Ubiquitin-Specific Proteases UBP12 and UBP13 Act in Circadian Clock and Photoperiodic Flowering Regulation in Arabidopsis

Oxford University Press (OUP) - Tập 162 Số 2 - Trang 897-906 - 2013
Xia Cui1, Falong Lu1, Yue Li2, Yongming Xue1,3, Yanyuan Kang1,3, Shuaibin Zhang1,3, Qi Qiu1,3, Xiekui Cui1, Shuzhi Zheng1, Bin Liu4, Xiaodong Xu2, Xiaofeng Cao1,3
1State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (Xia C., F.L., Y.X., Y.K., S.Zha., Q.Q., Xie.C., S.Zhe., X.Cao)
2Hebei Key Laboratory of Molecular Cell Biology, College of Biological Sciences, Hebei Normal University, Shijiazhuang, Hebei 050016, China (Y.L., X.X.)
3University of Chinese Academy of Sciences, Yuquan Road, Beijing 100039, China (Y.X., Y.K., S.Zha., Q.Q., Xie.C.); and
4Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China (B.L.)

Tóm tắt

Abstract Protein ubiquitination is involved in most cellular processes. In Arabidopsis (Arabidopsis thaliana), ubiquitin-mediated protein degradation regulates the stability of key components of the circadian clock feedback loops and the photoperiodic flowering pathway. Here, we identified two ubiquitin-specific proteases, UBP12 and UBP13, involved in circadian clock and photoperiodic flowering regulation. Double mutants of ubp12 and ubp13 display pleiotropic phenotypes, including early flowering and short periodicity of circadian rhythms. In ubp12 ubp13 double mutants, CONSTANS (CO) transcript rises earlier than that of wild-type plants during the day, which leads to increased expression of FLOWERING LOCUS T. This, and analysis of ubp12 co mutants, indicates that UBP12 and UBP13 regulate photoperiodic flowering through a CO-dependent pathway. In addition, UBP12 and UBP13 regulate the circadian rhythm of clock genes, including LATE ELONGATED HYPOCOTYL, CIRCADIAN CLOCK ASSOCIATED1, and TIMING OF CAB EXPRESSION1. Furthermore, UBP12 and UBP13 are circadian controlled. Therefore, our work reveals a role for two deubiquitinases, UBP12 and UBP13, in the control of the circadian clock and photoperiodic flowering, which extends our understanding of ubiquitin in daylength measurement in higher plants.

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Tài liệu tham khảo

Alabadí, 2001, Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock, Science, 293, 880, 10.1126/science.1061320

Baudry, 2010, F-box proteins FKF1 and LKP2 act in concert with ZEITLUPE to control Arabidopsis clock progression, Plant Cell, 22, 606, 10.1105/tpc.109.072843

Carré, 2002, MYB transcription factors in the Arabidopsis circadian clock, J Exp Bot, 53, 1551, 10.1093/jxb/erf027

Chandler, 1997, AtUBP3 and AtUBP4 are two closely related Arabidopsis thaliana ubiquitin-specific proteases present in the nucleus, Mol Gen Genet, 255, 302, 10.1007/s004380050501

Daubeuf, 2009, HSV ICP0 recruits USP7 to modulate TLR-mediated innate response, Blood, 113, 3264, 10.1182/blood-2008-07-168203

Doelling, 2007, The ubiquitin-specific protease subfamily UBP3/UBP4 is essential for pollen development and transmission in Arabidopsis, Plant Physiol, 145, 801, 10.1104/pp.106.095323

Doelling, 2001, The ubiquitin-specific protease UBP14 is essential for early embryo development in Arabidopsis thaliana, Plant J, 27, 393, 10.1046/j.1365-313X.2001.01106.x

Everett, 1997, A novel ubiquitin-specific protease is dynamically associated with the PML nuclear domain and binds to a herpesvirus regulatory protein, EMBO J, 16, 566, 10.1093/emboj/16.3.566

Ewan, 2011, Deubiquitinating enzymes AtUBP12 and AtUBP13 and their tobacco homologue NtUBP12 are negative regulators of plant immunity, New Phytol, 191, 92, 10.1111/j.1469-8137.2011.03672.x

Finley, 2009, Recognition and processing of ubiquitin-protein conjugates by the proteasome, Annu Rev Biochem, 78, 477, 10.1146/annurev.biochem.78.081507.101607

Fornara, 2009, Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response, Dev Cell, 17, 75, 10.1016/j.devcel.2009.06.015

Fujiwara, 2008, Circadian clock proteins LHY and CCA1 regulate SVP protein accumulation to control flowering in Arabidopsis, Plant Cell, 20, 2960, 10.1105/tpc.108.061531

Gendron, 2012, Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor, Proc Natl Acad Sci USA, 109, 3167, 10.1073/pnas.1200355109

Harmer, 2009, The circadian system in higher plants, Annu Rev Plant Biol, 60, 357, 10.1146/annurev.arplant.043008.092054

Huang, 2012, Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator, Science, 336, 75, 10.1126/science.1219075

Huang, 2011, Deubiquitylase HAUSP stabilizes REST and promotes maintenance of neural progenitor cells, Nat Cell Biol, 13, 142, 10.1038/ncb2153

Imaizumi, 2006, Photoperiodic control of flowering: not only by coincidence, Trends Plant Sci, 11, 550, 10.1016/j.tplants.2006.09.004

Imaizumi, 2005, FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis, Science, 309, 293, 10.1126/science.1110586

Ito, 2012, LOV domain-containing F-box proteins: light-dependent protein degradation modules in Arabidopsis, Mol Plant, 5, 573, 10.1093/mp/sss013

Jang, 2008, Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response, EMBO J, 27, 1277, 10.1038/emboj.2008.68

Katz, 2010, A new map to understand deubiquitination, Biochem Soc Trans, 38, 21, 10.1042/BST0380021

Khoronenkova, 2012, ATM-dependent downregulation of USP7/HAUSP by PPM1G activates p53 response to DNA damage, Mol Cell, 45, 801, 10.1016/j.molcel.2012.01.021

Kiba, 2007, Targeted degradation of PSEUDO-RESPONSE REGULATOR5 by an SCFZTL complex regulates clock function and photomorphogenesis in Arabidopsis thaliana, Plant Cell, 19, 2516, 10.1105/tpc.107.053033

Kim, 2007, ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light, Nature, 449, 356, 10.1038/nature06132

Kim, 2005, Independent roles for EARLY FLOWERING 3 and ZEITLUPE in the control of circadian timing, hypocotyl length, and flowering time, Plant Physiol, 139, 1557, 10.1104/pp.105.067173

Lau, 2012, The photomorphogenic repressors COP1 and DET1: 20 years later, Trends Plant Sci, 17, 584, 10.1016/j.tplants.2012.05.004

Li, 2008, A repressor complex governs the integration of flowering signals in Arabidopsis, Dev Cell, 15, 110, 10.1016/j.devcel.2008.05.002

Li, 2002, Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization, Nature, 416, 648, 10.1038/nature737

Liu, 2008, COP1-mediated ubiquitination of CONSTANS is implicated in cryptochrome regulation of flowering in Arabidopsis, Plant Cell, 20, 292, 10.1105/tpc.107.057281

Liu, 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, 10.1111/j.1365-313X.2008.03557.x

Lu, 2011, Arabidopsis REF6 is a histone H3 lysine 27 demethylase, Nat Genet, 43, 715, 10.1038/ng.854

Luo, 2008, UBIQUITIN-SPECIFIC PROTEASE 26 is required for seed development and the repression of PHERES1 in Arabidopsis, Genetics, 180, 229, 10.1534/genetics.108.091736

Maertens, 2010, Ubiquitin-specific proteases 7 and 11 modulate Polycomb regulation of the INK4a tumour suppressor, EMBO J, 29, 2553, 10.1038/emboj.2010.129

Más, 2003, Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana, Nature, 426, 567, 10.1038/nature02163

McClung, 2011, The genetics of plant clocks, Adv Genet, 74, 105, 10.1016/B978-0-12-387690-4.00004-0

Moon, 2004, The ubiquitin-proteasome pathway and plant development, Plant Cell, 16, 3181, 10.1105/tpc.104.161220

Nagel, 2012, Complexity in the wiring and regulation of plant circadian networks, Curr Biol, 22, R648, 10.1016/j.cub.2012.07.025

Nelson, 2000, FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis, Cell, 101, 331, 10.1016/S0092-8674(00)80842-9

Neutzner, 2012, Enzymes of ubiquitination and deubiquitination, Essays Biochem, 52, 37, 10.1042/bse0520037

Nicholson, 2011, The multifaceted roles of USP7: new therapeutic opportunities, Cell Biochem Biophys, 60, 61, 10.1007/s12013-011-9185-5

Nijman, 2005, A genomic and functional inventory of deubiquitinating enzymes, Cell, 123, 773, 10.1016/j.cell.2005.11.007

Niu, 2008, Redundant requirement for a pair of PROTEIN ARGININE METHYLTRANSFERASE4 homologs for the proper regulation of Arabidopsis flowering time, Plant Physiol, 148, 490, 10.1104/pp.108.124727

Plautz, 1997, Quantitative analysis of Drosophila period gene transcription in living animals, J Biol Rhythms, 12, 204, 10.1177/074873049701200302

Pokhilko, 2012, The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops, Mol Syst Biol, 8, 574, 10.1038/msb.2012.6

Reyes-Turcu, 2009, Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes, Annu Rev Biochem, 78, 363, 10.1146/annurev.biochem.78.082307.091526

Sawa, 2007, FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis, Science, 318, 261, 10.1126/science.1146994

Schmitz, 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, 10.1104/pp.108.131508

Song, 2008, The deubiquitinylation and localization of PTEN are regulated by a HAUSP-PML network, Nature, 455, 813, 10.1038/nature07290

Sridhar, 2007, Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination, Nature, 447, 735, 10.1038/nature05864

Takase, 2011, LOV KELCH PROTEIN2 and ZEITLUPE repress Arabidopsis photoperiodic flowering under non-inductive conditions, dependent on FLAVIN-BINDING KELCH REPEAT F-BOX1, Plant J, 67, 608, 10.1111/j.1365-313X.2011.04618.x

van der Horst, 2006, FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP, Nat Cell Biol, 8, 1064, 10.1038/ncb1469

van der Knaap, 2005, GMP synthetase stimulates histone H2B deubiquitylation by the epigenetic silencer USP7, Mol Cell, 17, 695, 10.1016/j.molcel.2005.02.013

Vierstra, 2009, The ubiquitin-26S proteasome system at the nexus of plant biology, Nat Rev Mol Cell Biol, 10, 385, 10.1038/nrm2688

Weigel, 2002, Arabidopsis: A Laboratory Manual.

Wing, 2003, Deubiquitinating enzymes—the importance of driving in reverse along the ubiquitin-proteasome pathway, Int J Biochem Cell Biol, 35, 590, 10.1016/S1357-2725(02)00392-8

Xu, 2010, Robust circadian rhythms of gene expression in Brassica rapa tissue culture, Plant Physiol, 153, 841, 10.1104/pp.110.155465

Yan, 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, 10.1104/pp.124.4.1828

Yanovsky, 2002, Molecular basis of seasonal time measurement in Arabidopsis, Nature, 419, 308, 10.1038/nature00996

Yu, 2008, COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability, Mol Cell, 32, 617, 10.1016/j.molcel.2008.09.026