Google Scholar 

  • Huang TT, D’Andrea AD (2006) Regulation of DNA repair by ubiquitylation. Nat Rev Mol Cell Biol 7:323–334

    Article  PubMed  CAS  Google Scholar 

  • Husnjak K, Elsasser S, Zhang N, Chen X, Randles L, Shi Y, Hofmann K, Walters KJ, Finley D, Dikic I (2008) Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453:481–488

    Article  PubMed  CAS  Google Scholar 

  • Itoh H, Matsuoka M, Steber CM (2003) A role for the ubiquitin-26S proteasome pathway in gibberellin signaling. Trends Plant Sci 8:492–497

    Article  PubMed  CAS  Google Scholar 

  • Jurado S, Abraham Z, Manzano C, Lopez-Torrejon G, Pacios LF, Del Pozo JC (2010) The Arabidopsis cell cycle F-box protein SKP2A binds to auxin. Plant Cell 22:3891–3904

    Article  PubMed  CAS  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451

    Article  PubMed  CAS  Google Scholar 

  • Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D’Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50:347–363

    Article  PubMed  CAS  Google Scholar 

  • Kim HS, Delaney TP (2002) Arabidopsis SON1 is an F-box protein that regulates a novel induced defense response independent of both salicylic acid and systemic acquired resistance. Plant Cell 14:1469–1482

    Article  PubMed  CAS  Google Scholar 

  • Kim S, Choi HI, Ryu HJ, Park JH, Kim MD, Kim SY (2004) ARIA, an Arabidopsis arm repeat protein interacting with a transcriptional regulator of abscisic acid-responsive gene expression, is a novel abscisic acid signaling component. Plant Physiol 136:3639–3648

    Article  PubMed  CAS  Google Scholar 

  • Koops P, Pelser S, Ignatz M, Klose C, Marrocco-Selden K, Kretsch T (2011) EDL3 is an F-box protein involved in the regulation of abscisic acid signalling in Arabidopsis thaliana. J Exp Bot 62:5547–5560

    Article  PubMed  CAS  Google Scholar 

  • Kraft E, Stone SL, Ma L, Su N, Gao Y, Lau OS, Deng XW, Callis J (2005) Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis. Plant Physiol 139:1597–1611

    Article  PubMed  CAS  Google Scholar 

  • Lambertson D, Chen L, Madura K (1999) Pleiotropic defects caused by loss of the proteasome-interacting factors Rad23 and Rpn10 of Saccharomyces cerevisiae. Genetics 153:69–79

    PubMed  CAS  Google Scholar 

  • Lechner E, Leonhardt N, Eisler H, Parmentier Y, Alioua M, Jacquet H, Leung J, Genschik P (2011) MATH/BTB CRL3 receptors target the homeodomain-leucine zipper ATHB6 to modulate abscisic acid signaling. Dev Cell 21:1116–1128

    Article  PubMed  CAS  Google Scholar 

  • Lee JH, Terzaghi W, Deng XW (2011) DWA3, an Arabidopsis DWD protein, acts as a negative regulator in ABA signal transduction. Plant Sci 180:352–357

    Article  PubMed  CAS  Google Scholar 

  • Lee JH, Terzaghi W, Gusmaroli G, Charron JB, Yoon HJ, Chen H, He YJ, Xiong Y, Deng XW (2008) Characterization of Arabidopsis and rice DWD proteins and their roles as substrate receptors for CUL4-RING E3 ubiquitin ligases. Plant Cell 20:152–167

    Article  PubMed  CAS  Google Scholar 

  • Lee JH, Yoon HJ, Terzaghi W, Martinez C, Dai M, Li J, Byun MO, Deng XW (2010) DWA1 and DWA2, two Arabidopsis DWD protein components of CUL4-based E3 ligases, act together as negative regulators in ABA signal transduction. Plant Cell 22:1716–1732

    Article  PubMed  CAS  Google Scholar 

  • Lyapina S, Cope G, Shevchenko A, Serino G, Tsuge T, Zhou C, Wolf DA, Wei N, Shevchenko A, Deshaies RJ (2001) Promotion of NEDD-CUL1 conjugate cleavage by COP9 signalosome. Science 292:1382–1385

    Article  PubMed  CAS  Google Scholar 

  • Mandadi KK, Misra A, Ren S, McKnight TD (2009) BT2, a BTB protein, mediates multiple responses to nutrients, stresses, and hormones in Arabidopsis. Plant Physiol 150:1930–1939

    Article  PubMed  CAS  Google Scholar 

  • Marrocco K, Zhou Y, Bury E, Dieterle M, Funk M, Genschik P, Krenz M, Stolpe T, Kretsch T (2006) Functional analysis of EID1, an F-box protein involved in phytochrome A-dependent light signal transduction. Plant J 45:423–438

    Article  PubMed  CAS  Google Scholar 

  • McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun TP, Steber CM (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15:1120–1130

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Hasegawa PM (2010) Sumoylation and other ubiquitin-like post-translational modifications in plants. Trends Cell Biol 20:223–232

    Article  PubMed  CAS  Google Scholar 

  • Mukhopadhyay D, Riezman H (2007) Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315:201–205

    Article  PubMed  CAS  Google Scholar 

  • Olzman JA, Chin LS (2008) Parkin-mediated K63-linked polyubiquitination: a signal for targeting misfolded proteins to the aggresomeautophagy pathway. Autophagy 4:85–87

    Google Scholar 

  • Parry G, Calderon-Villalobos LI, Prigge M, Peret B, Dharmasiri S, Itoh H, Lechner E, Gray WM, Bennett M, Estelle M (2009) Complex regulation of the TIR1/AFB family of auxin receptors. Proc Natl Acad Sci USA 106:22540–22545

    Article  PubMed  CAS  Google Scholar 

  • Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W, Pérez AC, Chico JM, Bossche RV, Sewell J, Gil E, García-Casado G, Witters E, Inzé D, Long JA, De Jaeger G, Solano R, Goossens A (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464:788–791

    Article  PubMed  CAS  Google Scholar 

  • Peng J, Yu D, Wang L, Xie M, Yuan C, Wang Y, Tang D, Zhao X, Liu X (2012) Arabidopsis F-box gene FOA1 involved in ABA signaling. Sci China Life Sci 55:497–506

    Article  PubMed  CAS  Google Scholar 

  • Petroski MD, Deshaies RJ (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6:9–20

    Article  PubMed  CAS  Google Scholar 

  • Piper RC, Lehner P (2011) Endosomal transportation via ubiquitination. Trends Cell Biol 21:647–655

    Article  PubMed  CAS  Google Scholar 

  • Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, Koncz C, Genschik P (2003) EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell 115:679–689

    Article  PubMed  CAS  Google Scholar 

  • Qiao H, Chang KN, Yazaki J, Ecker JR (2009) Interplay between ethylene, ETP1/ETP2 F-box proteins, and degradation of EIN2 triggers ethylene responses in Arabidopsis. Genes Dev 23:512–521

    Article  PubMed  CAS  Google Scholar 

  • Salmena L, Pandolfi PP (2007) Changing venues for tumour suppression: balancing destruction and localization by monoubiquitylation. Nat Rev Cancer 7:409–413

    Article  PubMed  CAS  Google Scholar 

  • Schwechheimer C, Serino G, Callis J, Crosby WL, Lyapina S, Deshaies RJ, Gray WM, Estelle M, Deng XW (2001) Interactions of the COP9 signalosome with the E3 ubiquitin ligase SCFTIR1 in mediating auxin response. Science 292:1379–1382

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Strader LC, Ritchie S, Soule JD, McGinnis KM, Steber CM (2004) Recessive-interfering mutations in the gibberellin signaling gene SLEEPY1 are rescued by overexpression of its homologue, SNEEZY. Proc Natl Acad Sci USA 101:12771–12776

    Article  PubMed  CAS  Google Scholar 

  • Thomann A, Brukhin V, Dieterle M, Gheyeselinck J, Vantard M, Grossniklaus U, Genschik P (2005) Arabidopsis CUL3A and CUL3B genes are essential for normal embryogenesis. Plant J 43:437–448

    Article  PubMed  CAS  Google Scholar 

  • Thomas SG, Sun TP (2004) Update on gibberellin signaling. A tale of the tall and the short. Plant Physiol 135:668–676

    Article  PubMed  CAS  Google Scholar 

  • Thrower JS, Hoffman L, Rechsteiner M, Pickart CM (2000) Recognition of the polyubiquitin proteolytic signal. EMBO J 19:94–102

    Article  PubMed  CAS  Google Scholar 

  • Ulrich HD (2005) Mutual interactions between the SUMO and ubiquitin systems: a plea of no contest. Trends Cell Biol 15:525–532

    Article  PubMed  CAS  Google Scholar 

  • Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcriptional transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637

    Article  PubMed  CAS  Google Scholar 

  • Verger A, Perdomo J, Crossley M (2003) Modification with SUMO. A role in transcriptional regulation. EMBO Rep 4:137–142

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Wang KL, Yoshida H, Lurin C, Ecker JR (2004) Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature 428:945–950

    Article  PubMed  CAS  Google Scholar 

  • Xiao S, Dai L, Liu F, Wang Z, Peng W, Xie D (2004) COS1: an Arabidopsis coronatine insensitive1 suppressor essential for regulation of jasmonate-mediated plant defense and senescence. Plant Cell 16:1132–1142

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Xu L, Liu F, Lechner E, Genschik P, Crosby WL, Ma H, Peng W, Huang D, Xie D (2002) The SCFCOI1 ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14:1919–1935

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94

    Article  PubMed  CAS  Google Scholar 

  • Yan J, Zhang C, Gu M, Bai Z, Zhang W, Qi T, Cheng Z, Peng W, Luo H, Nan F, Wang Z, Xie D (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21:2220–2236

    Article  PubMed  CAS  Google Scholar 

  • Yee D, Goring DR (2009) The diversity of plant U-box E3 ubiquitin ligases: from upstream activators to downstream target substrates. J Exp Bot 60:1109–1121

    Article  PubMed  CAS  Google Scholar 

  • Yu H, Wu J, Xu N, Peng M (2007) Roles of F-box proteins in plant hormone responses. Acta Biochim Biophys Sin (Shanghai) 39:915–922

    Article  CAS  Google Scholar 

  • Zeng LR, Park CH, Venu RC, Gough J, Wang GL (2008) Classification, expression pattern, and E3 ligase activity assay of rice U-boxcontaining proteins. Mol Plant 1:800–815

    Article  PubMed  CAS  Google Scholar 

  • Zhang C, Guo H, Zhang J, Guo G, Schumaker KS, Guo Y (2010) Arabidopsis cockayne syndrome A-like proteins 1A and 1B form a complex with CULLIN4 and damage DNA binding protein 1A and regulate the response to UV irradiation. Plant Cell 22:2353–2369

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Xu W, Li Z, Deng XW, Wu W, Xue Y (2008) F-box protein DOR functions as a novel inhibitory factor for abscisic acid-induced stomatal closure under drought stress in Arabidopsis. Plant Physiol 148:2121–2133

    Article  PubMed  CAS  Google Scholar 

  • Zheng X, Miller ND, Lewis DR, Christians MJ, Lee KH, Muday GK, Spalding EP, Vierstra RD (2011) AUXIN UP-REGULATED FBOX PROTEIN1 regulates the cross talk between auxin transport and cytokinin signaling during plant root growth. Plant Physiol 156:1878–1893

    Article  PubMed  CAS  Google Scholar 

  • Zheng N, Schulman BA, Song L, Miller JJ, Jeffrey PD, Wang P, Chu C, Koepp DM, Elledge SJ, Pagano M, Conaway RC, Conaway JW, Harper JW, Pavletich NP (2002) Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex. Nature 416:703–709

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jae-Hoon Lee.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Seo, KI., Song, E., Chung, S. et al. Roles of various cullin-RING E3 ligases involved in hormonal and stress responses in plants. J. Plant Biol. 55, 421–428 (2012). https://doi.org/10.1007/s12374-012-0902-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-012-0902-4

Keywords

Navigation