Abstract
The circadian clock serves the fitness of higher plants by controlling various aspects of plant growth and development ranging from photosynthesis to flowering and defense mechanisms. The key components of the core oscillator mediate the circadian output through transcriptional or post-transcriptional mechanisms by phase-wise expression and repression of numerous genes. Senescence on the other hand is a tightly regulated developmental process that facilitates the remobilization of nutrients and leads to inevitable death of the plant in the end. Thus, senescence is critical for flowering, ripening of fruits, biomass production and the yield of crop plants. The circadian clock and senescence are tightly interwoven in many eukaryotes. However, in plants the intricacy of regulations by the circadian oscillator for triggering the onset or progress of senescence is not known in detail. Clock regulation during senescence is known through several cross-signaling networks, such as age-dependent, hormone-mediated and dark-induced. The present review aims to expound on the recent advances in understanding the cross-network regulations of the circadian clock during different types of senescence in plants.
Similar content being viewed by others
Abbreviations
- ET:
-
Ethylene
- CK:
-
Cytokinin
- Phy:
-
Phytochrome
- ROS:
-
Reactive oxygen species
- ABA:
-
Abscisic acid
- JA:
-
Jasmonic acid
- SA:
-
Salicylic Acid
References
Adams S, Manfield I, Stockley P, Carré IA (2015) Revised morning loops of the Arabidopsis circadian clock based on analyses of direct regulatory interactions. PLoS ONE 10:e0143943. https://doi.org/10.1371/journal.pone.0143943
Alabadi D, Oyama T, Yanovsky MJ, Harmon FG, Mas P, Kay SA (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293:880–883. https://doi.org/10.1126/science.1061320
Ay N, Janack B, Humbeck K (2014) Epigenetic control of plant senescence and linked processes. J Exp Bot 65(14):3875–3887. https://doi.org/10.1093/jxb/eru132
Belbin FE, Hall GJ, Jackson AB, Schanschieff FE, Archibald G, Formstone C, Dodd AN (2019) Plant circadian rhythms regulate the effectiveness of a glyphosate-based herbicide. Nat Commun 10:3704. https://doi.org/10.1038/s41467-019-11709-5
Bergonzi S, Albani MC, Loren V, van Themaat E, Nordström KJ, Wang R, Schneeberger K, Moerland PD, Coupland G (2013) Mechanisms of age-dependent response to winter temperature in perennial flowering of Arabis alpina. Science 340(6136):1094–1097. https://doi.org/10.1126/science.1234116
Breeze E, Harrison E, Page T, Warner N, Shen C, Zhang C, Buchanan-Wollaston V (2008) Transcriptional regulation of plant senescence: from functional genomics to systems biology. Plant Biol (Stuttg) 1:99–109. https://doi.org/10.1111/j.1438-8677.2008.00076.x
Cheong YH, Kim KN, Pandey GK, Gupta R, Grant JJ, Luan S (2003) CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell 15(8):1833–1845. https://doi.org/10.1105/tpc.012393
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
Cominelli E, Galbiati M, Tonelli C (2010) Transcription factors controlling stomatal movements and drought tolerance. Transcription 1(1):41–45. https://doi.org/10.4161/trns.1.1.12064
Edgar RS, Green EW, Zhao Y, van Ooijen G, Olmedo M, Qin X et al (2012) Peroxiredoxins are conserved markers of circadian rhythms. Nature 485:459–464. https://doi.org/10.1038/nature11088
Espinoza C, Degenkolbe T, Caldana C, Zuther E, Leisse A, Willmitzer L et al (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
Fornara F, Panigrahi KCS, Gissot L, Sauerbrunn N, Rühl M, Jarillo JA et al (2009) Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev Cell 17(1):75–86. https://doi.org/10.1016/j.devcel.2009.06.015
Fujiwara S, Nakagawa M, Kamada H, Mizoguchi T (2005) Circadian clock components in Arabidopsis III. LHY/CCA1/GI in regulating the floral integrator genes LFY/SOC1/FT to control flowering time and shoot architecture. Plant Biotechnol 22(4):327–331. https://doi.org/10.5511/plantbiotechnology.22.327
Fukushima A, Kusano M, Nakamichi N, Kobayashi M, Hayashi N, Mizuno T et al (2009) Impact of clock-associated Arabidopsis pseudo-response regulators in metabolic coordination. PNAS USA 106:7251–7256. https://doi.org/10.1073/pnas.0900952106
Goodspeed D, Liu JD, Chehab EW, Sheng Z, Francisco M, Kliebenstein DJ, Braam J (2013) Postharvest circadian entrainment enhances crop pest resistance and phytochemical cycling. Curr Biol 23:1235–1241. https://doi.org/10.1016/j.cub.2013.05.034
Hung FY, Chen FF, Li C, Chen C, Chen JH, Cui Y, Wu K (2019) LDL1/2-HDA6 Histone modification complex interacts with TOC1 and regulates the core circadian clock components in Arabidopsis. Front Plant Sci 10:233. https://doi.org/10.3389/fpls.2019.00233
Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290:344–347
Kamioka M, Takao S, Suzuki T, Taki K, Higashiyama T, Kinoshita T, Nakamichi N (2016) Direct repression of evening genes by CIRCADIAN CLOCK-ASSOCIATED1 in the Arabidopsis Circadian Clock. Plant Cell 28:696–711. https://doi.org/10.1105/tpc.15.00737
Keily J, Macgregor DR, Smith RW, Millar AJ, Halliday KJ, Penfield S (2013) Model selection reveals control of cold signaling by evening-phased components of the plant circadian clock. Plant J 76:247–257. https://doi.org/10.1111/tpj.12303
Kim WY, Ali Z, Park HJ, Park SJ, Cha JY, Perez-Hormaeche J et al (2013) Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis. Nat Commun 4:1352. https://doi.org/10.1038/ncomms2357
Kim J, Woo HR, Nam HG (2016) Toward systems understanding of leaf senescence: an integrated multi-omics perspective on leaf senescence research. Mole Plant 9:813–825. https://doi.org/10.1016/j.molp.2016.04.017
Kim J, Kim JH, Lyu JI, Woo HR, Lim PO (2018) New insights into the regulation of leaf senescence in Arabidopsis. J Exp Bot 69(4):787–799. https://doi.org/10.1093/jxb/erx287
Lai AG, Doherty CJ, Mueller-Roeber B, Kay SA, Schippers JH, Dijkwel PP (2012) Circadian clock-associated 1 regulates ROS homeostasis and oxidative stress responses. PNAS USA 109:17129–17134. https://doi.org/10.1073/pnas.1209148109
Lee CM, Li MW, Feke A, Liu W, Saffer AM, Gendron JM (2019) GIGANTEA recruits the UBP12 and UBP13 deubiquitylases to regulate accumulation of the ZTL photoreceptor complex. Nat Commun 10:3750. https://doi.org/10.1038/s41467-019-11769-7
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 Z, Zhao Y, Liu X, Peng J, Guo H, Luo J (2014) LSD 2.0: an update of the leaf senescence database. Nucleic Acids Res 42:D1200–D1205. https://doi.org/10.1093/nar/gkt1061
Lim PO, Nam HG (2005) The molecular and genetic control of leaf senescence and longevity in Arabidopsis. Curr Opin Dev Biol 67:49–83. https://doi.org/10.1016/S0070-2153(05)67002-0
Lim PO, Woo HR, Nam HG (2003) Molecular genetics of leaf senescence in Arabidopsis. Trends Plant Sci 8(6):272–278. https://doi.org/10.1016/S1360-1385(03)00103-1
Liu T, Carlsson J, Takeuchi T, Newton L, Farre EM (2013) Direct regulation of abiotic responses by the Arabidopsis circadian clock component PRR7. Plant J 76:101–114. https://doi.org/10.1111/tpj.12276
Lu SX, Knowles SM, Andronis C, Ong MS, Tobin EM (2009) CIRCADIAN CLOCK ASSOCIATED1 and LATE ELONGATED HYPOCOTYL function synergistically in the circadian clock of Arabidopsis. Plant Physiol 150:834–843. https://doi.org/10.1104/pp.108.133272
Martí Ruiz MC, Hubbard KE, Gardner MJ et al (2018) Circadian oscillations of cytosolic free calcium regulate the Arabidopsis circadian clock. Nat Plants 4:690–698. https://doi.org/10.1038/s41477-018-0224-8
McClung CR (2011) The genetics of plant clocks. Adv Genet 74:105–139. https://doi.org/10.1016/B978-0-12-387690-4.00004-0
Mir R, Hernandez ML, Abou-Mansour E, Martinez-Rivas JM, Mauch F, Metraux JP, Leon J (2013) Pathogen and Circadian Controlled 1 (PCC1) regulates polar lipid content, ABA-related responses, and pathogen defence in Arabidopsis thaliana. J Exp Bot 64:3385–3395. https://doi.org/10.1093/jxb/ert177
Miyazaki Y, Abe H, Takase T, Kobayashi M, Kiyosue T (2015) Overexpression of LOV KELCH PROTEIN 2 confers dehydration tolerance and is associated with enhanced expression of dehydration-inducible genes in Arabidopsis thaliana. Plant Cell Rep 34:843–852. https://doi.org/10.1007/s00299-015-1746-4
Nakamichi N, Kita M, Ito S, Yamashino T, Mizuno T (2005) PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol 46:686–698. https://doi.org/10.1093/pcp/pci086
Nusinow DA, Helfer A, Hamilton EE, King JJ, Imaizumi T, Schultz TF, Farre EM, Kay SA (2011) The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475:398. https://doi.org/10.1038/nature10182
Rauf M, Arif M, Dortay H, Matallana-Ramirez LP, Waters MT, NamH G et al (2013) ORE1 balances leaf senescence against maintenance by antagonizing G2-like-mediated transcription. EMBO Rep 14:382–388. https://doi.org/10.1038/embor.2013.24
Rawat R, Takahashi N, Hsu PY, Jones MA, Schwartz J, Salemi MR, Phinney BS, Harmer SL (2011) REVEILLE8 and PSEUDO-REPONSE REGULATOR5 form a negative feedback loop within the Arabidopsis circadian clock. PLoS Genet 7:e1001350. https://doi.org/10.1371/journal.pgen.1001350
Sakuraba Y, Bulbul S, Piao W, Choi G, Paek NC (2017) Arabidopsis early flowering3 increases salt tolerance by suppressing salt stress response pathways. Plant J 92:1106–1120. https://doi.org/10.1111/tpj.13747
Schippers JHM, Schmidt R, Wagstaff C, Jing HC (2015) Living to die and dying to live: the survival strategy behind leaf senescence. Plant Physiol 169(2):914–930. https://doi.org/10.1104/pp.15.00498
Shin J, Heidrich K, Sanchez-Villarreal A, Parker JE, Davis SJ (2012) TIME FOR COFFEE represses accumulation of the MYC2 transcription factor to provide time-of-day regulation of jasmonate signaling in Arabidopsis. Plant Cell 24:2470–2482. https://doi.org/10.1105/tpc.111.095430
Sierla M, Rahikainen M, Salojarvi J, Kangasjarvi J, Kangasjarvi S (2013) Apoplastic and chloroplastic redox signaling networks in plant stress responses. Antioxid Redox Signal 18:2220–2239. https://doi.org/10.1089/ars.2012.5016
Silva CS, Nayak A, Lai X, Hutin S, Hugouvieux V, Jung JH, López-Vidriero I, Franco-Zorrilla JM, Panigrahi K, Nanao MH, Wigge PA, Zubieta C (2020) Molecular mechanisms of evening complex activity in Arabidopsis. PNAS USA 117(12):6901–6909. https://doi.org/10.1073/pnas.1920972117
Song Y, Jiang YP, Kuai BK, Li L (2018) Circadian clock-associated 1 inhibits leaf senescence in Arabidopsis. Front Plant Sci 8:280. https://doi.org/10.3389/fpls.2018.00280
Sun Q, Wang S, Xu G, Kang X, Zhang M, Min N (2019) SHB1 and CCA1 interaction desensitizes light responses and enhances thermomorphogenesis. Nat Commun 10:3110. https://doi.org/10.1038/s41467-019-11071-6
Talla SK, Panigrahy M, Kappara N, Saivishnupriya P, Sarla N, Ramanan R (2016) Cytokinin delays dark-induced senescence in rice by maintaining the chlorophyll cycle and photosynthetic complexes. J Exp Bot 67(6):1839–1851. https://doi.org/10.1093/jxb/erv575
Wang J-W (2014) Regulation of flowering time by the miR156-mediated age pathway. J Exp Bot 65(17):4723–4730. https://doi.org/10.1093/jxb/eru246
Wang L, Fujiwara S, Somers DE (2010) PRR5 regulates phosphorylation, nuclear import and subnuclear localization of TOC1 in the Arabidopsis circadian clock. EMBO J29:1903–1915. https://doi.org/10.1038/emboj.2010.196
Weckwerth P, Ehlert B, Romeis T (2015) ZmCPK1, a calcium-dependent kinase member of the Zea mays CDK gene family, functions as a negative regulator in cold stress signaling. Plant Cell Environ 38(3):544–558. https://doi.org/10.1111/pce.12414
Woo HR, Kim HJ, Nam HG, Lim PO (2013) Plant leaf senescence and death: regulation by multiple layers of control and implications for aging in general. J Cell Sci 126:4823–4833. https://doi.org/10.1242/jcs.109116
Yuan P, Yang T, Poovaiah BW (2018) Calcium signaling-mediated plant response to cold stress. Int J Mol Sci 19(12):3896. https://doi.org/10.3390/ijms19123896
Zeng H, Xu L, Singh A, Wang H, Du L, Poovaiah BW (2015) Involvement of calmodulin and calmodulin-like proteins in plant responses to abiotic stresses. Front Plant Sci 6:600. https://doi.org/10.3389/fpls.2015.00600
Zhang K, Gan SS (2012) An abscisic acid-AtNAP transcription factor-SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves. Plant Physiol 158:961–969. https://doi.org/10.1104/pp.111.190876
Zhang C, Xie Q, Anderson RG, Ng G, Seitz NC, Peterson T, McClung CR et al (2013) Crosstalk between the circadian clock and innate immunity in Arabidopsis. PLoS Pathog 9:e1003370. https://doi.org/10.1371/journal.ppat.1003370
Zhang C, Gao M, Seitz NC, William A, Hallworth A, Wiratan L et al (2019) LUX ARRHYTHMO mediates crosstalk between the circadian clock and defense in Arabidopsis. Nat Commun 10:2543. https://doi.org/10.1038/s41467-019-10485-6
Zhang Y, Wang Y, Wei H, Li N, Tian W, Chong K, Wang L (2018) Circadian evening complex represses jasmonate-induced leaf senescence in Arabidopsis. Mol Plant 11:326–337
Acknowledgements
This work is supported by the Department of Science and Technology (DST), Science and Engineering Research Board (SERB), India, Young Scientist Start-up Research grant no. YSS/2015/000659, and DST, India, WOS-A Women Scientist grant no. SR/WOS-A/LS-369/2018 awarded to MP. We thank the President, SOA Deemed to Be University, for all support. This work was funded by the Department of biotechnology (DBT), Ministry of Science and Technology, India to KCSP (BT/PBA/MF2014).
Author information
Authors and Affiliations
Contributions
NM and MP wrote the MS and analyzed the data. KCP, RJ and LBS read and edited the MS, provided the infrastructural facility and funds. MP received grants for research.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflicts of interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Majeed, N., Panigrahi, K.C.S., Sukla, L.B. et al. Regulatory mechanisms across networks of the circadian clock and senescence pathways. J. Plant Biochem. Biotechnol. 29, 665–674 (2020). https://doi.org/10.1007/s13562-020-00612-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13562-020-00612-6