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Interplay of Circadian Rhythms and Light in the Regulation of Photosynthesis-Derived Metabolism

Chapter
Part of the Progress in Botany book series

Abstract

Alternating periods of day and night confer an environmental rhythm upon terrestrial plants. Seasonal changes in light intensity and duration (as well as integrals of temperature) inform developmental decisions that directly impact upon plant growth. In response to the selective pressure of these daily rhythms, plants have evolved an endogenous, biological oscillator that coincides with these patterns. These circadian rhythms allow plants to anticipate daily transitions and consequently allocate specific metabolic functions to certain times of day. The circadian system also has a dramatic effect upon development, with the external coincidence model describing how plants measure day length to induce flowering under inductive conditions. Plants’ responses to environmental change are therefore a distillation of direct responses to abiotic factors and moderating factors derived from endogenous biological rhythms. This review summarizes our understanding of how metabolic processes are governed by these interactions, with particular attention to carbon and redox metabolism, two processes derived from photosynthesis.

References

  1. Alabadi D, Oyama T, Yanovsky M, Harmon F, Mas P, Kay S (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293(5531):880–883PubMedGoogle Scholar
  2. Allu AD, Soja AM, Wu A, Szymanski J, Balazadeh S (2014) Salt stress and senescence: identification of cross-talk regulatory components. J Exp Bot 65(14):3993–4008. doi:10.1093/jxb/eru173 PubMedPubMedCentralGoogle Scholar
  3. Andrés-Colás N, Perea-García A, Puig S, Peñarrubia L (2010) Deregulated copper transport affects Arabidopsis development especially in the absence of environmental cycles. Plant Physiol 153(1):170–184. doi:10.1104/pp.110.153676 PubMedPubMedCentralGoogle Scholar
  4. Baerenfaller K, Massonnet C, Walsh S, Baginsky S, Bühlmann P, Hennig L, Hirsch-Hoffmann M, Howell KA, Kahlau S, Radziejwoski A, Russenberger D, Rutishauser D, Small I, Stekhoven D, Sulpice ER, Svozil J, Wuyts N, Stitt M, Hilson P, Granier C, Gruissem W (2012) Systems-based analysis of Arabidopsis leaf growth reveals adaptation to water deficit. Mol Syst Biol 8:606. doi:10.1038/msb.2012.39 PubMedPubMedCentralGoogle Scholar
  5. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113. doi:10.1146/annurev.arplant.59.032607.092759 PubMedGoogle Scholar
  6. Barajas-López JD, Serrato AJ, Cazalis R, Meyer Y, Chueca A, Reichheld J-P, Sahrawy M (2011) Circadian regulation of chloroplastic f and m thioredoxins through control of the CCA1 transcription factor. J Exp Bot 62(6):2039–2051. doi:10.1093/jxb/erq394 Google Scholar
  7. Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65(5):1229–1240. doi:10.1093/jxb/ert375 PubMedGoogle Scholar
  8. Benina M, Ribeiro DM, Gechev TS, Mueller-Roeber B, Schippers JHM (2015) A cell type-specific view on the translation of mRNAs from ROS-responsive genes upon paraquat treatment of Arabidopsis thaliana leaves. Plant Cell Environ 38(2):349–363. doi:10.1111/pce.12355 PubMedGoogle Scholar
  9. Bläsing OE, Gibon Y, Günther M, Höhne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible W-R, Stitt M (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17(12):3257–3281. doi:10.1105/tpc.105.035261 PubMedPubMedCentralGoogle Scholar
  10. Borland A, Hartwell J, Jenkins GI, Wilkins M, Nimmo HG (1999) Metabolite control overrides circadian regulation of phosphoenolpyruvate carboxylase kinase and CO2 fixation in crassulacean acid metabolism. Plant Physiol 121(3):889–896PubMedPubMedCentralGoogle Scholar
  11. Boxall S, Foster J, Bohnert H, Cushman J, Nimmo H, Hartwell J (2005) Conservation and divergence of circadian clock operation in a stress-inducible crassulacean acid metabolism species reveals clock compensation against stress. Plant Physiol 137(3):969–982. doi:10.1104/pp.104.054577 PubMedPubMedCentralGoogle Scholar
  12. Brunkard JO, Runkel AM, Zambryski PC (2015) Chloroplasts extend stromules independently and in response to internal redox signals. Proc Natl Acad Sci U S A 112(32):10044–10049. doi:10.1073/pnas.1511570112 ADSPubMedPubMedCentralGoogle Scholar
  13. Carter PJ, Nimmo HG, Fewson CA, Wilkins MB (1991) Circadian rhythms in the activity of a plant protein kinase. EMBO J 10(8):2063–2068PubMedPubMedCentralGoogle Scholar
  14. Carter PJ, Wilkins MB, Nimmo HG, Fewson C (1995) The role of temperature in the regulation of the circadian rhythm of CO2 fixation in Bryophyllum fedtschenkoi. Planta 196(2). doi:10.1007/BF00201399
  15. Chen Y-Y, Wang Y, Shin L-J, Wu J-F, Shanmugam V, Tsednee M, Lo J-C, Chen C-C, Wu S-H, Yeh K-C (2013) Iron is involved in the maintenance of circadian period length in Arabidopsis. Plant Physiol 161(3):1409–1420. doi:10.1104/pp.112.212068 PubMedPubMedCentralGoogle Scholar
  16. Cheng JC, Seeley KA, Sung ZR (1995) RML1 and RML2, Arabidopsis genes required for cell proliferation at the root tip. Plant Physiol 107(2):365–376PubMedPubMedCentralGoogle Scholar
  17. Cho C-S, Yoon HJ, Kim JY, Woo HA, Rhee SG (2014) Circadian rhythm of hyperoxidized peroxiredoxin II is determined by hemoglobin autoxidation and the 20S proteasome in red blood cells. Proc Natl Acad Sci U S A 111(33):12043–12048. doi:10.1073/pnas.1401100111 ADSPubMedPubMedCentralGoogle Scholar
  18. 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(8):R130. doi:10.1186/gb-2008-9-8-r130 PubMedPubMedCentralGoogle Scholar
  19. Dalchau N, Baek SJ, Briggs HM, Robertson FC, Dodd AN, Gardner MJ, Stancombe MA, Haydon MJ, Stan G-B, Gonçalves JM, Webb AAR (2011) The circadian oscillator gene GIGANTEA mediates a long-term response of the Arabidopsis thaliana circadian clock to sucrose. Proc Natl Acad Sci U S A 108(12):5104–5109. doi:10.1073/pnas.1015452108 ADSPubMedPubMedCentralGoogle Scholar
  20. Del Río LA (2015) ROS and RNS in plant physiology: an overview. J Exp Bot 66(10):2827–2837. doi:10.1093/jxb/erv099 PubMedGoogle Scholar
  21. Dever LV, Boxall SF, Kneřová J, Hartwell J (2015) Transgenic perturbation of the decarboxylation phase of Crassulacean acid metabolism alters physiology and metabolism but has only a small effect on growth. Plant Physiol 167(1):44–59. doi:10.1104/pp.114.251827 PubMedGoogle Scholar
  22. Dietz K-J (2011) Peroxiredoxins in plants and cyanobacteria. Antioxid Redox Signal 15(4):1129–1159. doi:10.1089/ars.2010.3657 PubMedPubMedCentralGoogle Scholar
  23. Dietz K-J (2014) Redox regulation of transcription factors in plant stress acclimation and development. Antioxid Redox Signal 21(9):1356–1372. doi:10.1089/ars.2013.5672 PubMedGoogle Scholar
  24. Dietz K-J (2016) Thiol-based peroxidases and ascorbate peroxidases: why plants rely on multiple peroxidase systems in the photosynthesizing chloroplast? Mol Cells 39(1):20–25. doi:10.14348/molcells.2016.2324 PubMedPubMedCentralGoogle Scholar
  25. Dittrich P (1976) Nicotinamide adenine dinucleotide-specific “malic” enzyme in Kalanchoë daigremontiana and other plants exhibiting crassulacean acid metabolism. Plant Physiol 57(2):310–314PubMedPubMedCentralGoogle Scholar
  26. Dodd AN, Parkinson K, Webb AAR (2004) Independent circadian regulation of assimilation and stomatal conductance in the ztl-1 mutant of Arabidopsis. New Phytol 162(1):63–70. doi:10.1111/j.1469-8137.2004.01005.x Google Scholar
  27. Dodd AN, Salathia N, Hall A, Kevei E, Tóth R, Nagy F, Hibberd JM, Millar AJ, Webb AAR (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309(5734):630–633. doi:10.1126/science.1115581 ADSPubMedGoogle Scholar
  28. Dodd AN, Gardner MJ, Hotta CT, Hubbard KE, Dalchau N, Love J, Assie J-M, Robertson FC, Jakobsen MK, Gonçalves J, Sanders D, Webb AAR (2007) The Arabidopsis circadian clock incorporates a cADPR-based feedback loop. Science 318(5857):1789–1792ADSPubMedGoogle Scholar
  29. Dodd AN, Dalchau N, Gardner MJ, Baek S-J, Webb AAR (2014) The circadian clock has transient plasticity of period and is required for timing of nocturnal processes in Arabidopsis. New Phytol 201(1):168–179. doi:10.1111/nph.12489 PubMedGoogle Scholar
  30. Dodd AN, Belbin FE, Frank A, Webb AAR (2015) Interactions between circadian clocks and photosynthesis for the temporal and spatial coordination of metabolism. Front Plant Sci 6:245. doi:10.3389/fpls.2015.00245 PubMedPubMedCentralGoogle Scholar
  31. Duc C, Cellier F, Lobréaux S, Briat J-F, Gaymard F (2009) Regulation of iron homeostasis in Arabidopsis thaliana by the clock regulator time for coffee. J Biol Chem 284(52):36271–36281. doi:10.1074/jbc.M109.059873 PubMedPubMedCentralGoogle Scholar
  32. Dunand C, Crèvecoeur M, Penel C (2007) Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. New Phytol 174(2):332–341. doi:10.1111/j.1469-8137.2007.01995.x PubMedGoogle Scholar
  33. Edgar RS, Green EW, Zhao Y, Van Ooijen G, Olmedo M, Qin X, Xu Y, Pan M, Valekunja UK, Feeney KA, Maywood ES, Hastings MH, Baliga NS, Merrow M, Millar AJ, Johnson CH, Kyriacou CP, O’Neill JS, Reddy AB (2012) Peroxiredoxins are conserved markers of circadian rhythms. Nature 485(7399):459–464. doi:10.1038/nature11088 ADSPubMedPubMedCentralGoogle Scholar
  34. 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(11):e14101. doi:10.1371/journal.pone.0014101 ADSPubMedPubMedCentralGoogle Scholar
  35. Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345Google Scholar
  36. Feeney KA, Hansen LL, Putker M, Olivares-Yañez C, Day J, Eades LJ, Larrondo LF, Hoyle NP, O’Neill JS, Van Ooijen G (2016) Daily magnesium fluxes regulate cellular timekeeping and energy balance. Nature 532(7599):375–379. doi:10.1038/nature17407 ADSPubMedPubMedCentralGoogle Scholar
  37. Feugier FG, Satake A (2012) Dynamical feedback between circadian clock and sucrose availability explains adaptive response of starch metabolism to various photoperiods. Front Plant Sci 3:305. doi:10.3389/fpls.2012.00305 PubMedGoogle Scholar
  38. Figueroa CM, Lunn JE (2016) A tale of two sugars: trehalose 6-phosphate and sucrose. Plant Physiol 172(1):7–27. doi:10.1104/pp.16.00417 PubMedPubMedCentralGoogle Scholar
  39. Figueroa CM, Feil R, Ishihara H, Watanabe M, Kölling K, Krause U, Höhne M, Encke B, Plaxton WC, Zeeman SC, Li Z, Schulze WX, Hoefgen R, Stitt M, Lunn JE (2016) Trehalose 6-phosphate coordinates organic and amino acid metabolism with carbon availability. Plant J 85(3):410–423. doi:10.1111/tpj.13114 PubMedGoogle Scholar
  40. Fogelmark K, Troein C (2014) Rethinking transcriptional activation in the Arabidopsis circadian clock. PLoS Comput Biol 10(7):e1003705. doi:10.1371/journal.pcbi.1003705 ADSPubMedPubMedCentralGoogle Scholar
  41. Foyer CH, Noctor G (2016) Stress-triggered redox signalling: what’s in pROSpect? Plant Cell Environ 39(5):951–964. doi:10.1111/pce.12621 PubMedGoogle Scholar
  42. Gendron JM, Pruneda-Paz JL, Doherty CJ, Gross AM, Kang SE, Kay SA (2012) Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor. Proc Natl Acad Sci U S A 109(8):3167–3172. doi:10.1073/pnas.1200355109 ADSPubMedPubMedCentralGoogle Scholar
  43. Gibon Y, Bläsing OE, Palacios-Rojas N, Pankovic D, Hendriks JHM, Fisahn J, Höhne M, Günther M, Stitt M (2004) Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. Plant J 39(6):847–862. doi:10.1111/j.1365-313X.2004.02173.x PubMedGoogle Scholar
  44. Gibon Y, Usadel B, Blaesing OE, Kamlage B, Hoehne M, Trethewey R, Stitt M (2006) Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes. Genome Biol 7(8):R76. doi:10.1186/gb-2006-7-8-R76 PubMedPubMedCentralGoogle Scholar
  45. Gibon Y, Pyl E-T, Sulpice R, Lunn JE, Höhne M, Günther M, Stitt M (2009) Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. Plant Cell Environ 32(7):859–874. doi:10.1111/j.1365-3040.2009.01965.x PubMedGoogle Scholar
  46. Gould PD, Ugarte N, Domijan M, Costa M, Foreman J, Macgregor D, Rose K, Griffiths J, Millar AJ, Finkenstädt B, Penfield S, Rand DA, Halliday KJ, Hall AJW (2013) Network balance via CRY signalling controls the Arabidopsis circadian clock over ambient temperatures. Mol Syst Biol 9:650. doi:10.1038/msb.2013.7 PubMedPubMedCentralGoogle Scholar
  47. Graf A, Smith AM (2011) Starch and the clock: the dark side of plant productivity. Trends Plant Sci 16(3):169–175. doi:10.1016/j.tplants.2010.12.003 PubMedGoogle Scholar
  48. 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 U S A 107(20):9458–9463. doi:10.1073/pnas.0914299107 ADSPubMedPubMedCentralGoogle Scholar
  49. Hädrich N, Hendriks JHM, Kötting O, Arrivault S, Feil R, Zeeman SC, Gibon Y, Schulze WX, Stitt M, Lunn JE (2012) Mutagenesis of cysteine 81 prevents dimerization of the APS1 subunit of ADP-glucose pyrophosphorylase and alters diurnal starch turnover in Arabidopsis thaliana leaves. Plant J 70(2):231–242. doi:10.1111/j.1365-313X.2011.04860.x PubMedGoogle Scholar
  50. Hall A, Bastow RM, Davis SJ, Hanano S, McWatters HG, Hibberd V, Doyle MR, Sung S, Halliday KJ, Amasino RM, Millar AJ (2003) The TIME FOR COFFEE gene maintains the amplitude and timing of Arabidopsis circadian clocks. Plant Cell 15(11):2719–2729. doi:10.1105/tpc.013730. tpc.013730 [pii]PubMedPubMedCentralGoogle Scholar
  51. Hall A, Karplus PA, Poole LB (2009) Typical 2-Cys peroxiredoxins – structures, mechanisms and functions. FEBS J 276(9):2469–2477. doi:10.1111/j.1742-4658.2009.06985.x PubMedPubMedCentralGoogle Scholar
  52. Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290:2110–2113ADSPubMedGoogle Scholar
  53. Hartwell J (2008) The circadian clock in CAM plants. In: Annual plant reviews. doi:10.1016/j.ejcts.2009.02.013 Google Scholar
  54. Hartwell J, Gill A, Nimmo GA, Wilkins MB, Jenkins GI, Nimmo HG (1999) Phosphoenolpyruvate carboxylase kinase is a novel protein kinase regulated at the level of expression. Plant J 20(3):333–342. tpj609 [pii]PubMedGoogle Scholar
  55. Hartwell J, Dever LV, Boxall SF (2016) Emerging model systems for functional genomics analysis of crassulacean acid metabolism. Curr Opin Plant Biol 31:100–108. doi:10.1016/j.pbi.2016.03.019 PubMedGoogle Scholar
  56. Hastings MH, Maywood ES, O’Neill JS (2008) Cellular circadian pacemaking and the role of cytosolic rhythms. Curr Biol 18(17):R805–R815. doi:10.1016/j.cub.2008.07.021 PubMedGoogle Scholar
  57. Haydon MJ, Mielczarek O, Robertson FC, Hubbard KE, Webb AAR (2013) Photosynthetic entrainment of the Arabidopsis thaliana circadian clock. Nature 502(7473):689–692. doi:10.1038/nature12603 ADSPubMedGoogle Scholar
  58. Haydon MJ, Román Á, Arshad W (2015) Nutrient homeostasis within the plant circadian network. Front Plant Sci 6:299. doi:10.3389/fpls.2015.00299 PubMedPubMedCentralGoogle Scholar
  59. Helfer A, Nusinow DA, Chow BY, Gehrke AR, Bulyk ML, Kay SA (2011) LUX ARRHYTHMO encodes a nighttime repressor of circadian gene expression in the Arabidopsis core clock. Curr Biol 21(2):126–133. doi:10.1016/j.cub.2010.12.021 PubMedPubMedCentralGoogle Scholar
  60. Hennessey TL, Field CB (1991) Circadian rhythms in photosynthesis: oscillations in carbon assimilation and stomatal conductance under constant conditions. Plant Physiol 96(3):831–836. doi:10.1023/A:1011807229154 PubMedPubMedCentralGoogle Scholar
  61. Hermans C, Vuylsteke M, Coppens F, Craciun A, Inzé D, Verbruggen N (2010) Early transcriptomic changes induced by magnesium deficiency in Arabidopsis thaliana reveal the alteration of circadian clock gene expression in roots and the triggering of abscisic acid-responsive genes. New Phytol 187(1):119–131. doi:10.1111/j.1469-8137.2010.03258.x PubMedGoogle Scholar
  62. Holtum JAM, Smith JAC, Neuhaus HE (2005) Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism. Funct Plant Biol 32(5):429. doi:10.1071/FP04189 Google Scholar
  63. Hong S, Kim SA, Guerinot ML, McClung CR (2013) Reciprocal interaction of the circadian clock with the iron homeostasis network in Arabidopsis. Plant Physiol 161(2):893–903. doi:10.1104/pp.112.208603 PubMedGoogle Scholar
  64. Hsu PY, Harmer SL (2014) Wheels within wheels: the plant circadian system. Trends Plant Sci 19(4):240–249. doi:10.1016/j.tplants.2013.11.007 PubMedGoogle Scholar
  65. Huang W, Perez-Garcia P, Pokhilko A, Millar AJ, Antoshechkin I, Riechmann JL, Mas P (2012) Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 336(6077):75–79. doi:10.1126/science.1219075 ADSPubMedGoogle Scholar
  66. Ito S, Matsushika A, Yamada H, Sato S, Kato T, Tabata S, Yamashino T, Mizuno T (2003) Characterization of the APRR9 pseudo-response regulator belonging to the APRR1/TOC1 quintet in Arabidopsis thaliana. Plant Cell Physiol 44(11):1237–1245PubMedGoogle Scholar
  67. Johnson CH, Knight MR, Kondo T, Masson P, Sedbrook J, Haley A, Trewavas A (1995) Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science 269(5232):1863–1865ADSPubMedGoogle Scholar
  68. Jones MA, Covington MF, DiTacchio L, Vollmers C, Panda S, Harmer SL (2010) Jumonji domain protein JMJD5 functions in both the plant and human circadian systems. Proc Natl Acad Sci U S A 107(50):21623–21628. doi:10.1073/pnas.1014204108 ADSPubMedPubMedCentralGoogle Scholar
  69. Kim W, Fujiwara S, Suh S, Kim J, Kim Y, Han L, David K, Putterill J, Nam H, Somers D (2007) ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449(7160):356–360ADSPubMedGoogle Scholar
  70. Kim J, Geng R, Gallenstein RA, Somers DE (2013) The F-box protein ZEITLUPE controls stability and nucleocytoplasmic partitioning of GIGANTEA. Development 140(19):4060–4069. doi:10.1242/dev.096651 PubMedPubMedCentralGoogle Scholar
  71. Klose R, Kallin E, Zhang Y (2006) JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet 7(9):715–727PubMedGoogle Scholar
  72. Kölling K, Thalmann M, Müller A, Jenny C, Zeeman SC (2015) Carbon partitioning in Arabidopsis thaliana is a dynamic process controlled by the plants metabolic status and its circadian clock. Plant Cell Environ 38(10):1965–1979. doi:10.1111/pce.12512 PubMedPubMedCentralGoogle Scholar
  73. Lai AG, Doherty CJ, Mueller-Roeber B, Kay SA, Schippers JHM, Dijkwel PP (2012) CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses. Proc Natl Acad Sci U S A 109(42):17129–17134. doi:10.1073/pnas.1209148109 ADSPubMedPubMedCentralGoogle Scholar
  74. Lawson T, Blatt MR (2014) Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol 164(4):1556–1570. doi:10.1104/pp.114.237107 PubMedPubMedCentralGoogle Scholar
  75. Lázaro JJ, Jimenez A, Camejo D, Iglesias-Baena I, Martí MDC, Lázaro-Payo A, Barranco-Medina S, Sevilla F (2013) Dissecting the integrative antioxidant and redox systems in plant mitochondria. Effect of stress and S-nitrosylation. Front Plant Sci 4:460. doi:10.3389/fpls.2013.00460 PubMedPubMedCentralGoogle Scholar
  76. Legnaioli T, Cuevas J, Más P (2009) TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought. EMBO J 28(23):3745–3757. doi:10.1038/emboj.2009.297 PubMedPubMedCentralGoogle Scholar
  77. Litthauer S, Battle MW, Lawson T, Jones MA (2015) Phototropins maintain robust circadian oscillation of PSII operating efficiency under blue light. Plant J 83(6):1034–1045. doi:10.1111/tpj.12947 PubMedGoogle Scholar
  78. Liu T, Carlsson J, Takeuchi T, Newton L, Farré EM (2013) Direct regulation of abiotic responses by the Arabidopsiscircadian clock component PRR7. Plant J. doi:10.1111/tpj.12276 Google Scholar
  79. Locke J, Southern M, Kozma-Bognar L, Hibberd V, Brown P, Turner M, Millar A (2005) Extension of a genetic network model by iterative experimentation and mathematical analysis. Mol Syst Biol 1(2005):0013PubMedGoogle Scholar
  80. Love J, Dodd AN, Webb AAR (2004) Circadian and diurnal calcium oscillations encode photoperiodic information in Arabidopsis. Plant Cell 16(4):956–966. doi:10.1105/tpc.020214 PubMedPubMedCentralGoogle Scholar
  81. Lu Y, Gehan JP, Sharkey TD (2005) Daylength and circadian effects on starch degradation and maltose metabolism. Plant Physiol 138(4):2280–2291. doi:10.1104/pp.105.061903 PubMedPubMedCentralGoogle Scholar
  82. Lunn JE, Feil R, Hendriks JHM, Gibon Y, Morcuende R, Osuna D, Scheible W-R, Carillo P, Hajirezaei M-R, Stitt M (2006) Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem J 397(1):139–148. doi:10.1042/BJ20060083 PubMedPubMedCentralGoogle Scholar
  83. Lüttge U, Ball E (1978) Free running oscillations of transpiration and CO2 exchange in CAM plants without a concomitant rhythm of malate levels. Z Pflanzenphysiol 90(1):69–77. doi:10.1016/S0044-328X(78)80226-8 Google Scholar
  84. Malapeira J, Khaitova LC, Más P (2012) Ordered changes in histone modifications at the core of the Arabidopsis circadian clock. Proc Natl Acad Sci U S A 109(52):21540–21545. doi:10.1073/pnas.1217022110 ADSPubMedPubMedCentralGoogle Scholar
  85. Martins MCM, Hejazi M, Fettke J, Steup M, Feil R, Krause U, Arrivault S, Vosloh D, Figueroa CM, Ivakov A, Yadav UP, Piques M, Metzner D, Stitt M, Lunn JE (2013) Feedback inhibition of starch degradation in Arabidopsis leaves mediated by trehalose 6-phosphate. Plant Physiol 163(3):1142–1163. doi:10.1104/pp.113.226787 PubMedPubMedCentralGoogle Scholar
  86. Más P, Kim W-Y, Somers DE, Kay SA (2003) Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426(6966):567–570. doi:10.1038/nature02163 ADSPubMedGoogle Scholar
  87. McAusland L, Vialet-Chabrand S, Davey P, Baker NR, Brendel O, Lawson T (2016) Effects of kinetics of light-induced stomatal responses on photosynthesis and water-use efficiency. New Phytol 211(4):1209–1220. doi:10.1111/nph.14000 PubMedPubMedCentralGoogle Scholar
  88. McClung CR (2006) Plant circadian rhythms. Plant Cell 18(4):792–803. doi:10.1105/tpc.106.040980 PubMedPubMedCentralGoogle Scholar
  89. Michael T, Mockler T, Breton G, McEntee C, Byer A, Trout J, Hazen S, Shen R, Priest H, Sullivan C, Givan S, Yanovsky M, Hong F, Kay S, Chory J (2008) Network discovery pipeline elucidates conserved time-of-day-specific cis-regulatory modules. PLoS Genet 4(2):e14. doi:10.1371/journal.pgen.0040014 PubMedPubMedCentralGoogle Scholar
  90. Millar AJ (2016) The intracellular dynamics of circadian clocks reach for the light of ecology and evolution. Annu Rev Plant Biol 67:595–618. doi:10.1146/annurev-arplant-043014-115619 PubMedGoogle Scholar
  91. 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(3):481–487. doi:10.1093/pcp/pcn008 PubMedGoogle Scholar
  92. Mizuno T, Nomoto Y, Oka H, Kitayama M, Takeuchi A, Tsubouchi M, Yamashino T (2014) Ambient temperature signal feeds into the circadian clock transcriptional circuitry through the EC night-time repressor in Arabidopsis thaliana. Plant Cell Physiol 55(5):958–976. doi:10.1093/pcp/pcu030 PubMedGoogle Scholar
  93. Müller LM, von Korff M, Davis SJ (2014) Connections between circadian clocks and carbon metabolism reveal species-specific effects on growth control. J Exp Bot 65(11):2915–2923. doi:10.1093/jxb/eru117 PubMedGoogle Scholar
  94. Nakamichi N, Kiba T, Henriques R, Mizuno T, Chua N-H, Sakakibara H (2010) PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell 22(3):594–605. doi:10.1105/tpc.109.072892 PubMedPubMedCentralGoogle Scholar
  95. Nakamichi N, Kiba T, Kamioka M, Suzuki T, Yamashino T, Higashiyama T et al (2012) Transcriptional repressor PRR5 directly regulates clock-output pathways. Proc Natl Acad Sci U S A 109(42):17123–17128. doi:10.1073/pnas.1205156109 ADSPubMedPubMedCentralGoogle Scholar
  96. Nimmo HG (2000) The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends Plant Sci 5(2):75–80PubMedGoogle Scholar
  97. Niu Y, DesMarais TL, Tong Z, Yao Y, Costa M (2015) Oxidative stress alters global histone modification and DNA methylation. Free Radic Biol Med 82:22–28. doi:10.1016/j.freeradbiomed.2015.01.028 PubMedPubMedCentralGoogle Scholar
  98. Noordally ZB, Ishii K, Atkins KA, Wetherill SJ, Kusakina J, Walton EJ, Kato M, Azuma M, Tanaka K, Hanaoka M, Dodd AN (2013) Circadian control of chloroplast transcription by a nuclear-encoded timing signal. Science 339(6125):1316–1319. doi:10.1126/science.1230397 ADSPubMedGoogle Scholar
  99. 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. doi:10.1038/nature10182 PubMedPubMedCentralGoogle Scholar
  100. O’Neill JS, Reddy AB (2011) Circadian clocks in human red blood cells. Nature 469(7331):498–503. doi:10.1038/nature09702 ADSPubMedPubMedCentralGoogle Scholar
  101. O’Neill JS, Van Ooijen G, Dixon LE, Troein C, Corellou F, Bouget F-Y, Reddy AB, Millar AJ (2011) Circadian rhythms persist without transcription in a eukaryote. Nature 469(7331):554–558. doi:10.1038/nature09654 ADSPubMedPubMedCentralGoogle Scholar
  102. Perales M, Más P (2007) A functional link between rhythmic changes in chromatin structure and the Arabidopsis biological clock. Plant Cell 19(7):2111–2123. doi:10.1105/tpc.107.050807 PubMedPubMedCentralGoogle Scholar
  103. Pilkington SM, Encke B, Krohn N, Höhne M, Stitt M, Pyl E-T (2015) Relationship between starch degradation and carbon demand for maintenance and growth in Arabidopsis thaliana in different irradiance and temperature regimes. Plant Cell Environ 38(1):157–171. doi:10.1111/pce.12381 PubMedGoogle Scholar
  104. Pokhilko A, Más P, Millar AJ (2013) Modelling the widespread effects of TOC1 signalling on the plant circadian clock and its outputs. BMC Syst Biol 7:23. doi:10.1186/1752-0509-7-23 PubMedPubMedCentralGoogle Scholar
  105. Pokhilko A, Flis A, Sulpice R, Stitt M, Ebenhöh O (2014) Adjustment of carbon fluxes to light conditions regulates the daily turnover of starch in plants: a computational model. Mol Biosyst 10(3):613–627. doi:10.1039/c3mb70459a PubMedGoogle Scholar
  106. Rascher U, Hütt MT, Siebke K, Osmond B, Beck F, Lüttge U (2001) Spatiotemporal variation of metabolism in a plant circadian rhythm: the biological clock as an assembly of coupled individual oscillators. Proc Natl Acad Sci U S A 98(20):11801–11805. doi:10.1073/pnas.191169598 ADSPubMedPubMedCentralGoogle Scholar
  107. Ravet K, Touraine B, Boucherez J, Briat J-F, Gaymard F, Cellier F (2009) Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis. Plant J 57(3):400–412. doi:10.1111/j.1365-313X.2008.03698.x PubMedGoogle Scholar
  108. 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(3):e1001350. doi:10.1371/journal.pgen.1001350 PubMedPubMedCentralGoogle Scholar
  109. Robertson FC, Skeffington AW, Gardner MJ, Webb AAR (2008) Interactions between circadian and hormonal signalling in plants. Plant Mol Biol 69(4):419–427. doi:10.1007/s11103-008-9407-4 PubMedGoogle Scholar
  110. Rugnone ML, Faigón Soverna A, Sanchez SE, Schlaen RG, Hernando CE, Seymour DK, Mancini AC, Weigel D, Más P, Yanovsky MJ (2013) LNK genes integrate light and clock signaling networks at the core of the Arabidopsis oscillator. Proc Natl Acad Sci U S A 110(29):12120–12125. doi:10.1073/pnas.1302170110 ADSPubMedPubMedCentralGoogle Scholar
  111. Sage RF, Sage TL, Kocacinar F (2012) Photorespiration and the evolution of C4 photosynthesis. Annu Rev Plant Biol 63:19–47. doi:10.1146/annurev-arplant-042811-105511 PubMedGoogle Scholar
  112. 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(3):791–803. doi:10.1105/tpc.104.029504 PubMedPubMedCentralGoogle Scholar
  113. Salome 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(4):1674–1685PubMedPubMedCentralGoogle Scholar
  114. Salomé PA, Oliva M, Weigel D, Krämer U (2013) Circadian clock adjustment to plant iron status depends on chloroplast and phytochrome function. EMBO J 32(4):511–523. doi:10.1038/emboj.2012.330 PubMedGoogle Scholar
  115. Sanchez-Villarreal A, Shin J, Bujdoso N, Obata T, Neumann U, Du S-X, Ding Z, Davis AM, Shindo T, Schmelzer E, Sulpice R, Nunes-Nesi A, Stitt M, Fernie AR, Davis SJ (2013) TIME FOR COFFEE is an essential component in the maintenance of metabolic homeostasis in Arabidopsis thaliana. Plant J 76(2):188–200. doi:10.1111/tpj.12292 PubMedGoogle Scholar
  116. Sauve AA, Wolberger C, Schramm VL, Boeke JD (2006) The biochemistry of sirtuins. Annu Rev Biochem 75:435–465. doi:10.1146/annurev.biochem.74.082803.133500 PubMedGoogle Scholar
  117. Scialdone A, Mugford ST, Feike D, Skeffington A, Borrill P, Graf A, Smith AM, Howard M (2013) Arabidopsis plants perform arithmetic division to prevent starvation at night. Elife 2:e00669. doi:10.7554/eLife.00669 PubMedPubMedCentralGoogle Scholar
  118. Sevilla F, Camejo D, Ortiz-Espin A, Calderon A, Lazaro JJ, Jimenez A (2015) The thioredoxin/peroxiredoxin/sulfiredoxin system: current overview on its redox function in plants and regulation by reactive oxygen and nitrogen species. J Exp Bot 66(10):2945–2955. doi:10.1093/jxb/erv146 PubMedGoogle Scholar
  119. Sharkey TD (2015) Understanding carbon partitioning and its role in determining plant growth. Plant Cell Environ 38(10):1963–1964. doi:10.1111/pce.12543 PubMedGoogle Scholar
  120. Skeffington AW, Graf A, Duxbury Z, Gruissem W, Smith AM (2014) Glucan, water dikinase exerts little control over starch degradation in Arabidopsis leaves at night. Plant Physiol 165(2):866–879. doi:10.1104/pp.114.237016 PubMedPubMedCentralGoogle Scholar
  121. Smith AM (2012) Starch in the Arabidopsis plant. Starch Stärke. doi:10.1002/star.201100163 Google Scholar
  122. Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30(9):1126–1149. doi:10.1111/j.1365-3040.2007.01708.x PubMedGoogle Scholar
  123. Smith JAC, Winter K (1996) Taxonomic distribution of crassulacean acid metabolism. In: Chapter 27, vol 114. Springer, Berlin; Heidelberg, pp 427–436. doi:10.1007/978-3-642-79060-7_27 Google Scholar
  124. 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(1):2687–2699. doi:10.1104/pp.104.044347 PubMedPubMedCentralGoogle Scholar
  125. Somers D, Webb A, Pearson M, Kay S (1998) The short-period mutant, toc1-1, alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana. Development 125(3):485–494PubMedGoogle Scholar
  126. Spadaro D, Yun B-W, Spoel SH, Chu C, Wang Y-Q, Loake GJ (2010) The redox switch: dynamic regulation of protein function by cysteine modifications. Physiol Plant 138(4):360–371. doi:10.1111/j.1399-3054.2009.01307.x PubMedGoogle Scholar
  127. Spoel SH, Van Ooijen G (2014) Circadian redox signaling in plant immunity and abiotic stress. Antioxid Redox Signal 20(18):3024–3039. doi:10.1089/ars.2013.5530 PubMedPubMedCentralGoogle Scholar
  128. Stangherlin A, Reddy AB (2013) Regulation of circadian clocks by redox homeostasis. J Biol Chem 288(37):26505–26511. doi:10.1074/jbc.R113.457564 PubMedPubMedCentralGoogle Scholar
  129. Stitt M, Zeeman SC (2012) Starch turnover: pathways, regulation and role in growth. Curr Opin Plant Biol 15(3):282–292. doi:10.1016/j.pbi.2012.03.016 PubMedGoogle Scholar
  130. Stitt M, Lunn J, Usadel B (2010) Arabidopsis and primary photosynthetic metabolism – more than the icing on the cake. Plant J 61(6):1067–1091. doi:10.1111/j.1365-313X.2010.04142.x PubMedGoogle Scholar
  131. Sulpice R, Flis A, Ivakov AA, Apelt F, Krohn N, Encke B, Abel C, Feil R, Lunn JE, Stitt M (2014) Arabidopsis coordinates the diurnal regulation of carbon allocation and growth across a wide range of photoperiods. Mol Plant 7(1):137–155. doi:10.1093/mp/sst127 PubMedGoogle Scholar
  132. Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143(4):606–616. doi:10.1016/j.cell.2010.10.020 PubMedGoogle Scholar
  133. Usadel B, Bläsing OE, Gibon Y, Retzlaff K, Höhne M, Günther M, Stitt M (2008) Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes. Plant Physiol 146(4):1834–1861. doi:10.1104/pp.107.115592 PubMedPubMedCentralGoogle Scholar
  134. Vernoux T, Wilson RC, Seeley KA, Reichheld JP, Muroy S, Brown S, Maughan SC, Cobbett CS, Van Montagu M, Inze D, May MJ, Sung ZR (2000) The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12(1):97–110PubMedPubMedCentralGoogle Scholar
  135. Wang Z, Tobin E (1998) Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93(7):1207–1217PubMedGoogle Scholar
  136. Wang L, Kim J, Somers DE (2013) Transcriptional corepressor TOPLESS complexes with pseudoresponse regulator proteins and histone deacetylases to regulate circadian transcription. Proc Natl Acad Sci U S A 110(2):761–766. doi:10.1073/pnas.1215010110 ADSPubMedGoogle Scholar
  137. Warren D, Wilkins M (1961) An endogenous rhythm in the rate of dark-fixation of carbon dioxide in leaves of Bryophyllum fedtschenkoi. Nature 191(4789):686–688. doi:10.1038/191686a0 ADSGoogle Scholar
  138. Webb AAR, Satake A (2015) Understanding circadian regulation of carbohydrate metabolism in Arabidopsis using mathematical models. Plant Cell Physiol 56(4):586–593. doi:10.1093/pcp/pcv033 PubMedGoogle Scholar
  139. Wilkins MB (1992) Tansley review No. 37 circadian rhythms: their origin and control. New Phytol 121:347–375Google Scholar
  140. Wilkinson SR, Welch RM, Mayland HF, Grunes DL (1990) Magnesium in plants: uptake, distribution, function and utilization by man and animals. In: Metal ions in biological systems, vol 26, p 33Google Scholar
  141. Wouters MA, Fan SW, Haworth NL (2010) Disulfides as redox switches: from molecular mechanisms to functional significance. Antioxid Redox Signal 12(1):53–91. doi:10.1089/ars.2009.2510 PubMedGoogle Scholar
  142. Xie Q, Wang P, Liu X, Yuan L, Wang L, Zhang C, Li Y, Xing H, Zhi L, Yue Z, Zhao C, McClung CR, Xu X (2014) LNK1 and LNK2 are transcriptional coactivators in the Arabidopsis circadian oscillator. Plant Cell 26(7):2843–2857. doi:10.1105/tpc.114.126573 PubMedPubMedCentralGoogle Scholar
  143. Yadav UP, Ivakov A, Feil R, Duan GY, Walther D, Giavalisco P, Piques M, Carillo P, Hubberten H-M, Stitt M, Lunn JE (2014) The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. J Exp Bot 65(4):1051–1068. doi:10.1093/jxb/ert457 PubMedPubMedCentralGoogle Scholar
  144. Young MW, Kay SA (2001) Time zones: a comparative genetics of circadian clocks. Nat Rev Genet 2(9):702–715. doi:10.1038/35088576 PubMedGoogle Scholar
  145. Young NL, Dimaggio PA, Garcia BA (2010) The significance, development and progress of high-throughput combinatorial histone code analysis. Cell Mol Life Sci 67(23):3983–4000. doi:10.1007/s00018-010-0475-7 PubMedGoogle Scholar
  146. Yu M, Lamattina L, Spoel SH, Loake GJ (2014) Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytol 202(4):1142–1156. doi:10.1111/nph.12739 PubMedGoogle Scholar
  147. Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61:209–234. doi:10.1146/annurev-arplant-042809-112301 PubMedGoogle Scholar
  148. Zhong HH, McClung CR (1996) The circadian clock gates expression of two Arabidopsis catalase genes to distinct and opposite circadian phases. Mol Gen Genet 251(2):196–203PubMedGoogle Scholar
  149. Zhou M, Wang W, Karapetyan S, Mwimba M, Marqués J, Buchler NE, Dong X (2015) Redox rhythm reinforces the circadian clock to gate immune response. Nature 523:472–476. doi:10.1038/nature14449 ADSPubMedPubMedCentralGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of EssexColchesterUK

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