Abstract
The circadian clock is a cell autonomously and endogenously regulated biological timekeeper that detects changes in environmental stimuli and generates 24-h rhythms that are synched with day to day and periodic oscillations to govern many biological functions. Plant's circadian clocks enable them to anticipate environmental changes by modifying their physiological and biological traits to improve plant fitness. The internal circadian clock not only aids fitness but also allows the plant to time-gate the response to environmental stimuli. The latest evidence on the circadian clock suggests that the clock regulates/modulates the expression of abiotic stress-responsive pathways to improve tolerance to stresses without hampering plant growth. In turn, stress signaling also influences the activity of several clock components. This review emphasizes the interplay of the biological circadian clock with abiotic stress-responsive pathways (drought, heat, cold, and salt) for plant growth and survival as well as for stress resilience. A better comprehension of these mechanisms could aid in the development of genetic tools to improve breeding procedures and plant stress tolerance, thereby increasing crop yield and quality under changing ecological conditions.
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References
Adams S, Manfield I, Stockley P, Carre´ IA (2015) Revised morning loops of the Arabidopsis circadian clock based on analyses of direct regulatory interactions. PLoS One 10:e014394. https://doi.org/10.1371/journal.pone.0143943
Baek D, Kim WY, Cha JY, Park HJ, Shin G, Park J, Lim CJ, Chun HJ, Li N, Kim DH, Lee SY (2020) The GIGANTEA-ENHANCED EM LEVEL complex enhances drought tolerance via regulation of abscisic acid synthesis. Plant Physiol 184:443–458. https://doi.org/10.1104/pp.20.00779
Bhattacharya A, Khanale V, Char B (2017) Plant circadian rhythm in stress signaling. Indian J Plant Physiol 22:147–155. https://doi.org/10.1007/s40502-017-0299-7
Bieniawska Z, Espinoza C, Schlereth A, Sulpice R, Hincha DK, Hannah MA (2008) Disruption of the Arabidopsis circadian clock is responsible for extensive variation in the cold-responsive transcriptome. Plant Physiol 147:263–279. https://doi.org/10.1104/pp.108.118059
Blair EJ, Bonnot T, Hummel M, Hay E, Marzolino JM, Quijada IA, Nagel DH (2019) Contribution of time of day and the circadian clock to the heat stress responsive transcriptome in Arabidopsis. Sci Rep 9:1–12. https://doi.org/10.1038/s41598-019-41234-w
Cao S, Ye M, Jiang S (2005) Involvement of GIGANTEA gene in the regulation of the cold stress response in Arabidopsis. Plant Cell Rep 24:683–690. https://doi.org/10.1007/s00299-005-0061-x
Cao S, Jiang L, Song S, Jing R, Xu G (2006) AtGRP7 is involved in the regulation of abscisic acid and stress responses in Arabidopsis. Cell Mol Biol Lett 11:526–535. https://doi.org/10.2478/s11658-006-0042-2
Cao SQ, Song YQ, Su L (2007) Freezing sensitivity in the gigantea mutant of Arabidopsis is associated with sugar deficiency. Biol Plant 51:359–362. https://doi.org/10.1007/s10535-007-0073-1
Chen S, Huang HA, Chen JH, Fu CC, Zhan PL, Ke SW, Zhang XQ, Zhong TX, Xie XM (2020) SgRVE6, a LHY-CCA1-like transcription factor from fine-stem stylo, upregulates NB-LRR gene expression and enhances cold tolerance in tobacco. Front Plant Sci 11:1276. https://doi.org/10.3389/fpls.2020.01276
Chow BY, Sanchez SE, Breton G, Pruneda-Paz JL, Krogan NT, Kay SA (2014) Transcriptional regulation of LUX by CBF1 mediates cold input to the circadian clock in Arabidopsis. Curr Biol 24:1518–1524. https://doi.org/10.1016/j.cub.2014.05.029
Covington MF, Harmer SL (2007) The circadian clock regulates auxin signaling and responses in Arabidopsis. PLoS Biol 5:e222. https://doi.org/10.1371/journal.pbio.0050222
Covington M, Maloof J, Straume M, Kay S, Harmer S (2008) Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol 9:R130. https://doi.org/10.1186/gb-2008-9-8-r130
Coyne K, Davis MM, Mizoguchi T, Hayama R (2019) Temporal restriction of salt inducibility in expression of salinity-stress related gene by the circadian clock in Solanum lycopersicum. Plant Biotechnol J 36:195–200. https://doi.org/10.5511/plantbiotechnology.19.0703a
Creux N, Harmer S (2019a) Circadian rhythms in plants. Cold Spring Harb Perspect Biol 11(9):a034611. https://doi.org/10.1101/cshperspect.a034611
Creux N, Harmer S (2019b) Circadian rhythms in plants. Cold Spring Harb Perspect Biol 11:a034611. https://doi.org/10.1101/cshperspect.a034611
Dai A (2013) Increasing drought under global warming in observations and models. Nat Clim Change 3:52–58. https://doi.org/10.1038/nclimate1633
de Leone MJ, Hernando CE, Mora-García S, Yanovsky MJ (2020) It’s a matter of time: the role of transcriptional regulation in the circadian clock-pathogen crosstalk in plants. Transcription 11:100–116. https://doi.org/10.1080/21541264.2020.1820300
Dodd AN, Gardner MJ, Hotta CT, Hubbard KE, Dalchau N, Love J, Assie JM, Robertson FC, Jakobsen MK, Gonçalves J, Sanders D (2007) The Arabidopsis circadian clock incorporates a cADPR-based feedback loop. Science 318:1789–1792. https://doi.org/10.1126/science.1146757
Dong MA, Farré EM, Thomashow MF (2011) Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis. Proceed Natl Acad Sci 108:7241–7246. https://doi.org/10.1073/pnas.1103741108
Espinoza C, Degenkolbe T, Caldana C, Zuther E, Leisse A, Willmitzer L, Hincha DK, Hannah MA (2010) Interaction with diurnal and circadian regulation results in dynamic metabolic and transcriptional changes during cold acclimation in Arabidopsis. PLoS One 5:e14101. https://doi.org/10.1371/journal.pone.0014101
Filichkin SA, Breton G, Priest HD, Dharmawardhana P, Jaiswal P, Fox SE, Michael TP, Chory J, Kay SA, Mockler TC (2011) Global profiling of rice and poplar transcriptomes highlights key conserved circadian-controlled pathways and cis-regulatory modules. PLoS One 6:e16907. https://doi.org/10.1371/journal.pone.0016907
Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Morris B, Coupland G, Putterill J (1999) GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J 18:4679–4688. https://doi.org/10.1093/emboj/18.17.4679
Fowler SG, Cook D, Thomashow MF (2005) Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol 137:961–968. https://doi.org/10.1104/pp.104.058354
Fukushima A, Kusano M, Nakamichi N, Kobayashi M, Hayashi N, Sakakibara H, Mizuno T, Saito K (2009) Impact of clock-associated Arabidopsis pseudo-response regulators in metabolic coordination. Proc Natl Acad Sci 106:7251–7256. https://doi.org/10.1073/pnas.0900952106
Gierczik K, Novák A, Ahres M, Székely A, Soltész A, Boldizsár Á, Gulyás Z, Kalapos B, Monostori I, Kozma-Bognár L, Galiba G (2017) Circadian and light regulated expression of CBFs and their upstream signalling genes in barley. Int J Mol Sci 18:1828. https://doi.org/10.3390/ijms18081828
Greenham K, McClung CR (2015) Integrating circadian dynamics with physiological processes in plants. Nat Rev Genet 16:598–610. https://doi.org/10.1038/nrg3976
Grundy J, Stoker C, Carré IA (2015) Circadian regulation of abiotic stress tolerance in plants. Front Plant Sci 6:648. https://doi.org/10.3389/fpls.2015.00648
Guadagno CR, Ewers BE, Weinig C (2018) Circadian rhythms and redox state in plants: till stress do us part. Front Plant Sci 9:247. https://doi.org/10.3389/fpls.2018.00247
Hamilton EE, Kay SA (2008) SnapShot: circadian clock proteins. Cell 135:368–368
Hoffman DE, Jonsson P, Bylesjö MAX, Trygg J, Antti H, Eriksson ME, Moritz T (2010) Changes in diurnal patterns within the Populus transcriptome and metabolome in response to photoperiod variation. Plant Cell Environ 33:1298–1313. https://doi.org/10.1111/j.1365-3040.2010.02148.x
Hsu PY, Harmer SL (2014) Wheels within wheels: the plant circadian system. Trends Plant Sci 19:240–249. https://doi.org/10.1016/j.tplants.2013.11.007
James AB, Syed NH, Bordage S, Marshall J, Nimmo GA, Jenkins GI, Herzyk P, Brown JW, Nimmo HG (2012) Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes. Plant Cell 24:961–981. https://doi.org/10.1105/tpc.111.093948
Jarvis PG (1976) The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field. Phil Trans R Soc Lond B Biol Sci 273:593–610. https://doi.org/10.1098/rstb.1976.0035
Keily J, MacGregor DR, Smith RW, Millar AJ, Halliday KJ, Penfield S (2013) Model selection reveals control of cold signalling by evening-phased components of the plant circadian clock. Plant J 76:247–257. https://doi.org/10.1111/tpj.12303
Khan S, Rowe SC, Harmon FG (2010) Coordination of the maize transcriptome by a conserved circadian clock. BMC Plant Biol 10:1–15. https://doi.org/10.1186/1471-2229-10-126
Kidokoro S, Maruyama K, Nakashima K, Imura Y, Narusaka Y, Shinwari ZK, Osakabe Y, Fujita Y, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2009) The phytochrome-interacting factor PIF7 negatively regulates DREB1 expression under circadian control in Arabidopsis. Plant Physiol 151:2046–2057. https://doi.org/10.1104/pp.109.147033
Kidokoro S, Hayashi K, Haraguchi H, Ishikawa T, Soma F, Konoura I, Toda S, Mizoi J, Suzuki T, Shinozaki K, Yamaguchi-Shinozaki K (2021) Posttranslational regulation of multiple clock-related transcription factors triggers cold-inducible gene expression in Arabidopsis. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.2021048118
Kim JS, Jung HJ, Lee HJ, Kim KA, Goh CH, Woo Y, Oh SH, Han YS, Kang H (2008) Glycine-rich RNA-binding protein7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. Plant J 55:455–466. https://doi.org/10.1111/j.1365-313X.2008.03518.x
Kim WY, Ali Z, Park HJ, Park SJ, Cha JY, Perez-Hormaeche J, Quintero FJ, Shin G, Kim MR, Qiang Z, Ning L (2013) Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis. Nat Commun 4:1–13
Kim JA, Jung HE, Hong JK, Hermand V, McClung CR, Lee YH, Kim JY, Lee SI, Jeong MJ, Kim J, Yun D (2016) Reduction of GIGANTEA expression in transgenic Brassica rapa enhances salt tolerance. Plant Cell Rep 35:1943–1954. https://doi.org/10.1007/s00299-016-2008-9
Kolmos E, Chow BY, Pruneda-Paz JL, Kay SA (2014) HsfB2b-mediated repression of PRR7 directs abiotic stress responses of the circadian clock. Proceed Natl Acad Sci 111:16172–16177. https://doi.org/10.1073/pnas.1418483111
Kusakina J, Gould PD, Hall A (2014) A fast circadian clock at high temperatures is a conserved feature across A rabidopsis accessions and likely to be important for vegetative yield. Plant Cell Environ 37:327–340. https://doi.org/10.1111/pce.12152
Landgraf D, McCarthy MJ, Welsh DK (2014) The role of the circadian clock in animal models of mood disorders. Behav Neurosci 128:344. https://doi.org/10.1037/a0036029
Lee CM, Thomashow MF (2012) Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance in Arabidopsis thaliana. Proc Natl Acad Sci 109:15054–15059. https://doi.org/10.1073/pnas.1211295109
Lee HG, Mas P, Seo PJ (2016) MYB96 shapes the circadian gating of ABA signaling in Arabidopsis. Sci Rep 6:1–11. https://doi.org/10.1038/srep17754
Legnaioli T, Cuevas J, Mas P (2009) TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought. EMBO J 28:3745–3757. https://doi.org/10.1038/emboj.2009.297
Li B, Gao Z, Liu X, Sun D, Tang W (2019) 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 31:2353–2369. https://doi.org/10.1105/tpc.19.00519
Lin J, Yu Z, Ye C, Hong L, Chu Y, Shen Y, Li QQ (2021) Alternative polyadenylated mRNAs behave as asynchronous rhythmic transcription in Arabidopsis. RNA Biol. https://doi.org/10.1080/15476286.2021.1933732
Liu T, Carlsson J, Takeuchi T, Newton L, Farre EM (2013) Direct regulation of abiotic responses by the A rabidopsis circadian clock component PRR 7. Plant J 76:101–114. https://doi.org/10.1111/tpj.12276
Lu H, McClung CR, Zhang C (2017) Tick tock: circadian regulation of plant innate immunity. Annu Rev Phytopathol 55:287–311. https://doi.org/10.1146/annurev-phyto-080516-035451
Lu X, Song S, Xiao Y, Fan F, Zhou Y, Jia G, Tang W, Peng J (2021) Circadian clock-coordinated response to chilling stress in rice. Environ Exp Bot 185:104398. https://doi.org/10.1016/j.envexpbot.2021.104398
Marcolino-Gomes J, Rodrigues FA, Fuganti-Pagliarini R, Bendix C, Nakayama TJ, Celaya B, Molinari HBC, de Oliveira MCN, Harmon FG, Nepomuceno A (2014) Diurnal oscillations of soybean circadian clock and drought responsive genes. PLoS One 9:e86402
Melcher K, Ng LM, Zhou XE, Soon FF, Xu Y, Suino-Powell KM, Park SY, Weiner JJ, Fujii H, Chinnusamy V, Kovach A (2009) A gate–latch–lock mechanism for hormone signalling by abscisic acid receptors. Nature 462:602–608. https://doi.org/10.1038/nature08613
Michael TP, Mockler TC, Breton G, McEntee C, Byer A, Trout JD, Hazen SP, Shen R, Priest HD, Sullivan CM, Givan SA (2008) Network discovery pipeline elucidates conserved time-of-day–specific cis-regulatory modules. PLoS Genet 4:e14. https://doi.org/10.1371/journal.pgen.0040014
Mishra P, Panigrahi KC (2015) GIGANTEA–an emerging story. Front Plant Sci 6:8. https://doi.org/10.3389/fpls.2015.00008
Mizuno T, Yamashino T (2008) 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 49:481–487
Mockler TC, Michael TP, Priest HD, Shen R, Sullivan CM, Givan SA, McEntee C, Kay SA, Chory J (2007) The DIURNAL project: DIURNAL and circadian expression profiling, model-based pattern matching, and promoter analysis. Cold Spring Harbor Symposia Quantit Biol 72:353–363. https://doi.org/10.1101/sqb.2007.72.006
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Nagel DH, Pruneda-Paz JL, Kay SA (2014) FBH1 affects warm temperature responses in the Arabidopsis circadian clock. Proc Natl Acad Sci 111:14595–14600. https://doi.org/10.1073/pnas.1416666111
Nagel DH, Doherty CJ, Pruneda-Paz JL, Schmitz RJ, Ecker JR, Kay SA (2015) Genome-wide identification of CCA1 targets uncovers an expanded clock network in Arabidopsis. Proc Natl Acad Sci 112:E4802–E4810. https://doi.org/10.1073/pnas.1513609112
Nakamichi N, Kusano M, Fukushima A, Kita M, Ito S, Yamashino T, Saito K, Sakakibara H, Mizuno T (2009) 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 50:447–462. https://doi.org/10.1093/pcp/pcp004
Nakamichi N, Kiba T, Henriques R, Mizuno T, Chua NH, Sakakibara H (2010) Pseudo-response regulators 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell 22:594–605. https://doi.org/10.1105/tpc.109.072892
Nakashima A, Chen L, Thao NP, Fujiwara M, Wong HL, Kuwano M, Umemura K, Shirasu K, Kawasaki T, Shimamoto K (2008) RACK1 functions in rice innate immunity by interacting with the Rac1 immune complex. Plant Cell 20:2265–2279. https://doi.org/10.1105/tpc.107.054395
Nohales MA, Kay SA (2016) Molecular mechanisms at the core of the plant circadian oscillator. Nat Struct Mol Biol 23:1061. https://doi.org/10.1038/nsmb.3327
Nolte C, Staiger D (2015) RNA around the clock. Front Plant Sci 6:311. https://doi.org/10.3389/fpls.2015.00311
Park HJ, Kim WY, Yun DJ (2013) A role for GIGANTEA: keeping the balance between flowering and salinity stress tolerance. Plant Signal Behav 8:e24820. https://doi.org/10.4161/psb.24820
Park HJ, Qiang Z, Kim WY, Yun DJ (2016) Diurnal and circadian regulation of salt tolerance in Arabidopsis. J Plant Biol 59:569–578. https://doi.org/10.1007/s12374-016-0317-8
Perez-Santángelo S, Mancini E, Francey LJ, Schlaen RG, Chernomoretz A, Hogenesch JB, Yanovsky MJ (2014) Role for LSM genes in the regulation of circadian rhythms. Proceed Natl Acad Sci 111:15166–15171. https://doi.org/10.1073/pnas.1409791111
Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci 99:8436–8441. https://doi.org/10.1073/pnas.122224699
Robertson FC, Skeffington AW, Gardner MJ, Webb AA (2009) Interactions between circadian and hormonal signalling in plants. Plant Mol Biol 69:419. https://doi.org/10.1007/s11103-008-9407-4
Rodrigues FA, Fuganti-Pagliarini R, Marcolino-Gomes J, Nakayama TJ, Molinari HBC, Lobo FP, Harmon FG, Nepomuceno AL (2015) Daytime soybean transcriptome fluctuations during water deficit stress. BMC Genom 16:1–19. https://doi.org/10.1186/s12864-015-1731-x
Ruan SL, Ma HS, Wang SH, Fu YP, Xin Y, Liu WZ, Wang F, Tong JX, Wang SZ, Chen HZ (2011) Proteomic identification of OsCYP2, a rice cyclophilin that confers salt tolerance in rice (Oryza sativa L.) seedlings when overexpressed. BMC Plant Biol 11:1–15. https://doi.org/10.1186/1471-2229-11-34
Ruelland E, Vaultier MN, Zachowski A, Hurry V (2009) Cold signalling and cold acclimation in plants. Adv Bot Res 49:35–150. https://doi.org/10.1016/S0065-2296(08)00602-2
Rugnone ML, Faigo´nSoverna A, Sanchez SE, Schlaen RG, Hernando CE, Seymour DK, Mancini E, Chernomoretz A, Weigel D, Ma´s P et al (2013) LNK genes integrate light and clock signaling networks at the core of the Arabidopsis oscillator. Proc Natl Acad Sci 110:12120–12125. https://doi.org/10.1073/pnas.1302170110
Salomé PA, Weigel D, McClung CR (2010) The role of the Arabidopsis morning loop components CCA1, LHY, PRR7, and PRR9 in temperature compensation. Plant Cell 22:3650–3661. https://doi.org/10.1105/tpc.110.079087
Sanchez SE, Kay SA (2016) The plant circadian clock: from a simple timekeeper to a complex developmental manager. Cold Spring Harb Perspect Biol 8:a027748. https://doi.org/10.1101/cshperspect.a027748
Sanchez-Villarreal A, Shin J, Bujdoso N, Obata T, Neumann U, Du SX, Ding Z, Shindo DSJ, Schmelzer E, Sulpice R (2013) TIME FOR COFFEE is an essential component in the maintenance of metabolic homeostasis in Arabidopsis thaliana. Plant J 76:188–200. https://doi.org/10.1111/tpj.12292
Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys ActaBBA-Gene Regul Mech 1819:104–119. https://doi.org/10.1016/j.bbagrm.2011.10.002
Seo PJ, Mas P (2014) Multiple layers of posttranslational regulation refine circadian clock activity in Arabidopsis. Plant Cell 26:79–87. https://doi.org/10.1105/tpc.113.119842
Seo PJ, Mas P (2015) STRESSing the role of the plant circadian clock. Trends Plant Sci 20:230–237. https://doi.org/10.1016/j.tplants.2015.01.001
Seo PJ, Park MJ, Lim MH, Kim SG, Lee M, Baldwin IT, Park CM (2012) A self-regulatory circuit of CIRCADIAN CLOCK-ASSOCIATED1 underlies the circadian clock regulation of temperature responses in Arabidopsis. Plant Cell 24:2427–2442. https://doi.org/10.1105/tpc.112.098723
Sharma M, Bhatt D (2015) The circadian clock and defencesignalling in plants. Mol Plant Pathol 16:210–218. https://doi.org/10.1111/mpp.12178
Sharma A, Wai CM, Ming R, Yu Q (2017) Diurnal cycling transcription factors of pineapple revealed by genome-wide annotation and global transcriptomic analysis. Genome Boil Evol 9:2170–2190. https://doi.org/10.1093/gbe/evx161
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227. https://doi.org/10.1093/jxb/erl164
Smallwood M, Bowles DJ (2002) Plants in a cold climate. Philosophical transactions of the royal society of London. Series B Biol Sci 357(1423):831–847. https://doi.org/10.1098/rstb.2002.1073
Song H, Yi H, Han CT, Park JI, Hur Y (2018) Allelic variation in Brassica oleracea circadian clock associated 1 (BoCCA1) is associated with freezing tolerance. Hortic Environ Biotechnol 59:423–434. https://doi.org/10.1007/s13580-018-0045-8
Soni P, Kumar G, Soda N, Singla-Pareek SL, Pareek A (2013) Salt overly sensitive pathway members are influenced by diurnal rhythm in rice. Plant Signal Behav 8:e24738. https://doi.org/10.4161/psb.24738
Steed G, Ramirez DC, Hannah MA, Webb AA (2021) Chronoculture, harnessing the circadian clock to improve crop yield and sustainability. Science. https://doi.org/10.1126/science.abc9141
Syed NH, Prince SJ, Mutava RN, Patil G, Li S, Chen W, Babu V, Joshi T, Khan S, Nguyen HT (2015) Core clock, SUB1, and ABAR genes mediate flooding and drought responses via alternative splicing in soybean. J Exp Bot 66:7129–7149. https://doi.org/10.1093/jxb/erv407
Thakare D, Kumudini S, Dinkins RD (2010) Expression of flowering-time genes in soybean E1 near-isogenic lines under short and long day conditions. Planta 231:951–963. https://doi.org/10.1007/s00425-010-1100-6
Thomashow MF (2001) So what’s new in the field of plant cold acclimation? Lots! Plant Physiol 125:89–93. https://doi.org/10.1104/pp.125.1.89
Wang X, Wu F, Xie Q, Wang H, Wang Y, Yue Y, Gahura O, Ma S, Liu L, Cao Y, Jiao Y (2012) SKIP is a component of the spliceosome linking alternative splicing and the circadian clock in Arabidopsis. Plant Cell 24:3278–3295. https://doi.org/10.1105/tpc.112.100081
Wang J, Du Z, Huo X, Zhou J, Chen Y, Zhang J, Pan A, Wang X, Wang F, Zhang J (2020a) Genome-wide analysis of PRR gene family uncovers their roles in circadian rhythmic changes and response to drought stress in Gossypium hirsutum L. PeerJ 8:e9936. https://doi.org/10.7717/peerj.9936
Wang K, Bu T, Cheng Q, Dong L, Su T, Chen Z, Kong F, Gong Z, Liu B, Li M (2020b) Two homologous LHY pairs negatively control soybean drought tolerance by repressing the abscisic acid responses. New Phytol. https://doi.org/10.1111/nph.17019
Wei H, Wang X, HeY XuH, Wang L (2021) Clock component OsPRR73 positively regulates rice salt tolerance by modulating OsHKT2; 1-mediated sodium homeostasis. Embo 40:105086
Xie Q, Wang P, Liu X, Yuan L, Wang L, Zhang C, Li Y, Xing H, Zhi L, Yue Z et al (2014) LNK1 and LNK2 are transcriptional coactivators in the Arabidopsis circadian oscillator. Plant Cell 26:2843–2857. https://doi.org/10.1105/tpc.114.126573
Xie Q, Lou P, Hermand V, Aman R, Park HJ, Yun DJ, Kim WY, Salmela MJ, Ewers BE, Weinig C, Khan SL, McClung CR (2015) Allelic polymorphism of GIGANTEA is responsible for naturally occurring variation in circadian period in Brassica rapa. Proceed Natl Acad Sci 112:3829–3834. https://doi.org/10.1073/pnas.1421803112
Yang Z, Kim H, Ali A, Zheng Z, Zhang K (2017) Interaction between stress responses and circadian metabolism in metabolic disease. Liver Res 1:156–162. https://doi.org/10.1016/j.livres.2017.11.002
Zdepski A, Wang W, Priest HD, Ali F, Alam M, Mockler TC, Michael TP (2008) Conserved daily transcriptional programs in Carica papaya. Trop Plant Biol 1:236–245. https://doi.org/10.1007/s12042-008-9020-3
Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (2009) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J Exp Bot 60:3781–3796. https://doi.org/10.1093/jxb/erp214
Zhang D, Wang Y, Shen J, Yin J, Li D, Gao Y, Xu W, Liang J (2018) OsRACK1A, encodes a circadian clock-regulated WD40 protein, negatively affect salt tolerance in rice. Rice 11:1–15. https://doi.org/10.1186/s12284-018-0232-3
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PK and AD conceived the idea; PK, MS, and MI designed the article; PK, MS, and MI mined the literature and wrote the draft manuscript; AK, PK, MI, and AD reviewed and edited the manuscript. All the authors have read and approved the manuscript.
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Sharma, M., Irfan, M., Kumar, A. et al. Recent Insights into Plant Circadian Clock Response Against Abiotic Stress. J Plant Growth Regul 41, 3530–3543 (2022). https://doi.org/10.1007/s00344-021-10531-y
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DOI: https://doi.org/10.1007/s00344-021-10531-y