The circadian clock ticks in plant stress responses

Abstract

The circadian clock, a time-keeping mechanism, drives nearly 24-h self-sustaining rhythms at the physiological, cellular, and molecular levels, keeping them synchronized with the cyclic changes of environmental signals. The plant clock is sensitive to external and internal stress signals that act as timing cues to influence the circadian rhythms through input pathways of the circadian clock system. In order to cope with environmental stresses, many core oscillators are involved in defense while maintaining daily growth in various ways. Recent studies have shown that a hierarchical multi-oscillator network orchestrates the defense through rhythmic accumulation of gene transcripts, alternative splicing of mRNA precursors, modification and turnover of proteins, subcellular localization, stimuli-induced phase separation, and long-distance transport of proteins. This review summarizes the essential role of circadian core oscillators in response to stresses in Arabidopsis thaliana and crops, including daily and seasonal abiotic stresses (low or high temperature, drought, high salinity, and nutrition deficiency) and biotic stresses (pathogens and herbivorous insects). By integrating time-keeping mechanisms, circadian rhythms and stress resistance, we provide a temporal perspective for scientists to better understand plant environmental adaptation and breed high-quality crop germplasm for agricultural production.

Keywords

Circadian clock / Temperature stress / Drought / Salinity / Pathogen

References

[1] AdamsS, GrundyJ, VeflingstadSR, DyerNP, HannahMA, OttS, CarreIA. Circadian control of abscisic acid biosynthesis and signalling pathways revealed by genome-wide analysis of LHY binding targets. New Phytol, 2018, 220: 893-907

[2] Andres-ColasN, Perea-GarciaA, PuigS, PenarrubiaL. Deregulated copper transport affects Arabidopsis development especially in the absence of environmental cycles. Plant Physiol, 2010, 153: 170-184

[3] AtamianHS, HarmerSL. Circadian regulation of hormone signaling and plant physiology. Plant Mol Biol, 2016, 91: 691-702

[4] BaekD, KimWY, ChaJY, ParkHJ, ShinG, ParkJ, LimCJ, ChunHJ, LiN, KimDH, LeeSY, PardoJM, KimMC, YunDJ. The GIGANTEA-ENHANCED EM LEVEL complex enhances drought tolerance via regulation of abscisic acid synthesis. Plant Physiol, 2020, 184: 443-458

[5] BelbinFE, HallGJ, JacksonAB, SchanschieffFE, ArchibaldG, FormstoneC, DoddAN. Plant circadian rhythms regulate the effectiveness of a glyphosate-based herbicide. Nat Commun, 2019, 10: 3704

[6] BieniawskaZ, EspinozaC, SchlerethA, SulpiceR, HinchaDK, HannahMA. Disruption of the Arabidopsis circadian clock is responsible for extensive variation in the cold-responsive transcriptome. Plant Physiol, 2008, 147: 263-279

[7] BodenSA, WeissD, RossJJ, DaviesNW, TrevaskisB, ChandlerPM, SwainSM. EARLY FLOWERING3 regulates FLOWERING in spring barley by mediating gibberellin production and FLOWERING LOCUS T expression. Plant Cell, 2014, 26: 1557-1569

[8] BonnotT, BlairEJ, CordingleySJ, NagelDH. Circadian coordination of cellular processes and abiotic stress responses. Curr Opin Plant Biol, 2021, 64: 102133

[9] BoxMS, HuangBE, DomijanM, JaegerKE, KhattakAK, YooSJ, SedivyEL, JonesDM, HearnTJ, WebbAA, GrantA, LockeJC, WiggePA. ELF3 controls thermoresponsive growth in Arabidopsis. Curr Biol, 2015, 25: 194-199

[10] BriatJF, DucC, RavetK, GaymardF. Ferritins and iron storage in plants. Biochim Biophys Acta, 2010, 1800(8):806-814

[11] BritzSJ, BriggsWR. Circadian rhythms of chloroplast orientation and photosynthetic capacity in ulva. Plant Physiol, 1976, 58: 22-27

[12] BruceVG, WeightF, PittendrighCS. Resetting the sporulation rhythm in Pilobolus with short light flashes of high intensity. Science, 1960, 131(3402):728-730

[13] CaoS, YeM, JiangS. Involvement of GIGANTEA gene in the regulation of the cold stress response in Arabidopsis. Plant Cell Rep, 2005, 24(11):683-690

[14] CarréIA. ELF3: a circadian safeguard to buffer effects of light. Trends Plant Sci, 2002, 7: 4-6

[15] ChaJY, KimJ, KimTS, ZengQ, WangL, LeeSY, KimWY, SomersDE. GIGANTEA is a co-chaperone which facilitates maturation of ZEITLUPE in the Arabidopsis circadian clock. Nat Commun, 2017, 8: 3

[16] ChenWW, TakahashiN, HirataY, RonaldJ, PorcoS, DavisSJ, NusinowDA, KaySA, MasP. A mobile ELF4 delivers circadian temperature information from shoots to roots. Nat Plants, 2020, 6: 416-426

[17] ChenYY, WangY, ShinLJ, WuJF, ShanmugamV, TsedneeM, LoJC, ChenCC, WuSH, YehKC. Iron is involved in the maintenance of circadian period length in Arabidopsis. Plant Physiol, 2013, 161(3):1409-1420

[18] ChengQ, GanZ, WangY, LuS, HouZ, LiH, XiangH, LiuB, KongF, DongL. The soybean gene J contributes to salt stress tolerance by up-regulating salt-responsive genes. Front Plant Sci, 2020, 11: 272

[19] CovingtonMF, MaloofJN, StraumeM, KaySA, HarmerSL. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol, 2008, 9: R130

[20] CovingtonMF, PandaS, LiuXL, StrayerCA, WagnerDR, KaySA. ELF3 modulates resetting of the circadian clock in Arabidopsis. Plant Cell, 2001, 13: 1305-1316

[21] CreuxN, HarmerS. Circadian rhythms in plants. Cold Spring Harb Perspect Biol, 2019, 11: a034611

[22] de MeloJRF, GutschA, CaluweT, LeloupJC, GonzeD, HermansC, WebbAAR, VerbruggenN. Magnesium maintains the length of the circadian period in Arabidopsis. Plant Physiol, 2021, 185: 519-532

[23] DesaiJS, LawasLMF, ValenteAM, LemanAR, GrinevichDO, JagadishSVK, DohertyCJ. Warm nights disrupt transcriptome rhythms in field-grown rice panicles. Proc Natl Acad Sci U S A, 2021, 118: e2025899118

[24] DingL, WangS, SongZT, JiangY, HanJJ, LuSJ, LiL, LiuJX. Two B-Box domain proteins, BBX18 and BBX23, interact with ELF3 and regulate Thermomorphogenesis in Arabidopsis. Cell Rep, 2018, 25: 1718-1728

[25] DingZ, MillarAJ, DavisAM, DavisSJ. TIME FOR COFFEE encodes a nuclear regulator in the Arabidopsis thaliana circadian clock. Plant Cell, 2007, 19: 1522-1536

[26] DoddAN, SalathiaN, HallA, KeveiE, TothR, NagyF, HibberdJM, MillarAJ, WebbAAR. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science, 2005, 309: 630-633

[27] DongMA, FarréEM, ThomashowMF. CIRCADIAN CLOCK-ASSOCIATED 1 and LATE ELONGATED HYPOCOTYL regulate expression of the C-REPEAT BINDING FACTOR (CBF) pathway in Arabidopsis. Proc Natl Acad Sci U S A, 2011, 108: 7241-7246

[28] DucC, CellierF, LobreauxS, BriatJF, GaymardF. Regulation of iron homeostasis in Arabidopsis thaliana by the clock regulator time for coffee. J Biol Chem, 2009, 284: 36271-36281

[29] EdwardsKD, LynnJR, GyulaP, NagyF, MillarAJ. Natural allelic variation in the temperature-compensation mechanisms of the Arabidopsis thaliana circadian clock. Genetics, 2005, 170: 387-400

[30] EndoM, ShimizuH, NohalesMA, ArakiT, KaySA. Tissue-specific clocks in Arabidopsis show asymmetric coupling. Nature, 2014, 515: 419-422

[31] EzerD, JungJH, LanH, BiswasS, GregoireL, BoxMS, CharoensawanV, CortijoS, LaiX, StockleD, ZubietaC, JaegerKE, WiggePA. The evening complex coordinates environmental and endogenous signals in Arabidopsis. Nat Plants, 2017, 3(7):17087

[32] FeeneyKA, HansenLL, PutkerM, Olivares-YanezC, DayJ, EadesLJ, LarrondoLF, HoyleNP, O'NeillJS, van OoijenG. Daily magnesium fluxes regulate cellular timekeeping and energy balance. Nature, 2016, 532: 375-379

[33] FilichkinSA, MocklerTC. Unproductive alternative splicing and nonsense mRNAs: a widespread phenomenon among plant circadian clock genes. Biol Direct, 2012, 7: 20

[34] FornaraF, de MontaiguA, Sanchez-VillarrealA, TakahashiY, Ver Loren van ThemaatE, HuettelB, DavisSJ, CouplandG. The GI-CDF module of Arabidopsis affects freezing tolerance and growth as well as flowering. Plant J, 2015, 81: 695-706

[35] FranklinKA, LeeSH, PatelD, KumarSV, SpartzAK, GuC, YeS, YuP, BreenG, CohenJD, WiggePA, GrayWM. PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc Natl Acad Sci U S A, 2011, 108: 20231-20235

[36] FujiwaraS, WangL, HanL, SuhSS, SaloméPA, McClungCR, SomersDE. Post-translational regulation of the circadian clock through selective proteolysis and phosphorylation of pseudo-response regulator proteins. J Biol Chem, 2008, 283: 23073-23083

[37] GendronJM, Pruneda-PazJL, DohertyCJ, GrossAM, KangSE, KaySA. Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor. Proc Natl Acad Sci U S A, 2012, 109: 3167-3172

[38] GilKE, KimWY, LeeHJ, FaisalM, SaquibQ, AlatarAA, ParkCM. ZEITLUPE contributes to a Thermoresponsive protein quality control system in Arabidopsis. Plant Cell, 2017, 29(11):2882-2894

[39] GohCH, NamHG, ParkYS. Stress memory in plants: a negative regulation of stomatal response and transient induction of rd22 gene to light in abscisic acid-entrained Arabidopsis plants. Plant J, 2003, 36: 240-255

[40] GolL, HaraldssonEB, von KorffM. Ppd-H1 integrates drought stress signals to control spike development and flowering time in barley. J Exp Bot, 2021, 72: 122-136

[41] GoodspeedD, ChehabEW, Min-VendittiA, BraamJ, CovingtonMF. Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior. Proc Natl Acad Sci U S A, 2012, 109: 4674-4677

[42] GoodspeedD, LiuJD, ChehabEW, ShengZ, FranciscoM, KliebensteinDJ, BraamJ. Postharvest circadian entrainment enhances crop pest resistance and phytochemical cycling. Curr Biol, 2013, 23: 1235-1241

[43] GortonHL, WilliamsWE, AssmannSM. Circadian rhythms in stomatal responsiveness to red and blue light. Plant Physiol, 1993, 103: 399-406

[44] GouldPD, DomijanM, GreenwoodM, TokudaIT, ReesH, Kozma-BognarL, HallAJ, LockeJC. Coordination of robust single cell rhythms in the Arabidopsis circadian clock via spatial waves of gene expression. Elife, 2018, 7: e31700

[45] GrayWM, ÖstinA, SandbergG, RomanoCP, EstelleM. High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc Natl Acad Sci U S A, 1998, 95: 7197-7202

[46] GreenhamK, McClungCR. Integrating circadian dynamics with physiological processes in plants. Nat Rev Genet, 2015, 16: 598-610

[47] GrundyJ, StokerC, CarreIA. Circadian regulation of abiotic stress tolerance in plants. Front Plant Sci, 2015, 6: 648

[48] GutierrezRA, StokesTL, ThumK, XuX, ObertelloM, KatariMS, TanurdzicM, DeanA, NeroDC, McClungCR, CoruzziGM. Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. Proc Natl Acad Sci U S A, 2008, 105: 4939-4944

[49] HananoS, DomagalskaMA, NagyF, DavisSJ. Multiple phytohormones influence distinct parameters of the plant circadian clock. Genes Cells, 2006, 11: 1381-1392

[50] HarmerSL, HogeneschJB, StraumeM, ChangHS, HanB, ZhuT, WangX, KrepsJA, KaySA. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science, 2000, 290: 2110-2113

[51] HaydonMJ, MielczarekO, RobertsonFC, HubbardKE, WebbAA. Photosynthetic entrainment of the Arabidopsis thaliana circadian clock. Nature, 2013, 502: 689-692

[52] HermansC, VuylstekeM, CoppensF, CraciunA, InzeD, VerbruggenN. Early transcriptomic changes induced by magnesium deficiency in Arabidopsis thaliana reveal the alteration of circadian clock gene expression in roots and the triggering of abscisic acid-responsive genes. New Phytol, 2010, 187(1):119-131

[53] HolmesMG, KlienWH. Photocontrol of dark circadian rhythms in stomata of Phaseolus vulgaris L. Plant Physiol, 1986, 82: 28-33

[54] HongS, KimSA, GuerinotML, McClungCR. Reciprocal interaction of the circadian clock with the iron homeostasis network in Arabidopsis. Plant Physiol, 2013, 161: 893-903

[55] HsuPY, HarmerSL. Wheels within wheels: the plant circadian system. Trends Plant Sci, 2014, 19(4):240-249

[56] HuangH, AlvarezS, BindbeutelR, ShenZ, NaldrettMJ, EvansBS, BriggsSP, HicksLM, KaySA, NusinowDA. Identification of evening complex associated proteins in Arabidopsis by affinity purification and mass spectrometry. Mol Cell Proteomics, 2016, 15: 201-217

[57] HuangW, Pérez-GarcíaP, PokhilkoA, MillarAJ, AntoshechkinI, RiechmannJL, MasP. Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science, 2012, 336: 75-79

[58] IbanezC, KozarewaI, JohanssonM, OgrenE, RohdeA, ErikssonME. Circadian clock components regulate entry and affect exit of seasonal dormancy as well as winter hardiness in Populus trees. Plant Physiol, 2010, 153: 1823-1833

[59] ImaizumiT. Arabidopsis circadian clock and photoperiodism: time to think about location. Curr Opin Plant Biol, 2010, 13: 83-89

[60] ImaizumiT, SchultzTF, HarmonFG, HoLA, KaySA. FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science, 2005, 309: 293-297

[61] ImaizumiT, TranHG, SwartzTE, BriggsWR, KaySA. FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature, 2003, 426: 302-306

[62] JamesAB, SyedNH, BordageS, MarshallJ, NimmoGA, JenkinsGI, HerzyP, BrownJWS, NimmoHG. Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes. Plant Cell, 2012, 24(3):961-981

[63] JeongYM, DiasC, DiekmanC, BrochonH, KimP, KaurM, KimYS, JangHI, KimYI. Magnesium regulates the circadian oscillator in Cyanobacteria. J Biol Rhythm, 2019, 34(4):380-390

[64] JiangBC, ShiYT, ZhangXY, XinXY, QiLJ, GuoHW, LiJG, YangSH. PIF3 is a negative regulator of the CBF pathway and freezing tolerance in Arabidopsis. Proc Natl Acad Sci U S A, 2017, 114: E6695-E6702

[65] JiangY, YangC, HuangS, XieF, XuY, LiuC, LiL. The ELF3-PIF7 interaction mediates the circadian gating of the shade response in Arabidopsis. iScience, 2019, 22: 288-298

[66] JohnsonCH. Forty years of PRCs--what have we learned?. Chronobiol Intl, 1999, 16: 711-743

[67] JohnsonCH, KnightMR, KondoT, MassonP, SedbrookJ, HaleyA, TrewavasA. Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science, 1995, 269: 1863-1865

[68] JohnsonCH, MoriT, XuY. A cyanobacterial circadian clockwork. Curr Biol, 2008, 18: R816-R825

[69] JungJH, BarbosaAD, HutinS, KumitaJR, GaoMJ, DerwortD, SilvaCS, LaiXL, PierreE, GengF, KimSB, BaekS, ZubietaC, JaegerKE, WiggePA. A prion-like domain in ELF3 functions as a thermosensor inArabidopsis. Nature, 2020, 585: 256-260

[70] JungJH, DomijanM, KloseC, BiswasS, EzerD, GaoM, KhattakAK, BoxMS, CharoensawanV, CortijoS, KumarM, GrantA, LockeJC, SchaferE, JaegerKE, WiggePA. Phytochromes function as thermosensors in Arabidopsis. Science, 2016, 354: 886-889

[71] KamiokaM, TakaoS, SuzukiT, TakiK, HigashiyamaT, KinoshitaT, NakamichiN. Direct repression of evening genes by CIRCADIAN CLOCK-ASSOCIATED1 in the Arabidopsis circadian clock. Plant Cell, 2016, 28: 696-711

[72] KidokoroS, HayashiK, HaraguchiH, IshikawaT, SomaF, KonouraI, TodaS, MizoiJ, SuzukiT, ShinozakiK, Yamaguchi-ShinozakiK. Posttranslational regulation of multiple clock-related transcription factors triggers cold-inducible gene expression in Arabidopsis. Proc Natl Acad Sci U S A, 2021, 118: e2021048118

[73] KimTS, WangL, KimYJ, SomersDE. Compensatory mutations in GI and ZTL may modulate temperature compensation in the circadian clock. Plant Physiol, 2020, 182(2):1130-1141

[74] KimW-Y, AliZ, ParkHJ, ParkSJ, ChaJ-Y, Perez-HormaecheJ, QuinteroFJ, ShinG, KimMR, QiangZ, NingL, ParkHC, LeeSY, BressanRA, PardoJM, BohnertHJ, YunD-J. Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis. Nat Commun, 2013, 4: 1352

[75] KimW-Y, FujiwaraS, SuhS-S, KimJ, KimY, HanL, DavidK, PutterillJ, NamHG, SomersDE. ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature, 2007, 449: 356-360

[76] KoiniMA, AlveyL, AllenT, TilleyCA, HarberdNP, WhitelamGC, FranklinKA. High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr Biol, 2009, 19: 408-413

[77] LauOS, HuangX, CharronJ-B, LeeJ-H, LiG, DengXW. Interaction of Arabidopsis DET1 with CCA1 and LHY in mediating transcriptional repression in the plant circadian clock. Mol Cell, 2011, 43(5):703-712

[78] LeeC-M, ThomashowMF. Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance in Arabidopsis thaliana. Proc Natl Acad Sci U S A, 2012, 109: 15054-15059

[79] LeeKH, PiaoHL, KimHY, ChoiSM, JiangF, HartungW, HwangI, KwakJM, LeeIJ. Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell, 2006, 126(6):1109-1120

[80] LegnaioliT, CuevasJ, MasP. TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought. EMBO J, 2009, 28: 3745-3757

[81] LegrisM, KloseC, BurgieES, RojasCC, NemeM, HiltbrunnerA, WiggePA, SchaferE, VierstraRD, CasalJJ. Phytochrome B integrates light and temperature signals in Arabidopsis. Science, 2016, 354: 897-900

[82] LeiJ, JayaprakashaGK, SinghJ, UckooR, BorregoEJ, FinlaysonS, KolomietsM, PatilBS, BraamJ, Zhu-SalzmanK. CIRCADIAN CLOCK-ASSOCIATED1 controls resistance to aphids by altering indole Glucosinolate production. Plant Physiol, 2019, 181: 1344-1359

[83] LiBJ, GaoZH, LiuXY, SunDY, TangWQ. Transcriptional profiling reveals a time-of-Day-specific role of REVEILLE 4/8 in regulating the first wave of heat shock-induced gene expression in Arabidopsis. Plant Cell, 2019, 31: 2353-2369

[84] LiJ, YokoshoK, LiuS, CaoHR, YamajiN, ZhuXG, LiaoH, MaJF, ChenZC. Diel magnesium fluctuations in chloroplasts contribute to photosynthesis in rice. Nat Plants, 2020, 6: 848-859

[85] LiR, LlorcaLC, SchumanMC, WangY, WangL, JooY, WangM, VassaoDG, BaldwinIT. ZEITLUPE in the roots of wild tobacco regulates Jasmonate-mediated nicotine biosynthesis and resistance to a generalist herbivore. Plant Physiol, 2018, 177: 833-846

[86] LiY, WangL, YuanL, SongY, SunJ, JiaQ, XieQ, XuX. Molecular investigation of organ-autonomous expression of Arabidopsis circadian oscillators. Plant Cell Environ, 2020, 43: 1501-1512

[87] LiuT, CarlssonJ, TakeuchiT, NewtonL, FarréEM. Direct regulation of abiotic responses by the Arabidopsis circadian clock component PRR7. Plant J, 2013, 76: 101-114

[88] LiuTL, NewtonL, LiuMJ, ShiuSH, FarreEM. A G-Box-like motif is necessary for transcriptional regulation by circadian Pseudo-response regulators in Arabidopsis. Plant Physiol, 2016, 170: 528-539

[89] LoveJ, DoddAN, WebbAAR. Circadian and diurnal calcium oscillations encode photoperiodic information in Arabidopsis. Plant Cell, 2004, 16: 956-966

[90] LuS, ZhaoX, HuY, LiuS, NanH, LiX, FangC, CaoD, ShiX, KongL, SuT, ZhangF, LiS, WangZ, YuanX, CoberER, WellerJL, LiuB, HouX, TianZ, KongF. Natural variation at the soybean J locus improves adaptation to the tropics and enhances yield. Nat Genet, 2017, 49: 773-779

[91] MaY, GilS, GrasserKD, MasP. Targeted recruitment of the basal transcriptional machinery by LNK clock components controls the circadian rhythms of nascent RNAs in Arabidopsis. Plant Cell, 2018, 30: 907-924

[92] MarkhamKK, GreenhamK. Abiotic stress through time. New Phytol, 2021, 231: 40-46

[93] MartinG, RoviraA, VecianaN, SoyJ, Toledo-OrtizG, GommersCMM, BoixM, HenriquesR, MinguetEG, AlabadiD, HallidayKJ, LeivarP, MonteE. Circadian waves of transcriptional repression shape PIF-regulated photoperiod-responsive growth in Arabidopsis. Curr Biol, 2018, 28: 311-318

[94] McClungCR. The plant circadian oscillator. Biology (Basel), 2019, 8: 14

[95] McWattersHG, BastowRM, HallA, MillarAJ. The ELF3 zeitnehmer regulates light signalling to the circadian clock. Nature, 2000, 408: 716-720

[96] MelottoM, UnderwoodW, HeSY. Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytopathol, 2008, 46: 101-122

[97] MillarAJ, CarréIA, StrayerCA, ChuaN-H, KaySA. Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science, 1995, 267: 1161-1163

[98] MizunoT, TakeuchiA, NomotoY, NakamichiN, YamashinoT. The LNK1 night light-inducible and clock-regulated gene is induced also in response to warm-night through the circadian clock nighttime repressor in Arabidopsis thaliana. Plant Signal Behav, 2014, 9: e28505

[99] MizunoT, YamashinoT. Comparative transcriptome of diurnally oscillating genes and hormone-responsive genes in Arabidopsis thaliana: insight into circadian clock-controlled daily responses to common ambient stresses in plants. Plant Cell Physiol., 2008, 49: 481-487

[100] MocklerTC, MichaelTP, PriestHD, ShenR, SullivanCM, GivanSA, McEnteeC, KaySA, ChoryJ. The diurnal project: diurnal and circadian expression profiling, model-based pattern matching, and promoter analysis. Cold Spring Harb Symp Quant Biol, 2007, 72: 353-363

[101] NagelDH, DohertyCJ, Pruneda-PazJL, SchmitzRJ, EckerJR, KaySA. Genome-wide identification of CCA1 targets uncovers an expanded clock network in Arabidopsis. Proc Natl Acad Sci U S A, 2015, 112: E4802-E4810

[102] NakamichiN, KibaT, HenriquesR, MizunoT, ChuaN-H, SakakibaraH. PSEUDO-RESPONSE REGULATORS 9, 7 and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell, 2010, 22: 594-605

[103] NakamichiN, KitaM, ItoS, SatoE, YamashinoT, MizunoT. PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol., 2005, 46(5):686-698

[104] NakamichiN, KusanoM, FukushimaA, KitaM, ItoS, YamashinoT, SaitoK, SakakibaraH, MizunoT. Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. Plant Cell Physiol, 2009, 50(3):447-462

[105] NelsonDC, LasswellJ, RoggLE, CohenMA, BartelB. FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell, 2000, 101(3):331-340

[106] NiZ, KimE-D, HaM, LackeyE, LiuJ, ZhangY, SunQ, ChenZJ. Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature, 2009, 457: 327-331

[107] NohalesMA, KaySA. Molecular mechanisms at the core of the plant circadian oscillator. Nat Struct Mol Biol, 2016, 23: 1061-1069

[108] NusinowDA, HelferA, HamiltonEE, KingJJ, ImaizumiT, SchultzTF, FarreEM, KaySA. The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature, 2011, 475: 398-402

[109] ParaA, FarréEM, ImaizumiT, Pruneda-PazJL, HarmonFG, KaySA. PRR3 is a vascular regulator of TOC1 stability in the Arabidopsis circadian clock. Plant Cell, 2007, 19(11):3462-3473

[110] ParkHJ, QiangZ, KimWY, YunDJ. Diurnal and circadian regulation of salt tolerance in Arabidopsis. J Plant Biol, 2016, 59: 569-578

[111] PittendrighCS. On the temperature independence in the clock system controlling emergence time in Drosophila. Proc Natl Acad Sci U S A, 1954, 40(10):1018-1029

[112] PittendrighCS. Circadian rhythms and the circadian organization of living systems. Cold Spring Harb Symp Quant Biol, 1960, 25: 159-184

[113] Pruneda-PazJL, BretonG, ParaA, KaySA. A functional genomics approach reveals CHE as a novel component of the Arabidopsis circadian clock. Science, 2009, 323: 1481-1485

[114] PudasainiA, ShimJS, SongYH, ShiH, KibaT, SomersDE, ImaizumiT, ZoltowskiBD. Kinetics of the LOV domain of ZEITLUPE determine its circadian function in Arabidopsis. Elife, 2017, 6: e21646

[115] QiJ, SongCP, WangB, ZhouJ, KangasjarviJ, ZhuJK, GongZ. Reactive oxygen species signaling and stomatal movement in plant responses to drought stress and pathogen attack. J Integr Plant Biol, 2018, 60(9):805-826

[116] QiuY, PasoreckEK, YooCY, HeJ, WangH, BajracharyaA, LiM, LarsenHD, CheungS, ChenM. RCB initiates Arabidopsis thermomorphogenesis by stabilizing the thermoregulator PIF4 in the daytime. Nat Commun, 2021, 12: 2042

[117] SaiJ, JohnsonCH. Different circadian oscillators control ca(2+) fluxes and Lhcb gene expression. Proc Natl Acad Sci U S A, 1999, 96: 11659-11663

[118] SakurabaY, BulbulS, PiaoW, ChoiG, PaekNC. Arabidopsis EARLY FLOWERING3 increases salt tolerance by suppressing salt stress response pathways. Plant J, 2017, 92: 1106-1120

[119] SakurabaY, HanSH, YangHJ, PiaoW, PaekNC. Mutation of Rice early Flowering3.1 (OsELF3.1) delays leaf senescence in rice. Plant Mol Biol, 2016, 92: 223-234

[120] SaloméPA, McClungCR. What makes the Arabidopsis clock tick on time?: a review on entrainment. Plant Cell Environ, 2005, 28: 21-38

[121] SaloméPA, OlivaM, WeigelD, KrämerU. Circadian clock adjustment to plant iron status depends on chloroplast and phytochrome function. EMBO J, 2013, 32: 511-523

[122] SaloméPA, WeigelD, McClungCR. The role of the Arabidopsis morning loop components CCA1, LHY, PRR7 and PRR9 in temperature compensation. Plant Cell, 2010, 22: 3650-3661

[123] SanchezSE, PetrilloE, BeckwithEJ, ZhangX, RugnoneML, HernandoCE, CuevasJC, Godoy HerzMA, Depetris-ChauvinA, SimpsonCG, BrownJWS, CerdánPD, BorevitzJO, MasP, CerianiMF, KornblihttAR, YanovskyMJ. A methyl transferase links the circadian clock to the regulation of alternative splicing. Nature, 2010, 468: 112-116

[124] SanchezSE, RugnoneML, KaySA. Light perception: a matter of time. Mol Plant, 2020, 13: 363-385

[125] SchultzTF, KiyosueT, YanovskyM, WadaM, KaySA. A role for LKP2 in the circadian clock of Arabidopsis. Plant Cell, 2001, 13: 2659-2670

[126] SeoPJ, MasP. Multiple layers of posttranslational regulation refine circadian clock activity in Arabidopsis. Plant Cell, 2014, 26(1):79-87

[127] SeoPJ, MasP. STRESSing the role of the plant circadian clock. Trends Plant Sci, 2015, 20: 230-237

[128] SeoPJ, ParkMJ, LimMH, KimSG, LeeM, BaldwinIT, ParkCM. A self-regulatory circuit of CIRCADIAN CLOCK-ASSOCIATED1 underlies the circadian clock regulation of temperature responses in Arabidopsis. Plant Cell, 2012, 24: 2427-2442

[129] SomersDE, DevlinP, KaySA. Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science, 1998, 282(5393):1488-1490

[130] SomersDE, SchultzTF, MilnamowM, KaySA. ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell, 2000, 101: 319-329

[131] SongYH, ShimJS, Kinmonth-SchultzHA, ImaizumiT. Photoperiodic flowering: time measurement mechanisms in leaves. Annu Rev Plant Biol, 2015, 66(1):441-464

[132] SoyJ, LeivarP, Gonzalez-SchainN, MartinG, DiazC, SentandreuM, Al-SadyB, QuailPH, MonteE. Molecular convergence of clock and photosensory pathways through PIF3-TOC1 interaction and co-occupancy of target promoters. Proc Natl Acad Sci U S A, 2016, 113(17):4870-4875

[133] SteedG, RamirezDC, HannahMA, WebbAAR. Chronoculture, harnessing the circadian clock to improve crop yield and sustainability. Science, 2021, 372: eabc9141

[134] SunQ, WangS, XuG, KangX, ZhangM, NiM. SHB1 and CCA1 interaction desensitizes light responses and enhances thermomorphogenesis. Nat Commun, 2019, 10: 3110

[135] TakahashiN, HirataY, AiharaK, MasP. A hierarchical multi-oscillator network orchestrates the Arabidopsis circadian system. Cell, 2015, 163: 148-159

[136] ThainSC, HallA, MillarAJ. Functional independence of circadian clocks that regulate plant gene expression. Curr Biol, 2000, 10: 951-956

[137] ThinesB, HarmonFG. Ambient temperature response establishes ELF3 as a required component of the core Arabidopsis circadian clock. Proc Natl Acad Sci U S A, 2010, 107: 3257-3262

[138] ValimH, DaltonH, JooY, McGaleE, HalitschkeR, GaquerelE, BaldwinIT, SchumanMC. TOC1 in Nicotiana attenuata regulates efficient allocation of nitrogen to defense metabolites under herbivory stress. New Phytol, 2020, 228: 1227-1242

[139] ValimHF, McGaleE, YonF, HalitschkeR, FragosoV, SchumanMC, BaldwinIT. The clock gene TOC1 in shoots, not roots, determines fitness of Nicotiana attenuata under drought. Plant Physiol, 2019, 181: 305-318

[140] WangK, BuT, ChengQ, DongL, SuT, ChenZ, KongF, GongZ, LiuB, LiM. Two homologous LHY pairs negatively control soybean drought tolerance by repressing the abscisic acid responses. New Phytol, 2021, 229: 2660-2675

[141] WangL, FujiwaraS, SomersDE. PRR5 regulates phosphorylation, nuclear import and subnuclear localization of TOC1 in the Arabidopsis circadian clock. EMBO J, 2010, 29: 1903-1915

[142] WangL, KimJ, SomersDE. Transcriptional corepressor TOPLESS complexes with pseudoresponse regulator proteins and histone deacetylases to regulate circadian transcription. Proc Natl Acad Sci U S A, 2013, 110: 761-766

[143] WangP, CuiX, ZhaoC, ShiL, ZhangG, SunF, CaoX, YuanL, XieQ, XuX. COR27 and COR28 encode nighttime repressors integrating Arabidopsis circadian clock and cold response. J Integr Plant Biol, 2017, 59: 78-85

[144] WangW, BarnabyJY, TadaY, LiH, TörM, CaldelariD, LeeD-U, FuX-D, DongX. Timing of plant immune responses by a central circadian regulator. Nature, 2011, 470: 110-114

[145] WangY, HeY, SuC, ZentellaR, SunTP, WangL. Nuclear localized O-Fucosyltransferase SPY facilitates PRR5 proteolysis to fine-tune the pace of Arabidopsis circadian clock. Mol Plant, 2020, 13: 446-458

[146] WangY, YuanL, SuT, WangQ, GaoY, ZhangS, JiaQ, YuG, FuY, ChengQ, LiuB, KongF, ZhangX, SongCP, XuX, XieQ. Light- and temperature-entrainable circadian clock in soybean development. Plant Cell Environ, 2020, 43: 637-648

[147] WebbAAR, SekiM, SatakeA, CaldanaC. Continuous dynamic adjustment of the plant circadian oscillator. Nat Commun, 2019, 10: 550

[148] WeiH, WangX, HeY, XuH, WangL. Clock component OsPRR73 positively regulates rice salt tolerance by modulating OsHKT2;1-mediated sodium homeostasis. EMBO J, 2021, 40: e105086

[149] WuJF, TsaiHL, JoanitoI, WuYC, ChangCW, LiYH, WangY, HongJC, ChuJW, HsuCP, WuSH. LWD-TCP complex activates the morning gene CCA1 in Arabidopsis. Nat Commun, 2016, 7: 13181

[150] WuJ-F, WangY, WuS-H. Two new clock proteins, LWD1 and LWD2, regulate Arabidopsis photoperiodic flowering. Plant Physiol, 2008, 148: 948-959

[151] XieQ, LouP, HermandV, AmanR, ParkHJ, YunDJ, KimWY, SalmelaMJ, EwersBE, WeinigC, KhanSL, SchaibleDL, McClungCR. Allelic polymorphism of GIGANTEA is responsible for naturally occurring variation in circadian period in Brassica rapa. Proc Natl Acad Sci U S A, 2015, 112: 3829-3834

[152] XieQ, WangP, LiuX, YuanL, WangL, ZhangC, LiY, XingH, ZhiL, YueZ, ZhaoC, McClungCR, XuX. LNK1 and LNK2 are transcriptional coactivators in the Arabidopsis circadian oscillator. Plant Cell, 2014, 26: 2843-2857

[153] XuG, JiangZ, WangH, LinR. The central circadian clock proteins CCA1 and LHY regulate iron homeostasis in Arabidopsis. J Integr Plant Biol, 2019, 61(2):168-181

[154] XuX, HottaCT, DoddAN, LoveJ, SharrockR, LeeYW, XieQ, JohnsonCH, WebbAA. Distinct light and clock modulation of cytosolic free Ca2+ oscillations and rhythmic CHLOROPHYLL a/B BINDING PROTEIN2 promoter activity in Arabidopsis. Plant Cell, 2007, 19(11):3474-3490

[155] XuX, XieQ, McClungCR. Robust circadian rhythms of gene expression in Brassica rapa tissue culture. Plant Physiol, 2010, 153: 841-850

[156] XuX, YuanL, XieQ. Circadian rhythm: phase response curve and light entrainment. Methods Mol Biol, 2022, 2398: 1-13

[157] Xu X, Yuan L, Yang X, Zhang X, Wang L, Xie Q (2022b) Circadian clock in plants: linking timing to fitness. J Integr Plant Biol. https://doi.org/10.1111/jipb.13230

[158] YanJ, LiS, KimYJ, ZengQ, RadziejwoskiA, WangL, NomuraY, NakagamiH, SomersDE. TOC1 clock protein phosphorylation controls complex formation with NF-YB/C to repress hypocotyl growth. EMBO J, 2021, 40: e108684

[159] YangM, HanX, YangJ, JiangY, HuY. The Arabidopsis circadian clock protein PRR5 interacts with and stimulates ABI5 to modulate abscisic acid signaling during seed germination. Plant Cell, 2021, 33: 3022-3041

[160] YangY, GuoY. Unraveling salt stress signaling in plants. J Integr Plant Biol, 2018, 60: 796-804

[161] YanovskyMJ, IzaguirreM, WagmaisterJA, GatzC, JacksonSD, ThomasB, CasalJJ. Phytochrome a resets the circadian clock and delays tuber formation under long days in potato. Plant J, 2000, 23: 223-232

[162] YuanL, HuY, LiS, XieQ, XuX. PRR9 and PRR7 negatively regulate the expression of EC components under warm temperature in roots. Plant Signal Behav, 2020, 16: 1855384

[163] YuanL, XieGZ, ZhangS, LiB, WangX, LiY, LiuT, XuX. GmLCLs negatively regulate ABA perception and signalling genes in soybean leaf dehydration response. Plant Cell Environ, 2021, 44: 412-424

[164] YuanL, YuY, LiuM, SongY, LiH, SunJ, WangQ, XieQ, WangL, XuX. BBX19 fine-tunes the circadian rhythm by interacting with PSEUDO-RESPONSE REGULATOR proteins to facilitate their repressive effect on morning-phased clock genes. Plant Cell, 2021, 33: 2602-2617

[165] ZagottaMT, HicksKA, JacobsCI, YoungJC, HangarterRP, Meeks-WagnerDR. The Arabidopsis ELF3 gene regulates vegetative photomorphogenesis and the photoperiodic induction of flowering. Plant J, 1996, 10(4):691-702

[166] ZhangC, GaoM, SeitzNC, AngelW, HallworthA, WiratanL, DarwishO, AlkharoufN, DawitT, LinD, EgoshiR, WangXP, McClungCR, LuH. LUX ARRHYTHMO mediates crosstalk between the circadian clock and defense in Arabidopsis. Nat Commun, 2019, 10: 2543

[167] ZhangC, XieQ, AndersonRG, NgG, SeitzNC, PetersonT, McClungCR, McDowellJM, KongD, KwakJ, LuH. Crosstalk between the circadian clock and innate immunity in Arabidopsis. PLoS Pathog, 2013, 9: e1003370

[168] ZhangLL, LiW, TianYY, DavisSJ, LiuJX. The E3 ligase XBAT35 mediates thermoresponsive hypocotyl growth by targeting ELF3 for degradation in Arabidopsis. J Integr Plant Biol, 2021, 63: 1097-1103

[169] ZhangLL, ShaoYJ, DingL, WangMJ, DavisSJ, LiuJX. XBAT31 regulates thermoresponsive hypocotyl growth through mediating degradation of the thermosensor ELF3 in Arabidopsis. Sci Adv, 2021, 7: eabf4427

[170] ZhangS, WuQR, LiuLL, ZhangHM, GaoJW, PeiZM. Osmotic stress alters circadian cytosolic ca(2+) oscillations and OSCA1 is required in circadian gated stress adaptation. Plant Signal Behav, 2020, 15(12):1836883

[171] ZhuJH, LeeBH, DellingerM, CuiXP, ZhangCQ, WuS, NothnagelEA, ZhuJK. A cellulose synthase-like protein is required for osmotic stress tolerance in Arabidopsis. Plant J, 2010, 63: 128-140

[172] ZhuJK. Abiotic stress signaling and responses in plants. Cell, 2016, 167: 313-324

[173] ZhuJY, OhE, WangT, WangZY. TOC1-PIF4 interaction mediates the circadian gating of thermoresponsive growth in Arabidopsis. Nat Commun, 2016, 7: 13692

[174] ZimmermanWF, PittendrighCS, PavlidisT. Temperature compensation of the circadian oscillation in Drosophila pseudoobscura and its entrainment by temperature cycles. J Insect Physiol, 1968, 14: 669-684

Funding

National Natural Science Foundation of China(32170259, 31670285); National key research and development program(2021YFA1300402)