Skip to main content
Log in

Environment-mediated mutagenetic interference on genetic stabilization and circadian rhythm in plants

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Many mortal organisms on this planet have developed the potential to merge all internal as well as external environmental cues to regulate various processes running inside organisms and in turn make them adaptive to the environment through the circadian clock. This moving rotator controls processes like activation of hormonal, metabolic, or defense pathways, initiation of flowering at an accurate period, and developmental processes in plants to ensure their stability in the environment. All these processes that are under the control of this rotating wheel can be changed either by external environmental factors or by an unpredictable phenomenon called mutation that can be generated by either physical mutagens, chemical mutagens, or by internal genetic interruption during metabolic processes, which alters normal functionality of organisms like innate immune responses, entrainment of the clock, biomass reduction, chlorophyll formation, and hormonal signaling, despite its fewer positive roles in plants like changing plant type, loss of vernalization treatment to make them survivable in different latitudes, and defense responses during stress. In addition, with mutation, overexpression of gene components sometimes supresses mutation effect and promote normal circadian genes abundance in the cell, while sometimes it affects circadian functionality by generating arrhythmicity and shows that not only mutation but overexpression also effects normal functional activities of plant. Therefore, this review mainly summarizes the role of each circadian clock genes in regulating rhythmicity, and shows that how circadian outputs are controlled by mutations as well as overexpression phenomenon.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Availability of data and materials

Data generated during the study are subject to data sharing mandate and available in a public repository that does not issue datasets with DOI.

References

  1. Sanchez A, Shin J, Davis SJ (2011) Abiotic stress and the plant circadian clock. Plant Signal Behav 6:223–231. https://doi.org/10.4161/psb.6.2.14893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Butt GR, Qayyum ZA, Jones MA (2020) Plant defence mechanisms are modulated by the circadian system. Biology 9:454. https://doi.org/10.3390/biology9120454

    Article  CAS  PubMed Central  Google Scholar 

  3. Srivastava D, Shamim M, Kumar M, Mishra A, Maurya R, Sharma D, Pandey P, Singh K (2019) Role of circadian rhythm in plant system: an update from development to stress response. Environ Exp Bot 162:256–271. https://doi.org/10.1016/j.envexpbot.2019.02.025

    Article  Google Scholar 

  4. Dunlap JC (1999) Molecular bases for circadian clocks. Cell 96:271–290. https://doi.org/10.1016/S0092-8674(00)80566-8

    Article  CAS  PubMed  Google Scholar 

  5. Millar AJ, Kay SA (1991) Circadian control of cab gene transcription and mRNA accumulation in Arabidopsis. Plant Cell 3:541–550. https://doi.org/10.1105/tpc.3.5.541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Boikoglou E, Davis SJ (2009) Signaling in the circadian clock. Signaling in plants. Springer, Berlin, pp 261–285. https://doi.org/10.1007/978-3-540-89228-1_13

    Chapter  Google Scholar 

  7. Harmer SL (2009) The circadian system in higher plants. Annu Rev Plant Biol 60:357–377. https://doi.org/10.1146/annurev.arplant.043008.092054

    Article  CAS  PubMed  Google Scholar 

  8. Salome PA, McClung CR (2004) The Arabidopsis thaliana clock. J Biol Rhythms 19:425–435. https://doi.org/10.1177/0748730404268112

    Article  CAS  PubMed  Google Scholar 

  9. Worland A, Börner A, Korzun V, Li W, Petrovic S, Sayers E (1998) The influence of photoperiod genes on the adaptability of European winter wheats. Euphytica 100:385–394

    Article  CAS  Google Scholar 

  10. Jones H, Leigh FJ, Mackay I, Bower MA, Smith LM, Charles MP, Jones G, Jones MK, Brown TA, Powell W (2008) Population-based resequencing reveals that the flowering time adaptation of cultivated barley originated east of the Fertile Crescent. Mol Biol Evol 25:2211–2219. https://doi.org/10.1093/molbev/msn167

    Article  CAS  PubMed  Google Scholar 

  11. Yakir E, Hilman D, Harir Y, Green RM (2007) Regulation of output from the plant circadian clock. FEBS J 274:335–345. https://doi.org/10.1111/j.1742-4658.2006.05616.x

    Article  CAS  PubMed  Google Scholar 

  12. Robertson MC (2006) Plant circadian rhythms. Plant Cell 18:792–803

    Article  Google Scholar 

  13. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Covington MF, Maloof JN, Straume M, Kay SA, Harmer SL (2008) Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol 9:1–18. https://doi.org/10.1186/gb-2008-9-8-r130

    Article  CAS  Google Scholar 

  15. Goodspeed D, Chehab EW, Min-Venditti A, Braam J, Covington MF (2012) Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior. Proc Natl Acad Sci 109:4674–4677. https://doi.org/10.4161/psb.23123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Wang W, Barnaby JY, Tada Y, Li H, Tör M, Caldelari D, Lee D-u, Fu X-D, Dong X (2011) Timing of plant immune responses by a central circadian regulator. Nature 470:110–114

    Article  CAS  Google Scholar 

  17. Piechulla B (1993) ‘Circadian clock’directs the expression of plant genes. Plant Mol Biol 22:533–542

    Article  CAS  Google Scholar 

  18. Chaves I, Pokorny R, Byrdin M, Hoang N, Ritz T, Brettel K, Essen L-O, van der Horst GT, Batschauer A, Ahmad M (2011) The cryptochromes: blue light photoreceptors in plants and animals. Annu Rev Plant Biol 62:335–364. https://doi.org/10.1146/annurev-arplant-042110-103759

    Article  CAS  PubMed  Google Scholar 

  19. Liu B, Yang Z, Gomez A, Liu B, Lin C, Oka Y (2016) Signaling mechanisms of plant cryptochromes in Arabidopsis thaliana. J Plant Res 129:137–148. https://doi.org/10.1007/s10265-015-0782-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Millar A, Straum M, Chory J, Chua N, Kay S (1995) Phytochrome and blue responsive photoreceptors regulate circadian period in Arabidopsis thaliana. Science 267:1163–1166. https://doi.org/10.1126/science.7855596

    Article  CAS  PubMed  Google Scholar 

  21. Hicks K, Millar A, Carre I, Somers D, Straume M, Meeks-Wagner D, Kay S (1996) Conditional circadian dysfunction in the early-flowering 3 mutant of Arabidopsis. Science 274:790–792. https://doi.org/10.1126/science.274.5288.790

    Article  CAS  PubMed  Google Scholar 

  22. Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13:627–639. https://doi.org/10.1038/nrg3291

    Article  CAS  PubMed  Google Scholar 

  23. Michael TP, Mockler TC, Breton G, McEntee C, Byer A, Trout JD, Hazen SP, Shen R, Priest HD, Sullivan CM (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Hakeem KR, Ahmad P, Ozturk M (2013) Crop improvement: new approaches and modern techniques. Springer Science & Business Media, Boston

    Book  Google Scholar 

  25. Rhee SY, Beavis W, Berardini TZ, Chen G, Dixon D, Doyle A, Garcia-Hernandez M, Huala E, Lander G, Montoya M (2003) The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Res 31:224–228. https://doi.org/10.1093/nar/gkg076

    Article  CAS  PubMed  Google Scholar 

  26. Locke JC, Kozma-Bognár L, Gould PD, Fehér B, Kevei E, Nagy F, Turner MS, Hall A, Millar AJ (2006) Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Mol Syst Biol 2:59. https://doi.org/10.1038/msb4100102

    Article  PubMed  PubMed Central  Google Scholar 

  27. Zeilinger MN, Farré EM, Taylor SR, Kay SA, Doyle FJ III (2006) A novel computational model of the circadian clock in Arabidopsis that incorporates PRR7 and PRR9. Mol Syst Biol 2:58. https://doi.org/10.1038/msb4100101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Young MW, Kay SA (2001) Time zones: comparative genetics of circadian clocks. Nat Rev Genet 2:702–715. https://doi.org/10.1038/35088576

    Article  CAS  PubMed  Google Scholar 

  29. Dunlap JC, Loros JJ (2004) The Neurospora circadian system. J Biol Rhythms 19:414–424. https://doi.org/10.1177/0748730404269116

    Article  CAS  PubMed  Google Scholar 

  30. Nohales MA, Kay SA (2016) Molecular mechanisms at the core of the plant circadian oscillator. Nat Struct Mol Biol 23:1061–1069

    Article  CAS  Google Scholar 

  31. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Rugnone ML, Soverna AF, Sanchez SE, Schlaen RG, Hernando CE, Seymour DK, Mancini E, Chernomoretz A, Weigel D, Más P (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/10.1105/tpc.109.069922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Wu J-F, Tsai H-L, Joanito I, Wu Y-C, Chang C-W, Li Y-H, Wang Y, Hong JC, Chu J-W, Hsu C-P (2016) LWD–TCP complex activates the morning gene CCA1 in Arabidopsis. Nat Commun 7:1–10. https://doi.org/10.1038/ncomms13181

    Article  CAS  Google Scholar 

  34. Pomerening JR, Sontag ED, Ferrell JE (2003) Building a cell cycle oscillator: hysteresis and bistability in the activation of Cdc2. Nat Cell Biol 5:346–351. https://doi.org/10.1007/bf00015982

    Article  CAS  PubMed  Google Scholar 

  35. Ozbudak EM, Thattai M, Lim HN, Shraiman BI, Van Oudenaarden A (2004) Multistability in the lactose utilization network of Escherichia coli. Nature 427:737–740. https://doi.org/10.1038/nature02298

    Article  CAS  PubMed  Google Scholar 

  36. Ferrell JE Jr, Tsai TY-C, Yang Q (2011) Modeling the cell cycle: why do certain circuits oscillate? Cell 144:874–885. https://doi.org/10.1016/j.cell.2011.03.006

    Article  CAS  PubMed  Google Scholar 

  37. Nusinow DA, Helfer A, Hamilton EE, King JJ, Imaizumi T, Schultz TF, Farré EM, Kay SA (2011) The ELF4–ELF3–LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475:398–402. https://doi.org/10.1038/nature10182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Avendan M, Leidy C, Pedraza J (2013) Tuning the range and stability of multiple phenotypic states with coupled positive–negative feedback loops. Nat Commun. https://doi.org/10.1038/ncomms3605

    Article  Google Scholar 

  39. McWatters HG, Bastow RM, Hall A, Millar AJ (2000) The ELF3 zeitnehmer regulates light signaling to the circadian clock. Nature 408:716–720. https://doi.org/10.1038/35047079

    Article  CAS  PubMed  Google Scholar 

  40. Hicks KA, Albertson TM, Wagner DR (2001) EARLY FLOWERING3 encodes a novel protein that regulates circadian clock function and flowering in Arabidopsis. Plant Cell 13:1281–1292. https://doi.org/10.1105/TPC.010070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Putterill J, Laurie R, Macknight R (2004) It’s time to flower: the genetic control of flowering time. BioEssays 26:363–373. https://doi.org/10.1002/bies.20021

    Article  CAS  PubMed  Google Scholar 

  42. Mizoguchi T, Wheatley K, Hanzawa Y, Wright L, Mizoguchi M, Song H-R, Carré IA, Coupland G (2002) LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev Cell 2:629–641. https://doi.org/10.1016/S1534-5807(02)00170-3

    Article  CAS  PubMed  Google Scholar 

  43. Somers DE, Devlin PF, Kay SA (1998) Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science 282:1488–1490. https://doi.org/10.1126/science.282.5393.1488

    Article  CAS  PubMed  Google Scholar 

  44. Searle I, Coupland G (2004) Induction of flowering by seasonal changes in photoperiod. EMBO J 23:1217–1222. https://doi.org/10.1038/sj.emboj.7600117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Park D, Somer DE, Kim YS, Choy YH, Lim HK, Soh MS, Kim HJ, Kay SA, Nam HG (1999) Control of Circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA Gene. Science 285:1579–1582. https://doi.org/10.1126/science.285.5433.1579

    Article  CAS  PubMed  Google Scholar 

  46. Huq E, Tepperman JM, Quail PH (2000) GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. Proc Natl Acad Sci 97:9789–9794. https://doi.org/10.1073/pnas.170283997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Nakamichi N, Kita M, Niinuma K, Ito S, Yamashino T, Mizoguchi T, Mizuno T (2007) Arabidopsis clock-associated pseudo-response regulators PRR9, PRR7 and PRR5 coordinately and positively regulate flowering time through the canonical CONSTANS-dependent photoperiodic pathway. Plant Cell Physiol. https://doi.org/10.1093/pcp/pcm056

    Article  PubMed  Google Scholar 

  48. Nakamichi N, Kiba T, Kamioka M, Suzuki T, Yamashino T, Higashiyama T, Sakakibara H, Mizuno T (2012) Transcriptional repressor PRR5 directly regulates clock-output pathways. Proc Natl Acad Sci 109:17123–17128. https://doi.org/10.1073/pnas.1205156109

    Article  PubMed  PubMed Central  Google Scholar 

  49. Salomé PA, McClung CR (2005) PSEUDO-RESPONSE REGULATOR 7 and 9 are partially redundant genes essential for the temperature responsiveness of the Arabidopsis circadian clock. Plant Cell 17:791–803. https://doi.org/10.1105/tpc.104.029504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. 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

    Article  PubMed  PubMed Central  Google Scholar 

  53. Karayekov E, Sellaro R, Legris M, Yanovsky MJ, Casal JJ (2013) Heat shock–induced fluctuations in clock and light signaling enhance phytochrome B–mediated arabidopsis deetiolation. Plant Cell 25:2892–2906. https://doi.org/10.1105/tpc.113.114306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Liu T, Carlsson J, Takeuchi T, Newton L, Farre EM (2013) Direct regulation of abiotic responses by the Arabidopsis circadian clock component PRR 7. Plant J 76:101–114. https://doi.org/10.1111/tpj.12276

    Article  CAS  PubMed  Google Scholar 

  55. Haydon MJ, Mielczarek O, Robertson FC, Hubbard KE, Webb AA (2013) Photosynthetic entrainment of the Arabidopsis thaliana circadian clock. Nature 502:689–692

    Article  CAS  Google Scholar 

  56. Hubbard KE, Robertson FC, Dalchau N, Webb AA (2009) Systems analyses of circadian networks. Mol BioSyst 5:1502–1511. https://doi.org/10.1039/B907714F

    Article  CAS  PubMed  Google Scholar 

  57. Li Z, Bonaldi K, Uribe F, Pruneda-Paz JL (2018) A localized Pseudomonas syringae infection triggers systemic clock responses in Arabidopsis. Curr Biol 28(630–639):e634. https://doi.org/10.1016/j.cub.2018.01.001

    Article  CAS  Google Scholar 

  58. Hennessey TL, Field CB (1991) Circadian rhythms in photosynthesis: oscillations in carbon assimilation and stomatal conductance under constant conditions. Plant Physiol 96:831–836. https://doi.org/10.1104/pp.96.3.831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Graf A, Smith AM (2011) Starch and the clock: the dark side of plant productivity. Trends Plant Sci 16:169–175. https://doi.org/10.1016/j.tplants.2010.12.003

    Article  CAS  PubMed  Google Scholar 

  60. Fan G, Dong Y, Deng M, Zhao Z, Niu S, Xu E (2014) Plant-pathogen interaction, circadian rhythm, and hormone-related gene expression provide indicators of phytoplasma infection in Paulownia fortunei. Int J Mol Sci 15:23141–23162. https://doi.org/10.3390/ijms151223141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Karapetyan S, Dong X (2018) Redox and the circadian clock in plant immunity: a balancing act. Free Radical Biol Med 119:56–61. https://doi.org/10.1016/j.freeradbiomed.2017.12.024

    Article  CAS  Google Scholar 

  62. 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

    Article  CAS  PubMed  Google Scholar 

  63. Seifalian A, Hart A (2019) Circadian rhythms: will it revolutionise the management of diseases? J Lifestyle Med 9:1. https://doi.org/10.15280/jlm.2019.9.1.1

    Article  PubMed  PubMed Central  Google Scholar 

  64. Scheiermann C, Gibbs J, Ince L, Loudon A (2018) Clocking in to immunity. Nat Rev Immunol 18:423–437

    Article  CAS  Google Scholar 

  65. Abdul Malik NA, Kumar IS, Nadarajah K (2020) Elicitor and receptor molecules: orchestrators of plant defense and immunity. Int J Mol Sci 21:963. https://doi.org/10.3390/ijms21030963

    Article  CAS  PubMed Central  Google Scholar 

  66. Hayama R, Coupland G (2003) Shedding light on the circadian clock and the photoperiodic control of flowering. Curr Opin Plant Biol 6:13–19. https://doi.org/10.1016/S1369-5266(02)00011-0

    Article  CAS  PubMed  Google Scholar 

  67. Farré E (2012) The regulation of plant growth by the circadian clock. Plant Biol 14:401–410. https://doi.org/10.1111/j.1438-8677.2011.00548.x

    Article  CAS  PubMed  Google Scholar 

  68. Kobayashi Y, Weigel D (2007) Move on up, it’s time for change—mobile signals controlling photoperiod-dependent flowering. Genes Dev 21:2371–2384. https://doi.org/10.1101/gad.1589007

    Article  CAS  PubMed  Google Scholar 

  69. Inoue K, Araki T, Endo M (2018) Circadian clock during plant development. J Plant Res 131:59–66

    Article  Google Scholar 

  70. Pesti J (1976) Daily fluctuations in the sugar content of nectar and periodicity of secretion in the Compositae. Acta Agron Budap. https://doi.org/10.1007/s00018-022-04368-1

    Article  Google Scholar 

  71. Kolosova N, Gorenstein N, Kish CM, Dudareva N (2001) Regulation of circadian methyl benzoate emission in diurnally and nocturnally emitting plants. Plant Cell 13:2333–2347. https://doi.org/10.1105/tpc.010162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Verdonk JC, De Vos CR, Verhoeven HA, Haring MA, Van Tunen AJ, Schuurink RC (2003) Regulation of floral scent production in petunia revealed by targeted metabolomics. Phytochemistry 62:997–1008. https://doi.org/10.1016/S0031-9422(02)00707-0

    Article  CAS  PubMed  Google Scholar 

  73. Nakamichi N (2015) Adaptation to the local environment by modifications of the photoperiod response in crops. Plant Cell Physiol 56:594–604. https://doi.org/10.1093/pcp/pcu181

    Article  CAS  PubMed  Google Scholar 

  74. Millar AJ (2003) A suite of photoreceptors entrains the plant circadian clock. J Biol Rhythms 18:217–226. https://doi.org/10.1177/0748730403018003004

    Article  CAS  PubMed  Google Scholar 

  75. Nagy F, Fejes E, Wehmeyer B, Dallman G, Schafer E (1993) The circadian oscillator is regulated by a very low fluence response of phytochrome in wheat. Proc Natl Acad Sci 90:6290–6294. https://doi.org/10.1073/pnas.90.13.6290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Adams S, Langton F (2005) Photoperiod and plant growth: a review. J Hortic Sci Biotechnol 80:2–10. https://doi.org/10.1080/14620316.2005.11511882

    Article  Google Scholar 

  77. Lawlor DW (1993) Photosynthesis: molecular physiologial and environmental processes.

  78. Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034. https://doi.org/10.1126/science.1117619

    Article  CAS  PubMed  Google Scholar 

  79. Faure S, Turner AS, Gruszka D, Christodoulou V, Davis SJ, von Korff M, Laurie DA (2012) Mutation at the circadian clock gene EARLY MATURITY 8 adapts domesticated barley (Hordeum vulgare) to short growing seasons. Proc Natl Acad Sci 109:8328–8333. https://doi.org/10.1073/pnas.1120496109

    Article  PubMed  PubMed Central  Google Scholar 

  80. Thomas B, Vince-Prue D (1996) Photoperiodism in plants. Elsevier

    Google Scholar 

  81. Dodd AN, Salathia N, Hall A, Kévei E, Tóth R, Nagy F, Hibberd JM, Millar AJ, Webb AAR (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633

    Article  CAS  Google Scholar 

  82. Börner A, Buck-Sorlin G, Hayes P, Malyshev S, Korzun V (2002) Molecular mapping of major genes and quantitative trait loci determining flowering time in response to photoperiod in barley. Plant Breeding 121:129–132. https://doi.org/10.1046/j.1439-0523.2002.00691.x

    Article  Google Scholar 

  83. Franckowiak J, Lundqvist U, Konishi T, Gallagher L (1997) Description of Stock number: BGS 214. Barley Genetics Newsl 26:213–215

    Google Scholar 

  84. Chory J, Peto CA, Ashbaugh M, Saganich R, Pratt L, Ausubel F (1989) Different roles for phytochrome in etiolated and green plants deduced from characterization of Arabidopsis thaliana mutants. Plant Cell 1:867–880. https://doi.org/10.1105/tpc.1.9.867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Ahmad M, Cashmore AR (1993) HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 366:162–166

    Article  CAS  Google Scholar 

  86. Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C, Harmer SL, Maloof JN (2007) Rhythmic growth explained by coincidence between internal and external cues. Nature 448:358–361. https://doi.org/10.1038/nature05946

    Article  CAS  PubMed  Google Scholar 

  87. Stewart JL, Maloof JN, Nemhauser JL (2011) PIF genes mediate the effect of sucrose on seedling growth dynamics. PLoS ONE 6:e19894. https://doi.org/10.1371/journal.pone.0019894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Dowson-Day MJ, Millar AJ (1999) Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis. Plant J 17:63–71. https://doi.org/10.1046/j.1365-313X.1999.00353.x

    Article  CAS  PubMed  Google Scholar 

  89. Alabadı́ D, Oyama T, Yanovsky MJ, Harmon FG, Más 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

    Article  PubMed  Google Scholar 

  90. Locke JC, Southern MM, Kozma-Bognár L, Hibberd V, Brown PE, Turner MS, Millar AJ (2005) Extension of a genetic network model by iterative experimentation and mathematical analysis. Mol Syst Biol 1(2005):0013. https://doi.org/10.1038/msb4100018

    Article  CAS  PubMed  Google Scholar 

  91. Mizoguchi T, Wright L, Fujiwara S, Cremer F, Lee K, Onouchi H, Mouradov A, Fowler S, Kamada H, Putterill J (2005) Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17:2255–2270. https://doi.org/10.1105/tpc.105.033464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61:1001–1013. https://doi.org/10.1111/j.1365-313X.2010.04148.x

    Article  CAS  PubMed  Google Scholar 

  93. Kim W-Y, Hicks KA, Somers DE (2005) Independent roles for EARLY FLOWERING 3 and ZEITLUPE in the control of circadian timing, hypocotyl length, and flowering time. Plant Physiol 139:1557–1569. https://doi.org/10.1104/pp.105.067173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Kozma-Bognár L, Káldi K (2008) Synchronization of the fungal and the plant circadian clock by light. ChemBioChem 9:2565–2573. https://doi.org/10.1002/cbic.200800385

    Article  CAS  PubMed  Google Scholar 

  95. Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell 14:S111–S130. https://doi.org/10.1105/tpc.001362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Bryant TR (1972) Gas exchange in dry seeds: circadian rhythmicity in the absence of DNA replication, transcription, and translation. Science 178:634–636. https://doi.org/10.1126/science.178.4061.634

    Article  CAS  PubMed  Google Scholar 

  97. Smith SM, Fulton DC, Chia T, Thorneycroft D, Chapple A, Dunstan H, Hylton C, Zeeman SC, Smith AM (2004) Diurnal changes in the transcriptome encoding enzymes of starch metabolism provide evidence for both transcriptional and posttranscriptional regulation of starch metabolism in Arabidopsis leaves. Plant Physiol 136:2687–2699. https://doi.org/10.1104/pp.104.044347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30:1126–1149. https://doi.org/10.1111/j.1365-3040.2007.01708.x

    Article  CAS  PubMed  Google Scholar 

  99. Wang Z-Y, Tobin EM (1998) Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93:1207–1217. https://doi.org/10.1016/S0092-8674(00)81464-6

    Article  CAS  PubMed  Google Scholar 

  100. Zagotta MT, Hicks KA, Jacobs CI, Young JC, Hangarter RP, Meeks-Wagner DR (1996) The Arabidopsis ELF3 gene regulates vegetative photomorphogenesis and the photoperiodic induction of flowering. Plant J 10:691–702. https://doi.org/10.1046/j.1365-313X.1996.10040691.x

    Article  CAS  PubMed  Google Scholar 

  101. Hsiao A-S, Haslam RP, Michaelson LV, Liao P, Napier JA, Chye M-L (2014) Gene expression in plant lipid metabolism in Arabidopsis seedlings. PLoS ONE 9:e107372. https://doi.org/10.1371/journal.pone.0107372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Nakamura Y, Andrés F, Kanehara K, Liu Y-c, Coupland G, Dörmann P (2014) Diurnal and circadian expression profiles of glycerolipid biosynthetic genes in Arabidopsis. Plant Signal Behav 9:e29715. https://doi.org/10.4161/psb.29715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Bendix C, Marshall CM, Harmon FG (2015) Circadian clock genes universally control key agricultural traits. Mol Plant 8:1135–1152. https://doi.org/10.1016/j.molp.2015.03.003

    Article  CAS  PubMed  Google Scholar 

  104. Yanovsky MJ, Kay SA (2002) Molecular basis of seasonal time measurement in Arabidopsis. Nature 419:308–312. https://doi.org/10.1038/nature00996

    Article  CAS  PubMed  Google Scholar 

  105. McWatters HG, Devlin PF (2011) Timing in plants–a rhythmic arrangement. FEBS Lett 585:1474–1484. https://doi.org/10.1016/j.febslet.2011.03.051

    Article  CAS  PubMed  Google Scholar 

  106. Hayama R, Sarid-Krebs L, Richter R, Fernández V, Jang S, Coupland G (2017) PSEUDO RESPONSE REGULATORs stabilize CONSTANS protein to promote flowering in response to day length. EMBO J 36:904–918. https://doi.org/10.15252/embj.201693907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. 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

    Article  CAS  PubMed  Google Scholar 

  108. 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

    Article  CAS  Google Scholar 

  109. Liu XL, Covington MF, Fankhauser C, Chory J, Wagner DR (2001) ELF3 encodes a circadian clock–regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. The Plant Cell 13(6):1293–304. https://doi.org/10.1105/TPC.000475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Nelson DC, Lasswell J, Rogg LE, Cohen MA, Bartel B (2000) FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell 101:331–340. https://doi.org/10.1016/S0092-8674(00)80842-9

    Article  CAS  PubMed  Google Scholar 

  111. Koornneef M, Alonso-Blanco C, Peeters AJ, Soppe W (1998) Genetic control of flowering time in Arabidopsis. Annu Rev Plant Biol 49:345–370. https://doi.org/10.1146/annurev.arplant.49.1.345

    Article  CAS  Google Scholar 

  112. Pajoro A, Biewers S, Dougali E, Leal Valentim F, Mendes MA, Porri A, Coupland G, Van de Peer Y, Van Dijk AD, Colombo L (2014) The (r) evolution of gene regulatory networks controlling Arabidopsis plant reproduction: a two-decade history. J Exp Bot 65:4731–4745. https://doi.org/10.1093/jxb/eru233

    Article  CAS  PubMed  Google Scholar 

  113. Blázquez MA, Trénor M, Weigel D (2002) Independent control of gibberellin biosynthesis and flowering time by the circadian clock in Arabidopsis. Plant Physiol 130:1770–1775. https://doi.org/10.1104/pp.007625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Moon J, Suh SS, Lee H, Choi KR, Hong CB, Paek NC, Kim SG, Lee I (2003) The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J 35:613–623. https://doi.org/10.1046/j.1365-313X.2003.01833.x

    Article  CAS  PubMed  Google Scholar 

  115. Blázquez MA, Green R, Nilsson O, Sussman MR, Weigel D (1998) Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell 10:791–800. https://doi.org/10.1105/tpc.10.5.791

    Article  PubMed  PubMed Central  Google Scholar 

  116. Putterill J, Robson F, Lee K, Simon R, Coupland G (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80:847–857. https://doi.org/10.1016/0092-8674(95)90288-0

    Article  CAS  PubMed  Google Scholar 

  117. Suarez-Lopez P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410:1116–1120

    Article  CAS  Google Scholar 

  118. Johnson E, Bradley M, Harberd NP, Whitelam GC (1994) Photoresponses of light-grown phyA mutants of Arabidopsis (phytochrome A is required for the perception of daylength extensions). Plant Physiol 105:141–149. https://doi.org/10.1104/pp.105.1.141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Guo H, Yang H, Mockler TC, Lin C (1998) Regulation of flowering time by Arabidopsis photoreceptors. Science 279:1360–1363. https://doi.org/10.1126/science.279.5355.1360

    Article  CAS  PubMed  Google Scholar 

  120. El-Assal SE-D, Alonso-Blanco C, Peeters AJ, Raz V, Koornneef M (2001) A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nat Genet 29:435–440. https://doi.org/10.1038/ng767

    Article  CAS  Google Scholar 

  121. Cerdán PD, Chory J (2003) Regulation of flowering time by light quality. Nature 423:881–885. https://doi.org/10.1038/nature01636

    Article  CAS  PubMed  Google Scholar 

  122. Mockler T, Yang H, Yu X, Parikh D, Cheng Y-c, Dolan S, Lin C (2003) Regulation of photoperiodic flowering by Arabidopsis photoreceptors. Proc Natl Acad Sci 100:2140–2145. https://doi.org/10.1073/pnas.0437826100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303:1003–1006. https://doi.org/10.1126/science.1091761

    Article  CAS  PubMed  Google Scholar 

  124. Zuo Z, Liu H, Liu B, Liu X, Lin C (2011) Blue light-dependent interaction of CRY2 with SPA1 regulates COP1 activity and floral initiation in Arabidopsis. Curr Biol 21:841–847

    Article  CAS  Google Scholar 

  125. Yang J, Zhang J, Wang Z, Zhu Q, Wang W (2001) Remobilization of carbon reserves in response to water deficit during grain filling of rice. Field Crop Res 71:47–55. https://doi.org/10.1016/S0378-4290(01)00147-2

    Article  Google Scholar 

  126. Wang H, Ma L-G, Li J-M, Zhao H-Y, Deng XW (2001) Direct interaction of Arabidopsis cryptochromes with COP1 in light control development. Science 294:154–158. https://doi.org/10.1126/science.1063630

    Article  CAS  PubMed  Google Scholar 

  127. Zeng L, Imamoto A, Rosner MR (2008) Raf kinase inhibitory protein (RKIP): a physiological regulator and future therapeutic target. Expert Opin Ther Targets 12:1275–1287. https://doi.org/10.1517/14728222.12.10.1275

    Article  CAS  PubMed  Google Scholar 

  128. Reed JW, Nagpal P, Poole DS, Furuya M, Chory J (1993) Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 5:147–157. https://doi.org/10.1105/tpc.5.2.147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Ishikawa R, Tamaki S, Yokoi S, Inagaki N, Shinomura T, Takano M, Shimamoto K (2005) Suppression of the floral activator Hd3a is the principal cause of the night break effect in rice. Plant Cell 17:3326–3336. https://doi.org/10.1105/tpc.105.037028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Imaizumi T, Tran HG, Swartz TE, Briggs WR, Kay SA (2003) FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426:302–306. https://doi.org/10.1038/nature02090

    Article  CAS  PubMed  Google Scholar 

  131. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2:e718. https://doi.org/10.1371/journal.pone.0000718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Sawa M, Nusinow DA, Kay SA, Imaizumi T (2007) FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318:261–265. https://doi.org/10.1126/science.1146994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Sawa M, Kay SA (2011) GIGANTEA directly activates Flowering Locus T in Arabidopsis thaliana. Proc Natl Acad Sci 108:11698–11703. https://doi.org/10.1073/pnas.1106771108

    Article  PubMed  PubMed Central  Google Scholar 

  134. Koornneef M, Hanhart C, Van der Veen J (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet MGG 229:57–66. https://doi.org/10.1007/bf00264213

    Article  CAS  PubMed  Google Scholar 

  135. Araki T, Komeda Y (1993) Analysis of the role of the late-flowering locus, GI, in the flowering of Arabidopsis thaliana. Plant J 3:231–239. https://doi.org/10.1046/j.1365-313X.1993.t01-15-00999.x

    Article  Google Scholar 

  136. Más P, Kim W-Y, Somers DE, Kay SA (2003) Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426:567–570. https://doi.org/10.1038/nature02163

    Article  CAS  PubMed  Google Scholar 

  137. Ito S, Nakamichi N, Kiba T, Yamashino T, Mizuno T (2007) Rhythmic and light-inducible appearance of clock-associated pseudo-response regulator protein PRR9 through programmed degradation in the dark in Arabidopsis thaliana. Plant Cell Physiol 48:1644–1651. https://doi.org/10.1093/pcp/pcm122

    Article  CAS  PubMed  Google Scholar 

  138. Kiba T, Henriques R, Sakakibara H, Chua N-H (2007) Targeted degradation of PSEUDO-RESPONSE REGULATOR5 by an SCFZTL complex regulates clock function and photomorphogenesis in Arabidopsis thaliana. Plant Cell 19:2516–2530. https://doi.org/10.1105/tpc.107.053033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Fujiwara S, Wang L, Han L, Suh S-S, Salomé PA, McClung CR, Somers DE (2008) Post-translational regulation of the Arabidopsis circadian clock through selective proteolysis and phosphorylation of pseudo-response regulator proteins. J Biol Chem 283:23073–23083. https://doi.org/10.1074/jbc.M803471200

    Article  CAS  PubMed  Google Scholar 

  140. Pin PA, Zhang W, Vogt SH, Dally N, Büttner B, Schulze-Buxloh G, Jelly NS, Chia TY, Mutasa-Göttgens ES, Dohm JC (2012) The role of a pseudo-response regulator gene in life cycle adaptation and domestication of beet. Curr Biol 22:1095–1101. https://doi.org/10.1016/j.cub.2012.04.007

    Article  CAS  PubMed  Google Scholar 

  141. Murphy RL, Klein RR, Morishige DT, Brady JA, Rooney WL, Miller FR, Dugas DV, Klein PE, Mullet JE (2011) Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum. Proc Natl Acad Sci 108:16469–16474. https://doi.org/10.1073/pnas.1106212108

    Article  PubMed  PubMed Central  Google Scholar 

  142. Campoli C, Drosse B, Searle I, Coupland G, von Korff M (2012) Functional characterization of HvCO1, the barley (Hordeum vulgare) flowering time ortholog of CONSTANS. Plant J 69:868–880. https://doi.org/10.1111/j.1365-313X.2011.04839.x

    Article  CAS  PubMed  Google Scholar 

  143. Koo B-H, Yoo S-C, Park J-W, Kwon C-T, Lee B-D, An G, Zhang Z, Li J, Li Z, Paek N-C (2013) Natural variation in OsPRR37 regulates heading date and contributes to rice cultivation at a wide range of latitudes. Mol Plant 6:1877–1888. https://doi.org/10.1093/mp/sst088

    Article  CAS  PubMed  Google Scholar 

  144. Shaw LM, Turner AS, Laurie DA (2012) The impact of photoperiod insensitive Ppd-1a mutations on the photoperiod pathway across the three genomes of hexaploid wheat (Triticum aestivum). Plant J 71:71–84. https://doi.org/10.1111/j.1365-313X.2012.04971.x

    Article  CAS  PubMed  Google Scholar 

  145. Yamamoto Y, Sato E, Shimizu T, Nakamich N, Sato S, Kato T, Tabata S, Nagatani A, Yamashino T, Mizuno T (2003) Comparative genetic studies on the APRR5 and APRR7 genes belonging to the APRR1/TOC1 quintet implicated in circadian rhythm, control of flowering time, and early photomorphogenesis. Plant Cell Physiol 44:1119–1130. https://doi.org/10.1093/pcp/pcg148

    Article  CAS  PubMed  Google Scholar 

  146. Murakami M, Yamashino T, Mizuno T (2004) Quintet of circadian associated APRR1/TOC1 family in Arabidopsis thaliana: characterization of a transgenic line aberrantly overexpressing APRR3. Plant Cell Physiol. https://doi.org/10.1093/pcp/pch065

    Article  PubMed  Google Scholar 

  147. Para A, Farré EM, Imaizumi T, Pruneda-Paz JL, Harmon FG, Kay SA (2007) PRR3 is a vascular regulator of TOC1 stability in the Arabidopsis circadian clock. Plant Cell 19:3462–3473. https://doi.org/10.1105/tpc.107.054775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Más P, Alabadí D, Yanovsky MJ, Oyama T, Kay SA (2003) Dual role of TOC1 in the control of circadian and photomorphogenic responses in Arabidopsis. Plant Cell 15:223–236. https://doi.org/10.1105/tpc.006734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Song YH, Shim JS, Kinmonth-Schultz HA, Imaizumi T (2015) Photoperiodic flowering: time measurement mechanisms in leaves. Annu Rev Plant Biol 66:441–464. https://doi.org/10.1126/science.282.5393.1488

    Article  CAS  PubMed  Google Scholar 

  150. Zhang B, Wang L, Zeng L, Zhang C, Ma H (2015) Arabidopsis TOE proteins convey a photoperiodic signal to antagonize CONSTANS and regulate flowering time. Genes Dev 29:975–987. https://doi.org/10.1101/gad.251520.114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Lonergan TA (1981) A circadian rhythm in the rate of light-induced electron flow in three leguminous species. Plant Physiol 68:1041–1046. https://doi.org/10.1104/pp.68.5.1041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Graf A, Schlereth A, Stitt M, Smith AM (2010) Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc Natl Acad Sci 107:9458–9463. https://doi.org/10.1073/pnas.0914299107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Pantin F, Simonneau T, Rolland G, Dauzat M, Muller B (2011) Control of leaf expansion: a developmental switch from metabolics to hydraulics. Plant Physiol 156:803–815. https://doi.org/10.1104/pp.111.176289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Gorton HL, Williams WE, Binns ME, Gemmell CN, Leheny EA, Shepherd AC (1989) Circadian stomatal rhythms in epidermal peels from Vicia faba. Plant Physiol 90:1329–1334. https://doi.org/10.4161/psb.23123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Meidner H, Willmer C (1993) Circadian rhythm of stomatal movements in epidermal strips. J Exp Bot 44:1649–1652. https://doi.org/10.1093/jxb/44.11.1649

    Article  Google Scholar 

  156. Salomé PA, Michael TP, Kearns EV, Fett-Neto AG, Sharrock RA, McClung CR (2002) The out of phase 1 mutant defines a role for PHYB in circadian phase control in Arabidopsis. Plant Physiol 129:1674–1685. https://doi.org/10.1104/pp.003418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Satter R, Geballe G, Applewhite P, Galston A (1974) Potassium flux and leaf movement in Samanea saman: I. Rhythmic movement. J Gen Physiol 64:413–430. https://doi.org/10.1085/jgp.64.4.413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Mayer W-E, Fischer C (1994) Protoplasts from Phaseolus coccineus L. pulvinar motor cells show circadian volume oscillations. Chronobiol Int 11:156–164. https://doi.org/10.3109/07420529409057235

    Article  CAS  PubMed  Google Scholar 

  159. Kiyosawa K (1979) Unequal distribution of potassium and anions within the Phaseolus pulvinus during circadian leaf movement. Plant Cell Physiol 20:1621–1634. https://doi.org/10.1093/oxfordjournals.pcp.a075965

    Article  CAS  Google Scholar 

  160. De Veylder L, Beeckman T, Beemster GT, Krols L, Terras F, Landrieu I, Van Der Schueren E, Maes S, Naudts M, Inzé D (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13:1653–1668. https://doi.org/10.1105/TPC.010087

    Article  PubMed  PubMed Central  Google Scholar 

  161. Autran D, Jonak C, Belcram K, Beemster GT, Kronenberger J, Grandjean O, Inzé D, Traas J (2002) Cell numbers and leaf development in Arabidopsis: a functional analysis of the STRUWWELPETER gene. EMBO J 21:6036–6049. https://doi.org/10.1093/emboj/cdf614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Sweeney BM, Hastings JW (1958) Rhythmic cell division in populations of Gonyaulax polyedra. J Protozool 5:217–224. https://doi.org/10.1111/j.1550-7408.1958.tb02555.x

    Article  Google Scholar 

  163. Edmunds LN, Laval-Martin DL (1984) Cell division cycles and Orcadian oscillators in Euglena. Chronobiol Int 1:1–9. https://doi.org/10.3109/07420528409059112

    Article  PubMed  Google Scholar 

  164. Carré IA, Edmunds L (1993) Oscillator control of cell division in Euglena: cyclic AMP oscillations mediate the phasing of the cell division cycle by the circadian clock. J Cell Sci 104:1163–1173. https://doi.org/10.1242/jcs.104.4.1163

    Article  PubMed  Google Scholar 

  165. Goto K, Johnson CH (1995) Is the cell division cycle gated by a circadian clock? The case of Chlamydomonas reinhardtii. J Cell Biol 129:1061–1069. https://doi.org/10.1083/jcb.129.4.1061

    Article  CAS  PubMed  Google Scholar 

  166. Makarov VN, Schoschina EV, Lüning K (1995) Diurnal and circadian periodicity of mitosis and growth in marine macroalgae. I. Juvenile sporophytes of Laminariales (Phaeophyta). Eur J Phycol 30:261–266. https://doi.org/10.1080/09670269500651031

    Article  Google Scholar 

  167. Nikaido SS, Johnson CH (2000) Daily and circadian variation in survival from ultraviolet radiation in Chlamydomonas reinhardtii. Photochem Photobiol 71:758–765. https://doi.org/10.1562/0031-8655(2000)0710758DACVIS2.0.CO2

    Article  CAS  PubMed  Google Scholar 

  168. Nagel KA, Schurr U, Walter A (2006) Dynamics of root growth stimulation in Nicotiana tabacum in increasing light intensity. Plant, Cell Environ 29:1936–1945. https://doi.org/10.1111/j.1365-3040.2006.01569.x

    Article  CAS  Google Scholar 

  169. Iijima M, Matsushita N (2011) A circadian and an ultradian rhythm are both evident in root growth of rice. J Plant Physiol 168:2072–2080. https://doi.org/10.1016/j.jplph.2011.06.005

    Article  CAS  PubMed  Google Scholar 

  170. Maizel A, von Wangenheim D, Federici F, Haseloff J, Stelzer EH (2011) High-resolution live imaging of plant growth in near physiological bright conditions using light sheet fluorescence microscopy. Plant J 68:377–385. https://doi.org/10.1111/j.1365-313X.2011.04692.x

    Article  CAS  PubMed  Google Scholar 

  171. Yazdanbakhsh N, Fisahn J (2011) Mutations in leaf starch metabolism modulate the diurnal root growth profiles of Arabidopsis thaliana. Plant Signal Behav 6:995–998. https://doi.org/10.4161/psb.6.7.15484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Sothern RB, Tseng T-S, Orcutt SL, Olszewski NE, Koukkari WL (2002) GIGANTEA and SPINDLY genes linked to the clock pathway that controls circadian characteristics of transpiration in Arabidopsis. Chronobiol Int 19:1005–1022. https://doi.org/10.1081/CBI-120015965

    Article  CAS  PubMed  Google Scholar 

  173. Dodd AN, Parkinson K, Webb AA (2004) Independent circadian regulation of assimilation and stomatal conductance in the ztl-1 mutant of Arabidopsis. New Phytol 162:63–70. https://doi.org/10.1111/j.1469-8137.2004.01005.x

    Article  Google Scholar 

  174. Niwa Y, Yamashino T, Mizuno T (2009) The circadian clock regulates the photoperiodic response of hypocotyl elongation through a coincidence mechanism in Arabidopsis thaliana. Plant Cell Physiol 50:838–854. https://doi.org/10.1093/pcp/pcp028

    Article  CAS  PubMed  Google Scholar 

  175. Coluccio MP, Sanchez SE, Kasulin L, Yanovsky MJ, Botto JF (2011) Genetic mapping of natural variation in a shade avoidance response: ELF3 is the candidate gene for a QTL in hypocotyl growth regulation. J Exp Bot 62:167–176. https://doi.org/10.1093/jxb/erq253

    Article  CAS  PubMed  Google Scholar 

  176. Kerwin RE, Jimenez-Gomez JM, Fulop D, Harmer SL, Maloof JN, Kliebenstein DJ (2011) Network quantitative trait loci mapping of circadian clock outputs identifies metabolic pathway-to-clock linkages in Arabidopsis. Plant Cell 23:471–485. https://doi.org/10.1105/tpc.110.082065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Kunihiro A, Yamashino T, Nakamichi N, Niwa Y, Nakanishi H, Mizuno T (2011) Phytochrome-interacting factor 4 and 5 (PIF4 and PIF5) activate the homeobox ATHB2 and auxin-inducible IAA29 genes in the coincidence mechanism underlying photoperiodic control of plant growth of Arabidopsis thaliana. Plant Cell Physiol 52:1315–1329. https://doi.org/10.1093/pcp/pcr076

    Article  CAS  PubMed  Google Scholar 

  178. Ni Z, Kim E-D, Ha M, Lackey E, Liu J, Zhang Y, Sun Q, Chen ZJ (2009) Altered circadian rhythms regulate growth vigor in hybrids and allopolyploids. Nature 457:327–331. https://doi.org/10.1038/nature07523

    Article  CAS  PubMed  Google Scholar 

  179. Shin J, Davis SJ (2010) Recent advances in computational modeling as a conduit to understand the plant circadian clock. F1000 Biol Rep. https://doi.org/10.3410/B2-49

    Article  PubMed  PubMed Central  Google Scholar 

  180. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Hanano S, Domagalska MA, Nagy F, Davis SJ (2006) Multiple phytohormones influence distinct parameters of the plant circadian clock. Genes Cells 11:1381–1392. https://doi.org/10.1111/j.1365-2443.2006.01026.x

    Article  CAS  PubMed  Google Scholar 

  182. Michael TP, Breton G, Hazen SP, Priest H, Mockler TC, Kay SA, Chory J (2008) A morning-specific phytohormone gene expression program underlying rhythmic plant growth. PLoS Biol 6:e225. https://doi.org/10.1371/journal.pbio.0060225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Kurepa J, Smalle J, Va M, Montagu N, Inzé D (1998) Oxidative stress tolerance and longevity in Arabidopsis: the late-flowering mutant gigantea is tolerant to paraquat. Plant J 14:759–764. https://doi.org/10.1046/j.1365-313x.1998.00168.x

    Article  CAS  PubMed  Google Scholar 

  185. Messerli G, Partovi Nia V, Trevisan M, Kolbe A, Schauer N, Geigenberger P, Chen J, Davison AC, Fernie AR, Zeeman SC (2007) Rapid classification of phenotypic mutants of Arabidopsis via metabolite fingerprinting. Plant Physiol 143:1484–1492. https://doi.org/10.1104/pp.106.090795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Rédei GP (1962) Supervital mutants of Arabidopsis. Genetics 47:443

    Article  Google Scholar 

  187. Kami C, Lorrain S, Hornitschek P, Fankhauser C (2010) Light-regulated plant growth and development. Curr Top Dev Biol 91:29–66. https://doi.org/10.1016/S0070-2153(10)91002-8

    Article  CAS  PubMed  Google Scholar 

  188. Tóth R, Kevei E, Hall A, Millar AJ, Nagy F, Kozma-Bognár L (2001) Circadian clock-regulated expression of phytochrome and cryptochrome genes in Arabidopsis. Plant Physiol 127:1607–1616. https://doi.org/10.1104/pp.010467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Thomas PW, Woodward FI, Quick WP (2004) Systemic irradiance signalling in tobacco. New Phytol 161:193–198

    Article  CAS  Google Scholar 

  190. Sarid-Krebs L, Panigrahi KC, Fornara F, Takahashi Y, Hayama R, Jang S, Tilmes V, Valverde F, Coupland G (2015) Phosphorylation of CONSTANS and its COP 1-dependent degradation during photoperiodic flowering of Arabidopsis. Plant J 84:451–463. https://doi.org/10.1111/tpj.13022

    Article  CAS  PubMed  Google Scholar 

  191. Anderson SL, Kay SA (1996) Illuminating the mechanism of the circadian clock in plants. Trends Plant Sci 1:51–57. https://doi.org/10.1016/S1360-1385(96)80029-X

    Article  Google Scholar 

  192. Assmann SM (1993) Signal transduction in guard cells. Annu Rev Cell Biol 9:345–375. https://doi.org/10.1146/annurev.cb.09.110193.002021

    Article  CAS  PubMed  Google Scholar 

  193. Kim HY, Coté GG, Crain RC (1993) Potassium channels in Samanea saman protoplasts controlled by phytochrome and the biological clock. Science 260:960–962. https://doi.org/10.1126/science.260.5110.960

    Article  CAS  PubMed  Google Scholar 

  194. Spoel SH, Dong X (2008) Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 3:348–351. https://doi.org/10.1016/j.chom.2008.05.009

    Article  CAS  PubMed  Google Scholar 

  195. Miller RNG, Costa Alves GS, Van Sluys M-A (2017) Plant immunity: unraveling the complexity of plant responses to biotic stresses. Ann Bot 119:681–687. https://doi.org/10.1093/aob/mcw284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  196. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  Google Scholar 

  197. Hua J (2013) Modulation of plant immunity by light, circadian rhythm, and temperature. Curr Opin Plant Biol 16:406–413. https://doi.org/10.1016/j.pbi.2013.06.017

    Article  CAS  PubMed  Google Scholar 

  198. Bhardwaj V, Meier S, Petersen LN, Ingle RA, Roden LC (2011) Defence responses of Arabidopsis thaliana to infection by Pseudomonas syringae are regulated by the circadian clock. PLoS ONE 6:e26968. https://doi.org/10.1371/journal.pone.0026968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  199. Gallé Á, Czékus Z, Bela K, Horváth E, Ördög A, Csiszár J, Poór P (2019) Plant glutathione transferases and light. Front Plant Sci 9:1944. https://doi.org/10.3389/fpls.2018.01944

    Article  PubMed  PubMed Central  Google Scholar 

  200. Korneli C, Danisman S, Staiger D (2014) Differential control of pre-invasive and post-invasive antibacterial defense by the Arabidopsis circadian clock. Plant Cell Physiol 55:1613–1622. https://doi.org/10.1093/pcp/pcu092

    Article  CAS  PubMed  Google Scholar 

  201. Brody S (2019) Circadian rhythms in fungi: structure/function/evolution of some clock components. J Biol Rhythms 34:364–379. https://doi.org/10.1177/0748730419852832

    Article  CAS  PubMed  Google Scholar 

  202. Zhang J, Ren Z, Zhou Y, Ma Z, Ma Y, Hou D, Xu Z, Huang X (2019) NPR1 and Redox rhythm: connections, between circadian clock and plant immunity. Int J Mol Sci 20:1211. https://doi.org/10.3390/ijms20051211

    Article  CAS  PubMed Central  Google Scholar 

  203. Tamaoki D, Seo S, Yamada S, Kano A, Miyamoto A, Shishido H, Miyoshi S, Taniguchi S, Akimitsu K, Gomi K (2013) Jasmonic acid and salicylic acid activate a common defense system in rice. Plant Signal Behav 8:e24260. https://doi.org/10.4161/psb.24260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  204. Goodspeed D, Chehab EW, Covington MF, Braam J (2013) Circadian control of jasmonates and salicylates: the clock role in plant defense. Plant Signal Behav 8:e23123

    Article  Google Scholar 

  205. Loake G, Grant M (2007) Salicylic acid in plant defence—the players and protagonists. Curr Opin Plant Biol 10:466–472. https://doi.org/10.1016/j.pbi.2007.08.008

    Article  CAS  PubMed  Google Scholar 

  206. Bechtold U, Karpinski S, Mullineaux P (2005) The influence of the light environment and photosynthesis on oxidative signaling responses in plant-biotrophic pathogen interaction. Plant, Cell Environ 28:1046–1055. https://doi.org/10.1111/j.1365-3040.2005.01340.x

    Article  CAS  Google Scholar 

  207. Roden LC, Ingle RA (2009) Lights, rhythms, infection: the role of light and the circadian clock in determining the outcome of plant–pathogen interactions. Plant Cell 21:2546–2552. https://doi.org/10.1105/tpc.109.069922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  208. Yang Y-X, Wang M-M, Yin Y-L, Onac E, Zhou G-F, Peng S, Xia X-J, Shi K, Yu J-Q, Zhou Y-H (2015) RNA-seq analysis reveals the role of red light in resistance against Pseudomonas syringae pv. tomato DC3000 in tomato plants. BMC Genomics 16:1–16. https://doi.org/10.1186/s12864-015-1228-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  209. Pathania D, Sharma M, Kumar S, Thakur P, Torino E, Janas D, Thakur S (2021) Essential oil derived biosynthesis of metallic nano-particles: implementations above essence. Sustain Mater Technol. https://doi.org/10.1016/j.susmat.2021.e00352

    Article  Google Scholar 

  210. Sharma M, Bassi H, Chauhan P, Thakur P, Chauhan A, Kolarigowda RH, Thakur NK Inhibition of the growth of bacteria and synergism of Ag and ZnO: Calendulla officinalis mediated green approach towards Ag-ZnO nanoparticles and impact of altitude. Calendulla Officinalis

  211. Mas P, Yanovsky MJ (2009) Time for circadian rhythms: plants get synchronized. Curr Opin Plant Biol 12:574–579. https://doi.org/10.1016/j.pbi.2009.07.010

    Article  CAS  PubMed  Google Scholar 

  212. Costantini C, Renga G, Sellitto F, Borghi M, Stincardini C, Pariano M, Zelante T, Chiarotti F, Bartoli A, Mosci P (2020) Microbes in the era of circadian medicine. Front Cell Infect Microbiol 10:30. https://doi.org/10.3389/fcimb.2020.00030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  213. Nomoto Y, Kubozono S, Yamashino T, Nakamichi N, Mizuno T (2012) Circadian clock-and PIF4-controlled plant growth: a coincidence mechanism directly integrates a hormone signaling network into the photoperiodic control of plant architectures in Arabidopsis thaliana. Plant Cell Physiol 53:1950–1964. https://doi.org/10.1093/pcp/pcs137

    Article  CAS  PubMed  Google Scholar 

  214. Singh M, Mas P (2018) A functional connection between the circadian clock and hormonal timing in Arabidopsis. Genes 9:567. https://doi.org/10.3390/genes9120567

    Article  CAS  PubMed Central  Google Scholar 

  215. Rawat R, Schwartz J, Jones MA, Sairanen I, Cheng Y, Andersson CR, Zhao Y, Ljung K, Harmer SL (2009) REVEILLE1, a Myb-like transcription factor, integrates the circadian clock and auxin pathways. Proc Natl Acad Sci 106:16883–16888. https://doi.org/10.1073/pnas.0813035106

    Article  PubMed  PubMed Central  Google Scholar 

  216. Arana MV, Marín-de la Rosa N, Maloof JN, Blázquez MA, Alabadí D (2011) Circadian oscillation of gibberellin signaling in Arabidopsis. Proc Natl Acad Sci 108:9292–9297. https://doi.org/10.1073/pnas.1101050108

    Article  PubMed  PubMed Central  Google Scholar 

  217. Filo J, Wu A, Eliason E, Richardson T, Thines BC, Harmon FG (2015) Gibberellin driven growth in elf3 mutants requires PIF4 and PIF5. Plant Signal Behav 10:e992707. https://doi.org/10.4161/15592324.2014.992707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  218. Wilson RN, Heckman JW, Somerville CR (1992) Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol 100:403–408. https://doi.org/10.1104/pp.100.1.403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  219. Thompson AJ, Andrews J, Mulholland BJ, McKee JM, Hilton HW, Horridge JS, Farquhar GD, Smeeton RC, Smillie IR, Black CR (2007) Overproduction of abscisic acid in tomato increases transpiration efficiency and root hydraulic conductivity and influences leaf expansion. Plant Physiol 143:1905–1917. https://doi.org/10.1104/pp.106.093559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  220. Lim PO, Kim HJ, Gil Nam H (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136. https://doi.org/10.1146/annurev.arplant.57.032905.105316

    Article  CAS  PubMed  Google Scholar 

  221. Kocsy G, Owttrim G, Brander K, Brunold C (1997) Effect of chilling on the diurnal rhythm of enzymes involved in protection against oxidative stress in a chilling-tolerant and a chilling-sensitive maize genotype. Physiol Plant 99:249–254. https://doi.org/10.1111/j.1399-3054.1997.tb05409.x

    Article  CAS  Google Scholar 

  222. Petersen-Mahrt SK, Ekelund NG, Widell S (1994) Influence of UV-B radiation and nitrogen starvation on daily rhythms in phototaxis and cell shape of Euglena gracilis. Physiol Plant 92:501–505. https://doi.org/10.1111/j.1399-3054.1994.tb08842.x

    Article  CAS  Google Scholar 

  223. Herppich M, Von Willert D, Herppich W (1995) Diurnal rhythm in citric acid content preceded the onset of nighttime malic acid accumulation during metabolic changes from C3 to CAM in salt-stressed plants of Mesembryanthemum crystallinum. J Plant Physiol 147:38–42. https://doi.org/10.1016/S0176-1617(11)81409-4

    Article  CAS  Google Scholar 

  224. Spiller SC, Kaufman LS, Thompson WF, Briggs WR (1987) Specific mRNA and rRNA levels in greening pea leaves during recovery from iron stress. Plant Physiol 84:409–414. https://doi.org/10.1104/pp.84.2.409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  225. Korneli C, Gehan MA, Greenham K, Mockler TC, McClung CR (2015) Transcriptional networks—crops, clocks, and abiotic stress. Curr Opin Plant Biol 24:39–46. https://doi.org/10.1016/j.pbi.2015.01.004

    Article  CAS  Google Scholar 

  226. Matsuzaki J, Kawahara Y, Izawa T (2015) Punctual transcriptional regulation by the rice circadian clock under fluctuating field conditions. Plant Cell 27:633–648. https://doi.org/10.1105/tpc.114.135582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  227. Vogt JH, Schippers JH (2015) Setting the PAS, the role of circadian PAS domain proteins during environmental adaptation in plants. Front Plant Sci 6:513. https://doi.org/10.3389/fpls.2015.00513

    Article  PubMed  PubMed Central  Google Scholar 

  228. Erdei L, Szegletes Z, Barabás KN, Pestenácz A, Fülöp K, Kalmár L, Kovács A, Tóth B, Dér A (1998) Environmental stress and the biological clock in plants: changes of rhythmic behavior of carbohydrates, antioxidant enzymes and stomatal resistance by salinity. J Plant Physiol 152:265–271. https://doi.org/10.1016/S0176-1617(98)80141-7

    Article  CAS  Google Scholar 

  229. 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

    Article  CAS  PubMed  Google Scholar 

  230. Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690. https://doi.org/10.1105/tpc.003483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  231. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought-and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406. https://doi.org/10.1105/tpc.10.8.1391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  232. Castells E, Portolés S, Huang W, Mas P (2010) A functional connection between the clock component TOC1 and abscisic acid signaling pathways. Plant Signal Behav 5:409–411. https://doi.org/10.4161/psb.5.4.11213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  233. Shen Y-Y, Wang X-F, Wu F-Q, Du S-Y, Cao Z, Shang Y, Wang X-L, Peng C-C, Yu X-C, Zhu S-Y (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443:823–826. https://doi.org/10.1038/nature05176

    Article  CAS  PubMed  Google Scholar 

  234. Seo PJ, Park M-J, Lim M-H, Kim S-G, Lee M, Baldwin IT, Park C-M (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  235. 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. https://doi.org/10.1093/pcp/pcn008

    Article  CAS  PubMed  Google Scholar 

  236. Suzuki N, Bassil E, Hamilton JS, Inupakutika MA, Zandalinas SI, Tripathy D, Luo Y, Dion E, Fukui G, Kumazaki A (2016) ABA is required for plant acclimation to a combination of salt and heat stress. PLoS ONE 11:e0147625. https://doi.org/10.1371/journal.pone.0147625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  237. Robertson FC, Skeffington AW, Gardner MJ, Webb AA (2009) Interactions between circadian and hormonal signalling in plants. Plant Mol Biol 69:419–427. https://doi.org/10.1007/s11103-008-9407-4

    Article  CAS  PubMed  Google Scholar 

  238. 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

    Article  PubMed  PubMed Central  Google Scholar 

  239. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell Environ 33:453–467. https://doi.org/10.1111/j.1365-3040.2009.02041.x

    Article  CAS  Google Scholar 

  240. 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. Proc Natl Acad Sci 109:17129–17134. https://doi.org/10.1073/pnas.1209148109

    Article  PubMed  PubMed Central  Google Scholar 

  241. Maatta S, Scheu B, Roth MR, Tamura P, Li M, Williams TD, Wang X, Welti R (2012) Levels of Arabidopsis thaliana leaf phosphatidic acids, phosphatidylserines, and most trienoate-containing polar lipid molecular species increase during the dark period of the diurnal cycle. Front Plant Sci 3:49. https://doi.org/10.3389/fpls.2012.00049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  242. Alderete LGS, Flor S, Lucangioli S, Agostini E (2020) Impact of phenol on the glycerophospholipid turnover and potential role of circadian clock in the plant response against this pollutant in tobacco hairy roots. Plant Physiol Biochem 151:411–420. https://doi.org/10.1016/j.plaphy.2020.03.041

    Article  CAS  Google Scholar 

  243. Joo Y, Fragoso V, Yon F, Baldwin IT, Kim SG (2017) Circadian clock component, LHY, tells a plant when to respond photosynthetically to light in nature. J Integr Plant Biol 59:572–587. https://doi.org/10.1111/jipb.12547

    Article  CAS  PubMed  Google Scholar 

  244. Seluzicki A, Burko Y, Chory J (2017) Dancing in the dark: darkness as a signal in plants. Plant, Cell Environ 40:2487–2501. https://doi.org/10.1111/pce.12900

    Article  CAS  Google Scholar 

  245. Kim JA, Kim H-S, Choi S-H, Jang J-Y, Jeong M-J, Lee SI (2017) The importance of the circadian clock in regulating plant metabolism. Int J Mol Sci 18:2680. https://doi.org/10.3390/ijms18122680

    Article  CAS  PubMed Central  Google Scholar 

  246. Recondo E, Leloir LF ( 1961) Adenosine diphosphate glucose and starch synthesis. Biochem Biophys Res Commun 6:85–88. https://doi.org/10.1016/0006-291x(61)90389-8

  247. Nelson OE, Rines HW (1962) The enzymatic deficiency in the waxy mutant of maize. Biochem Biophys Res Commun 9:297–300. https://doi.org/10.1016/0006-291X(62)90043-8

    Article  CAS  PubMed  Google Scholar 

  248. Tenorio G, Orea A, Romero JM, Mérida Á (2003) Oscillation of mRNA level and activity of granule-bound starch synthase I in Arabidopsis leaves during the day/night cycle. Plant Mol Biol 51:949–958

    Article  CAS  Google Scholar 

  249. Ral J-P, Colleoni C, Wattebled F, Dauvillée D, Nempont C, Deschamps P, Li Z, Morell MK, Chibbar R, Purton S (2006) Circadian clock regulation of starch metabolism establishes GBSSI as a major contributor to amylopectin synthesis in Chlamydomonas reinhardtii. Plant Physiol 142:305–317. https://doi.org/10.1104/pp.106.081885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  250. Bunik VI, Tylicki A, Lukashev NV (2013) Thiamin diphosphate-dependent enzymes: from enzymology to metabolic regulation, drug design and disease models. FEBS J 280:6412–6442. https://doi.org/10.1111/febs.12512

    Article  CAS  PubMed  Google Scholar 

  251. Noordally ZB, Trichtinger C, Dalvit I, Hofmann M, Roux C, Zamboni N, Pourcel L, Gas-Pascual E, Gisler A, Fitzpatrick TB (2020) The coenzyme thiamine diphosphate displays a daily rhythm in the Arabidopsis nucleus. Commun Biol 3:1–13. https://doi.org/10.1038/s42003-020-0927-z

    Article  CAS  Google Scholar 

  252. McClung CR (2006) Plant circadian rhythms. Plant Cell 18:792–803

    Article  CAS  Google Scholar 

  253. Kloppstech K (1985) Diurnal and circadian rhythmicity in the expression of light-induced plant nuclear messenger RNAs. Planta 165:502–506. https://doi.org/10.1007/bf00398095

    Article  CAS  PubMed  Google Scholar 

  254. Dodd AN, Griffiths H, Taybi T, Cushman JC, Borland AM (2003) Integrating diel starch metabolism with the circadian and environmental regulation of Crassulacean acid metabolism in Mesembryanthemum crystallinum. Planta 216:789–797. https://doi.org/10.1007/s00425-002-0930-2

    Article  CAS  PubMed  Google Scholar 

  255. Wyka TP, Lüttge UE (2003) Contribution of C3 carboxylation to the circadian rhythm of carbon dioxide uptake in a Crassulacean acid metabolism plant Kalanchoë daigremontiana. J Exp Bot 54(386):1471–1479. https://doi.org/10.1093/jxb/erg152

    Article  CAS  PubMed  Google Scholar 

  256. Webb AA (2003) The physiology of circadian rhythms in plants. New Phytol 160:281–303. https://doi.org/10.1046/j.1469-8137.2003.00895.x

    Article  CAS  PubMed  Google Scholar 

  257. Hartwell J, Nimmo GA, Wilkins MB, Jenkins GI, Nimmo HG (2002) Probing the circadian control of phosphoenolpyruvate carboxylase kinase expression in Kalanchoë fedtschenkoi. Funct Plant Biol 29:663–668. https://doi.org/10.1071/PP01208

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This review article would not have been possible without the encouragement and facility and environment provided by Shoolini University, Solan and Central University of Himachal Pradesh. Authors are also thankful to Silesian University of Technology, Gliwice, Poland for inspiration and guidance throughout in making, designing, and final presentation of the review article.

Funding

The authors have not disclosed any funding.

Author information

Authors and Affiliations

Authors

Contributions

Conception or designing of work has been done by MS. Data collection, analysis, and interpretation has been done by Nidhi and ST. Critical revision of the article and final approval of the version have done by PK.

Corresponding author

Correspondence to Mamta Sharma.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interest.

Consent for publication

Not applicable.

Ethics approval and consent to participate

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nidhi, Kumar, P., Pathania, D. et al. Environment-mediated mutagenetic interference on genetic stabilization and circadian rhythm in plants. Cell. Mol. Life Sci. 79, 358 (2022). https://doi.org/10.1007/s00018-022-04368-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00018-022-04368-1

Keywords

Navigation