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UBIQUITIN-SPECIFIC PROTEASES function in plant development and stress responses

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UBIQUITIN-SPECIFIC PROTEASES play important roles in plant development and stress responses.

Abstract

Protein ubiquitination and deubiquitination are reversible processes, which can modulate the stability, activity as well as subcellular localization of the substrate proteins. UBIQUITIN-SPECIFIC PROTEASE (UBP) protein family participates in protein deubiquitination. Members of UBP family are involved in a variety of physiological processes in plants, as evidenced by their functional characterization in model plant Arabidopsis and other plants. UBPs are conserved in plants and distinct UBPs function in different regulatory processes, although functional redundancies exist between some members. Here we briefly reviewed recent advances in understanding the biological functions of UBP protein family in Arabidopsis, particularly the molecular mechanisms by which UBPs regulate plant development and stress responses. We believe that elucidation of UBPs function and regulation in Arabidopsis will provide new insights about protein deubiquitination and might shed light on the understanding of the mechanistic roles of UBPs in general, which will definitely contribute to crop improvement in agriculture.

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References

  • Amerik AY, Hochstrasser M (2004) Mechanism and function of deubiquitinating enzymes. BBA 1695:189–207

    CAS  PubMed  Google Scholar 

  • Aung K, Hu J (2012) Differential roles of Arabidopsis dynamin-related proteins DRP3A, DRP3B, and DRP5B in organelle division. J Integr Plant Biol 54:921–931

    CAS  PubMed  Google Scholar 

  • Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19:90–98

    Article  CAS  PubMed  Google Scholar 

  • Barberon M, Zelazny E, Robert S et al (2011) Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants. Proc Natl Acad Sci USA 108:E450–E458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bartel B, Citovsky V (2012) Focus on ubiquitin in plant biology. Plant Physiol 160:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berger F, Grini PE, Schnittger A (2006) Endosperm: an integrator of seed growth and development. Curr Opin Plant Biol 9:664–670

    Article  CAS  PubMed  Google Scholar 

  • Bernhardt C, Zhao M, Gonzalez A et al (2005) The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis. Development 132(2):291–298

    Article  CAS  PubMed  Google Scholar 

  • Bonnet JP, Romier C, Tora L et al (2008) Zinc-finger UBPs: regulators of deubiquitylation. Trend Biochem Sci 33:369–375

    Article  CAS  PubMed  Google Scholar 

  • Cao Y, Dai Y, Cui S et al (2008) Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. Plant Cell 20:2586–2602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Capron A, Okresz L, Genschik P (2003) First glance at the plant APC/C, a highly conserved ubiquitin-protein ligase. Trends Plant Sci 8:83–89

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Chen ZJ, Sun LJ (2009) Nonproteolytic functions of ubiquitin in cell signaling. Mol Cell 33:275–286

    Article  CAS  PubMed  Google Scholar 

  • Cui X, Lu F, Li Y et al (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 

  • Cutler SR, Rodriguez PL, Finkelstein RR et al (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Article  CAS  PubMed  Google Scholar 

  • Dangl J, Jones J (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    Article  CAS  PubMed  Google Scholar 

  • Edgar B, Zielke N, Gutierrez C (2014) Endocycles: a recurrent evolutionary innovation for post-mitotic cell growth. Nat Rev Mol Cell Biol 15:197–210

    Article  PubMed  CAS  Google Scholar 

  • De Gara L, Locato V, Dipierro S et al (2010) Redox homeostasis in plants. The challenge of living with endogenous oxygen production. Respir Physiol Neurobiol 173:S13–S19

    Article  PubMed  CAS  Google Scholar 

  • Derkacheva M, Liu S, Figueiredo D et al (2016) H2A deubiquitinases UBP12/13 are part of the Arabidopsis Polycomb group protein system. Nat Plant 2:16126

    Article  CAS  Google Scholar 

  • Doelling J, Yan N, Kurepa J et al (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 J, Phillips A, Soyler-Ogretim G et al (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 

  • Dreher K, Callis J (2007) Ubiquitin, hormones and biotic stress in plants. Annu Bot 99:787–822

    Article  CAS  Google Scholar 

  • Du L, Li N, Chen L et al (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 et al (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 

  • Filimonenko M, Stuffers S, Raiborg C, Yamamoto A et al (2007) Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. J Cell Biol 179:485–500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischer J (2003) Deubiquitinating enzymes: their roles in development, differentiation, and disease. Int Rev Cytol 229:43–72

    Article  CAS  PubMed  Google Scholar 

  • Friedman JR, Nunnari J (2014) Mitochondrial form and function. Nature 505:335–343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gegas VC, Nazari A, Griffiths S et al (2010) A genetic framework for grain size and shape variation in wheat. Plant Cell 22:1046–1056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilroy S, Jones DL (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci 5:56–60

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez N, De Bodt S, Sulpice R et al (2010) Increased leaf size: different means to an end. Plant Physiol 153:1261–1279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haglund K, Dikic I (2005) Ubiquitylation and cell signaling. EMBO J 24:3353–3359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harmer SL (2009) The circadian system in higher plants. Annu Rev Plant Biol 60:357–377

    Article  CAS  PubMed  Google Scholar 

  • Hase Y, Trung K, Matsunaga T et al (2006) A mutation in the uvi4 gene promotes progression of endo-reduplication and confers increased tolerance towards ultraviolet B light. Plant J 46:317–326

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa P (2013) Sodium (Na+) homeostasis and salt tolerance of plants. Environ Exp Bot 92:19–31

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hepler P, Vidali L, Cheung A (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 17:159–187

    Article  CAS  PubMed  Google Scholar 

  • Hepler PK, Kunkel JG, Rounds CM et al (2012) Calcium entry into pollen tubes. Trends Plant Sci 17:32–38

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Heyman J, De Veylder L (2012) The anaphase-promoting complex/cyclosome in control of plant development. Mol Plant 5:1182–1194

    Article  CAS  PubMed  Google Scholar 

  • Higashiyama T, Takeuchi H (2015) The mechanism and key molecules involved in pollen tube guidance. Annu Rev Plant Biol 66:393–413

    Article  CAS  PubMed  Google Scholar 

  • Hochstrasser M (1996) Ubiquitin-dependent protein degradation. Annu Rev Genet 30:405–439

    Article  CAS  PubMed  Google Scholar 

  • Hu M, Li P, Li M et al (2002) Crystal structure of a UBP-family deubiquitinating enzyme in isolation and in complex with ubiquitin aldehyde. Cell 111:1041–1054

    Article  CAS  PubMed  Google Scholar 

  • Huang OW, Cochran AG (2013) Regulation of deubiquitinase proteolytic activity. Curr Opin Struct Biol 23:806–811

    Article  CAS  PubMed  Google Scholar 

  • Ishida T, Kurata T, Okada K et al (2008) A genetic regulatory network in the development of trichomes and root hairs. Annu Rev Plant Biol 59(1):365–386

    Article  CAS  PubMed  Google Scholar 

  • Isono E, Nagel M (2014) Deubiquitylating enzymes and their emerging role in plant biology. Front Plant Sci 5:56

    Article  PubMed  PubMed Central  Google Scholar 

  • Jamai A, Salome P, Schilling S et al (2009) Arabidopsis photorespiratory serine hydroxymethyltransferase activity requires the mitochondrial accumulation of ferredoxin-dependent glutamate synthase. Plant Cell 21:595–606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung C, Muller AE (2009) Flowering time control and applications in plant breeding. Trends Plant Sci 14:563–573

    Article  CAS  PubMed  Google Scholar 

  • Kanaoka MM, Higashiyama T (2015) Peptide signaling in pollen tube guidance. Curr Opin Plant Biol 28:127–136

    Article  CAS  PubMed  Google Scholar 

  • Katsiarimpa A, Kalinowska K, Anzenberger F et al (2013) The deubiquitinating enzyme AMSH1 and the ESCRT-III subunit VPS2.1 are required for autophagic degradation in Arabidopsis. Plant Cell 25:2236–2252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kerscher O, Felberbaum R, Hochstrasser M (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22:159–180

    Article  CAS  PubMed  Google Scholar 

  • Kwak S, Schiefelbein J (2007) The role of the SCRAMBLED receptor-like kinase in patterning the Arabidopsis root epidermis. Dev Biol 302:118–131

    Article  CAS  PubMed  Google Scholar 

  • Lafonplacette C, Kohler C (2014) Embryo and endosperm, partners in seed development. Curr Opin Plant Biol 17:64–69

    Article  Google Scholar 

  • Larson-Rabin Z, Li Z, Masson P et al (2009) FZR2/CCS52A1 expression is a determinant of endoreduplication and cell expansion in Arabidopsis. Plant Physiol 149:874–884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee HK, Cho SK, Son O, Xu Z, Hwang I et al (2009) Drought stress-induced Rma1H1, a RING membrane-anchor E3 ubiquitin ligase homolog, regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants. Plant Cell 21:622–641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leishman M, Westoby M (1994) The role of seed size in seedling establishment in dry soil-conditions: experimental-evidence from semiarid species. J Ecol 82:249–258

    Article  Google Scholar 

  • Leitner J, Petrasek J, Tomanov K et al (2012) Lysine63-linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth. Proc Natl Acad Sci USA 109:8322–8327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Zheng L, Corke F et al (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 et al (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 

  • Lim K, Lim GG (2011) K63-linked ubiquitination and neurodegeneration. Neurobiol Dis 43:9–16

    Article  CAS  PubMed  Google Scholar 

  • Linkies A, Graeber K, Knight CA et al (2010) The evolution of seeds. New Phytol 186:817–831

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Wang F, Zhang H et al (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 L, Cui F, Li Q, Yin B et al (2011) The endoplasmic reticulum-associated degradation is necessary for plant salt tolerance. Cell Res 21:957–969

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Bucio J, Cruz-Ramirez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287

    Article  CAS  PubMed  Google Scholar 

  • Lu D, Lin W, Gao X et al (2011) Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332:1439–1442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luisa I, Iniesto E, Rodriguez L et al (2014) Targeted degradation of abscisic acid receptors is mediated by the ubiquitin ligase substrate adaptor DDA1 in Arabidopsis. Plant Cell 26:712–728

    Article  CAS  Google Scholar 

  • Luo M, Luo M, Buzas D et al (2008) UBIQUITIN-SPECIFIC PROTEASE26 is required for seed development and the repression of PHERES1 in Arabidopsis. Genetics 180:229–236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lyzenga WJ, Stone SL (2012) Abiotic stress tolerance mediated by protein ubiquitination. J Exp Bot 63:599–616

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Szostkiewicz I, Korte A et al (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068

    CAS  PubMed  Google Scholar 

  • Makarevich G, Leroy O, Akinci U et al (2006) Different Polycomb group complexes regulate common target genes in Arabidopsis. EMBO Rep 7:947–952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marino D, Peeters N, Rivas S (2012) Ubiquitination during plant immune signaling. Plant Physiol 160:15–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McClung C, Hsu M, Painter J et al (2000) Integrated temporal regulation of the photorespiratory pathway. Circadian regulation of two Arabidopsis genes encoding serine hydroxymethyltransferase. Plant Physio 123:381–392

    Article  CAS  Google Scholar 

  • Mcgouran JF, Gaertner SR, Altun M, Kramer HB et al (2013) Deubiquitinating enzyme specificity for ubiquitin chain topology profiled by di-ubiquitin activity probes. Chem Biol 20:1447–1455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meinke DW (2003) Molecular genetics of plant embryogenesis. Annu Rev Plant Biol 46:369–394

    Article  Google Scholar 

  • Melaragno JE, Mehrotra BL, Coleman AW (1993) Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5:1661–1668

    Article  PubMed  PubMed Central  Google Scholar 

  • Michaels S, Amasino R (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyakawa T, Fujita Y, Yamaguchishinozaki K et al (2013) Structure and function of abscisic acid receptors. Trends Plant Sci 18:259–266

    Article  CAS  PubMed  Google Scholar 

  • Moon J, Parry G, Estelle M (2004) The ubiquitin-proteasome pathway and plant development. Plant Cell 16:3181–3195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moon YK, Hong J, Cho Y et al (2009) Structure and expression of OsUBP6, an ubiquitin-specific protease 6 homolog in rice (Oryza sativa L.). Mol Cell 28:463–472

    Article  CAS  Google Scholar 

  • Moreno J, Martín R, Castresana C (2005) Arabidopsis SHMT1, a serine hydroxymethyltransferase that functions in the photorespiratory pathway influences resistance to biotic and abiotic stress. Plant J 41:451–463

    Article  CAS  PubMed  Google Scholar 

  • Nijman SM, Lunavargas MP, Velds A et al (2005) A genomic and functional inventory of deubiquitinating enzymes. Cell 123:773–786

    Article  CAS  PubMed  Google Scholar 

  • Nowack MK, Harashima H, Dissmeyer N et al (2012) Genetic framework of cyclin-dependent kinase function in Arabidopsis. Dev Cell 22:1030–1040

    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 SY, Fung P, Nishimura N et al (2009) Abscisic acid inhibits type 2 C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071

    CAS  PubMed  PubMed Central  Google Scholar 

  • Paul MH (2003) Plant cellular and molecular responses to high salinity. Annu Rev Plant Biol 51:463–499

    Google Scholar 

  • Peret B, Clement M, Nussaume L et al (2011) Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci 16:442–450

    Article  CAS  PubMed  Google Scholar 

  • Pickart CM (2003) Mechanisms underlying ubiquitination. Annu Rev Biochem 70:503–533

    Article  Google Scholar 

  • Pickart C, Eddins M (2004) Ubiquitin: structures, functions, mechanisms. BBA Mol Cell Res 1695:55–72

    CAS  Google Scholar 

  • Pien S, Fleury D, Mylne JS et al (2008) ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 20:580–588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piper RC, Dikic I, Lukacs GL (2014) Ubiquitin-dependent sorting in endocytosis. CSH Perspect Biol 6:a016808

    Google Scholar 

  • Qiu Q, Guo Y, Dietrich M et al (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99:8436–8441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qu X, Jiang Y, Chang M et al (2015) Organization and regulation of the actin cytoskeleton in the pollen tube. Front Plant Sci 5:786

    Article  PubMed  PubMed Central  Google Scholar 

  • Quan R, Lin H, Mendoza I et al (2007) SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 19:1415–1431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Racioppi J, Dahlman D, Neukranz R (1981) Effects of L-Canavanine on arginine catabolism in Manduca-sexta (Sphingidae,Lepidoptera). Comp Biochem Physiol B 70:639–642

    Article  Google Scholar 

  • Raghavendra AS, Gonugunta VK, Christmann A et al (2010) ABA perception and signalling. Trends Plant Sci 15:395–401

    Article  CAS  PubMed  Google Scholar 

  • Raonaik C, Chandler J, Mcardle B et al (2000) Ubiquitin-specific proteases from Arabidopsis thaliana: cloning of AtUBP5 and analysis of substrate specificity of AtUBP3, AtUBP4, and AtUBP5 using Escherichia coli in vivo and in vitro assays. Arch Biochem Biophys 379:198–208

    Article  CAS  Google Scholar 

  • Reyesturcu FE, Ventii KH, Wilkinson KD (2009) Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 78:363–397

    Article  CAS  Google Scholar 

  • Rosenthal G (1991) The biochemical basis for the deleterious effects of L-canavanine. Phytochemistry 30:1055–1058

    Article  CAS  Google Scholar 

  • Rubio V, Linhares FR, Solano R et al (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Gene Dev 15:2122–2133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rusten TE, Vaccari T, Lindmo K, Rodahl LM et al (2007) ESCRTs and Fab1 regulate distinct steps of autophagy. Curr Biol 17:1817–1825

    Article  CAS  PubMed  Google Scholar 

  • Salazarhenao JE, Velezbermudez IC, Schmidt W (2016) The regulation and plasticity of root hair patterning and morphogenesis. Development 143:1848–1858

    Article  CAS  Google Scholar 

  • Sanchezcalderon L, Lopezbucio J, Chaconlopez A et al (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46:174–184

    Article  CAS  Google Scholar 

  • Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69

    Article  CAS  PubMed  Google Scholar 

  • Schiefelbein J, Kwak S, Wieckowski Y et al (2009) The gene regulatory network for root epidermal cell-type pattern formation in Arabidopsis. J Exp Bot 60:1515–1521

    Article  CAS  PubMed  Google Scholar 

  • Schmitz RJ, Tamada Y, Doyle MR et al (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 

  • Searle N (2003) Physiology of flowering. Annu Rev Plant Biol 16:97–118

    Article  Google Scholar 

  • Sheldon CC, Burn JE, Perez P et al (1999) The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11:445–458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi H, Ishitani M, Kim C et al (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896–6901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Somerville C, Ogren W (1981) Photorespiration-deficient Mutants of Arabidopsis thaliana lacking mitochondrial serine transhydroxymethylase activity. Plant Physiol 67:666–671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sridhar V, Kapoor A, Zhang K et al (2007) Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature 447:735–U18

    Article  CAS  PubMed  Google Scholar 

  • Steinhorst L, Kudla J (2013) Calcium: a central regulator of pollen germination and tube growth. BBA 1833:1573–1581

    CAS  PubMed  Google Scholar 

  • Suarezlopez P, Wheatley K, Robson F et al (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410:1116–1120

    Article  CAS  Google Scholar 

  • Sullivan ML, Callis J, Vierstra RD (1990) High performance liquid chromatography resolution of ubiquitin pathway enzymes from wheat germ. Plant Physiol 94:710–716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor LP, Hepler PK (2003) Pollengermination and tube growth. Annu Rev Plant Biol 48:461–491

    Article  Google Scholar 

  • Thomma B, Nurnberger T, Joosten M (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turck F, Fornara F, Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59:573–594

    Article  CAS  PubMed  Google Scholar 

  • Ulrich H (2012) Ubiquitin and SUMO in DNA repair at a glance. J Cell Sci 125:249–254

    Article  CAS  PubMed  Google Scholar 

  • Urade R (2009) The endoplasmic reticulum stress signaling pathways in plants. Biofactors 35:326–331

    Article  CAS  PubMed  Google Scholar 

  • Verma R, Aravind L, Oania R et al (2002) Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26 S proteasome. Science 298:611–615

    Article  CAS  PubMed  Google Scholar 

  • Vierstra R (1996) Proteolysis in plants: mechanisms and functions. Plant Mol Biol 32:275–302

    Article  CAS  PubMed  Google Scholar 

  • Voll L, Jamai A, Renne P et al (2006) The photorespiratory Arabidopsisshm1 mutant is deficient in SHM1. Plant Physiol 140:59–66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang F, Liu P, Zhang Q et al (2012) Phosphorylation and ubiquitination of dynamin-related proteins (AtDRP3A/3B) synergically regulate mitochondrial proliferation during mitosis. Plant J 72:43–56

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson KD (1997) Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. FASEB J 11:1245–1256

    CAS  PubMed  Google Scholar 

  • Wilkinson KD (2000) Ubiquitination and deubiquitination: targeting of proteins for degradation by the proteasome. Semin Cell Dev Biol 11:141–148

    Article  CAS  PubMed  Google Scholar 

  • Xia T, Li N, Dumenil J et al (2013) The ubiquitin receptor DA1 interacts with the E3 ubiquitin ligase DA2 to regulate seed and organ size in Arabidopsis. Plant Cell 25:3347–3359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Jin W, Li N et al (2016) UBIQUITIN-SPECIFIC PROTEASE 14 interacts with ULTRAVIOLET-B INSENSITIVE 4 to regulate endoreduplication and cell and organ growth in Arabidopsis. Plant Cell 28:1200–1214

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yan N, Doelling J, Falbel T et al (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 

  • Zelazny E, Barberon M, Curie C, Vert G (2011) Ubiquitination of transporters at the forefront of plant nutrition. Plant Signal Behav 6:1597–1599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y (2003) Transcriptional regulation by histone ubiquitination and deubiquitination. Gene Dev 17:2733–2740

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Garreton V, Chua N (2005) The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Gene Dev 19:1532–1543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Zhou H, Zhang M et al (2016) Ubiquitin-specific protease24 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 et al (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 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  CAS  PubMed  Google Scholar 

  • Zielke N, Querings S, Rottig C et al (2008) The anaphase-promoting complex/cyclosome (APC/C) is required for rereplication control in endoreplication cycles. Genes Dev 22:1690–1703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zipfel C (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20:10–16

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We sincerely apologize to those authors for not being able to cite their works in this review due to space limitation. We thank Dr. Yan Guo from China Agricultural University for critical reading of the manuscript and stimulating discussions. This work was supported by the National Natural Science Foundation of China (31600201 to H.Z.).

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All the authors contributed to the discussion. JC illustrated the artwork. HZ wrote the article.

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Correspondence to Huapeng Zhou.

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Accession numbers: Sequence data of AtUBPs related to this review can be found in the Arabidopsis Genome Initiative or GenBank/EMBL databases under the following accession numbers: At2g32780 (AtUBP1), At1g04860 (AtUBP2), At4g39910 (AtUBP3), At2g22310 (AtUBP4), At2g40930 (AtUBP5), At1g51710 (AtUBP6), At3g21280 (AtUBP7), At5g22030 (AtUBP8), At4g10570 (AtUBP9), At4g10590 (AtUBP10), At1g32850 (AtUBP11), At5g06600 (AtUBP12), At3g11910 (AtUBP13), At3g20630 (AtUBP14), At1g17110 (AtUBP15), At4g24560 (AtUBP16), At5g65450 (AtUBP17), At4g31670 (AtUBP18), At2g24640 (AtUBP19), At4g17895 (AtUBP20), At5g46740 (AtUBP21), At5g10790 (AtUBP22), At5g57990 (AtUBP23), At4g30890 (AtUBP24), At3g14400 (AtUBP25), At3g49600 (AtUBP26), and At4g39370 (AtUBP27).

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Zhou, H., Zhao, J., Cai, J. et al. UBIQUITIN-SPECIFIC PROTEASES function in plant development and stress responses. Plant Mol Biol 94, 565–576 (2017). https://doi.org/10.1007/s11103-017-0633-5

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