Circadian regulation of hormone signaling and plant physiology

Abstract

The survival and reproduction of plants depend on their ability to cope with a wide range of daily and seasonal environmental fluctuations during their life cycle. Phytohormones are plant growth regulators that are involved in almost every aspect of growth and development as well as plant adaptation to myriad abiotic and biotic conditions. The circadian clock, an endogenous and cell-autonomous biological timekeeper that produces rhythmic outputs with close to 24-h rhythms, provides an adaptive advantage by synchronizing plant physiological and metabolic processes to the external environment. The circadian clock regulates phytohormone biosynthesis and signaling pathways to generate daily rhythms in hormone activity that fine-tune a range of plant processes, enhancing adaptation to local conditions. This review explores our current understanding of the interplay between the circadian clock and hormone signaling pathways.

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References

  1. Adams S, Carre IA (2011) Downstream of the plant circadian clock: output pathways for the control of physiology and development. Essays Biochem 49:53–69. doi:10.1042/BSE0490053

    CAS  PubMed  Article  Google Scholar 

  2. Adams S, Manfield I, Stockley P, Carre IA (2015) Revised morning loops of the Arabidopsis circadian clock based on analyses of direct regulatory interactions. PLoS One 10:e0143943. doi:10.1371/journal.pone.0143943

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  3. Angelmann W, Johnsson A (1998) Rhythms in organ movement. In: Lumsden PJ, Millar AJ (eds) Biological Rhythms and photoperiodism in plants, 1st edn. BIOS Scientific, Abingdon, pp 35–50

    Google Scholar 

  4. Arana MV, Marin-de la Rosa N, Maloof JN, Blazquez MA, Alabadi D (2011) Circadian oscillation of gibberellin signaling in Arabidopsis. Proc Natl Acad Sci USA 108:9292–9297. doi:10.1073/pnas.1101050108

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  5. Bancos S, Nomura T, Sato T, Molnar G, Bishop GJ, Koncz C, Yokota T et al (2002) Regulation of transcript levels of the Arabidopsis cytochrome p450 genes involved in brassinosteroid biosynthesis. Plant Physiol 130:504–513. doi:10.1104/pp.005439

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  6. Barta C, Loreta F (2006) The relationship between the methyl-erythritol phosphate pathway leading to emission of volatile isopreniods and abscisic acid content in leaves. Plant Physiol 141:1676–1683

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  7. Bernardo-Garcia S, de Lucas M, Martinez C, Espinosa-Ruiz A, Daviere JM, Prat S (2014) BR-dependent phosphorylation modulates PIF4 transcriptional activity and shapes diurnal hypocotyl growth. Genes Dev 28:1681–1694. doi:10.1101/gad.243675.114

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. 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. doi:10.1371/journal.pone.0026968

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. Blanco F, Salinas P, Cecchini NM, Jordana X, Van Hummelen P, Alvarez ME, Holuigue L (2009) Early genomic responses to salicylic acid in Arabidopsis. Plant Mol Biol 70:79–102. doi:10.1007/s11103-009-9458-1

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  11. Boden SA, Weiss D, Ross JJ, Davies NW, Trevaskis B, Chandler PM, Swain SM (2014) EARLY FLOWERING3 regulates flowering in spring barley by mediating gibberellin production and FLOWERING LOCUS T expression. Plant Cell 26:1557–1569. doi:10.1105/tpc.114.123794

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  12. Burschka C, Tenhunen JD, Hartung W (1983) Diurnal variations in abscisic acid content and stomatal response to applied abscisic acid in leaves of irrigated and non-irrigated Arbutus unedo plants under naturally fluctuating environmental conditions. Oecologia 58:128–131

    Article  Google Scholar 

  13. Carrera E, Jackson SD, Prat S (1999) Feedback control and diurnal regulation of gibberellin 20-oxidase transcript levels in potato. Plant Physiol 119:765–774

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  14. Covington MF, Harmer SL (2007) The circadian clock regulates auxin signaling and responses in Arabidopsis. PLoS Biol 5:e222. doi:10.1371/journal.pbio.0050222

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  15. 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:R130. doi:10.1186/gb-2008-9-8-r130

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  16. de Jong M, Leyser O (2012) Developmental plasticity in plants. Cold Spring Harb Symp Quant Biol 77:63–73. doi:10.1101/sqb.2012.77.014720

    PubMed  Article  Google Scholar 

  17. de Lucas M, Daviere JM, Rodriguez-Falcon M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C et al (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451:480–484. doi:10.1038/nature06520

    PubMed  Article  CAS  Google Scholar 

  18. Dempsey DA, Vlot AC, Wildermuth MC, Klessig DF (2011) Salicylic acid biosynthesis and metabolism. The Arabidopsis Book 9:e0156. doi:10.1199/tab.0156

    PubMed  PubMed Central  Article  Google Scholar 

  19. Dharmawardhana P, Ren L, Amarasinghe V, Monaco M, Thomason J, Ravenscroft D, McCouch S et al (2013) A genome scale metabolic network for rice and accompanying analysis of tryptophan, auxin and serotonin biosynthesis regulation under biotic stress. Rice 6:15. doi:10.1186/1939-8433-6-15

    PubMed  PubMed Central  Article  Google Scholar 

  20. Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hibberd JM et al (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633. doi:10.1126/science.1115581

    CAS  PubMed  Article  Google Scholar 

  21. Dodd AN, Gardner MJ, Hotta CT, Hubbard KE, Dalchau N, Love J, Assie JM et al (2007) The Arabidopsis circadian clock incorporates a cADPR-based feedback loop. Science 318:1789–1792

    CAS  PubMed  Article  Google Scholar 

  22. Dornbusch T, Michaud O, Xenarios I, Fankhauser C (2014) Differentially phased leaf growth and movements in Arabidopsis depend on coordinated circadian and light regulation. Plant Cell 26:3911–3921. doi:10.1105/tpc.114.129031

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. Dowson-Day MJ, Millar AJ (1999) Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis. Plant J 17:63–71

    CAS  PubMed  Article  Google Scholar 

  24. Emery RJN, Reid DM, Chinnappa CC (1994) Phenotypic plasticity of stem eiongation in two ecotypes of Stellaria longipes: the role of ethylene and response to wind. Plant Cell Environ 17:691–700

    Article  Google Scholar 

  25. Endo M, Shimizu H, Nohales MA, Araki T, Kay SA (2014) Tissue-specific clocks in Arabidopsis show asymmetric coupling. Nature 515:419–422. doi:10.1038/nature13919

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  26. Farre EM (2012) The regulation of plant growth by the circadian clock. Plant Biol 14:401–410. doi:10.1111/j.1438-8677.2011.00548.x

    CAS  PubMed  Article  Google Scholar 

  27. Farre EM, Weise SE (2012) The interactions between the circadian clock and primary metabolism. Curr Opin Plant Biol 15:293–300. doi:10.1016/j.pbi.2012.01.013

    CAS  PubMed  Article  Google Scholar 

  28. Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F, Chen L et al (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451:475–479. doi:10.1038/nature06448

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  29. Filichkin SA, Breton G, Priest HD, Dharmawardhana P, Jaiswal P, Fox SE, Michael TP et al (2011) Global profiling of rice and poplar transcriptomes highlights key conserved circadian-controlled pathways and cis-regulatory modules. PLoS One 6:e16907. doi:10.1371/journal.pone.0016907

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  30. 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. doi:10.4161/15592324.2014.992707

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  31. Finlayson SA, Lee IJ, Morgan PW (1998) Phytochrome B and the regulation of circadian ethylene production in sorghum. Plant Physiol 116:17–25

    CAS  PubMed Central  Article  Google Scholar 

  32. Fogelmark K, Troein C (2014) Rethinking transcriptional activation in the Arabidopsis circadian clock. PLoS Comput Biol 10:e1003705. doi:10.1371/journal.pcbi.1003705

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  33. Foster KR, Morgan PW (1995) Genetic regulation of development in Sorghum bicolor (IX. The ma3R allele disrupts diurnal control of gibberellin biosynthesis). Plant Physiol 108:337–343

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Franklin KA, Lee SH, Patel D, Kumar SV, Spartz AK, Gu C, Ye S et al (2011) Phytochrome-interacting factor 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc Natl Acad Sci USA 108:20231–20235. doi:10.1073/pnas.1110682108

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  35. Freschi L, Nievola CC, Rodrigues MA, Domingues DS, Van Sluys MA, Mercier H (2009) Thermoperiod affects the diurnal cycle of nitrate reductase expression and activity in pineapple plants by modulating the endogenous levels of cytokinins. Physiol Plantarum 137:201–212. doi:10.1111/j.1399-3054.2009.01283.x

    CAS  Article  Google Scholar 

  36. Fukuda H, Nakamichi N, Hisatsune M, Murase H, Mizuno T (2007) Synchronization of plant circadian oscillators with a phase delay effect of the vein network. Phys Rev Lett 99:098102. doi:10.1103/PhysRevLett.99.098102

    PubMed  Article  CAS  Google Scholar 

  37. Fukushima A, Kusano M, Nakamichi N, Kobayashi M, Hayashi N, Sakakibara H, Mizuno T et al (2009) Impact of clock-associated Arabidopsis pseudo-response regulators in metabolic coordination. Proc Natl Acad Sci USA 106:7251–7256. doi:10.1073/pnas.0900952106

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  38. Garcia-Martinez JL, Gil J (2002) Light regulation of gibberellin biosynthesis and mode of action. J Plant Growth Regul 20:354–368

    Article  CAS  Google Scholar 

  39. 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 USA 109:4674–4677. doi:10.1073/pnas.1116368109

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  40. Goodspeed D, Liu JD, Chehab EW, Sheng Z, Francisco M, Kliebenstein DJ, Braam J (2013) Postharvest circadian entrainment enhances crop pest resistance and phytochemical cycling. Curr Biol 23:1235–1241. doi:10.1016/j.cub.2013.05.034

    CAS  PubMed  Article  Google Scholar 

  41. Greenham K, McClung CR (2015) Integrating circadian dynamics with physiological processes in plants. Nat Rev Genet 16:598–610. doi:10.1038/nrg3976

    CAS  PubMed  Article  Google Scholar 

  42. Gupta R, Chakrabarty SK (2013) Gibberellic acid in plant: still a mystery unresolved. Plant Signal Behav. doi:10.4161/psb.25504

    Google Scholar 

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

    CAS  Article  Google Scholar 

  44. Haydon MJ, Mielczarek O, Robertson FC, Hubbard KE, Webb AA (2013) Photosynthetic entrainment of the Arabidopsis thaliana circadian clock. Nature 502:689–692. doi:10.1038/nature12603

    CAS  PubMed  Article  Google Scholar 

  45. Henson IE, Alagarswamy G, Mahalakshmi V, Bidinger FR (1982) Diurnal changes in endogenous abscisic acid in leaves of pearl millet (Pennisetum americanum (L.) Leeke) under field conditions. J Exp Bot 33:416–425

    CAS  Article  Google Scholar 

  46. Hevia MA, Canessa P, Muller-Esparza H, Larrondo LF (2015) A circadian oscillator in the fungus Botrytis cinerea regulates virulence when infecting Arabidopsis thaliana. Proc Natl Acad Sci USA 112:8744–8749. doi:10.1073/pnas.1508432112

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  47. Hisamatsu T, King RW, Helliwell CA, Koshioka M (2005) The involvement of gibberellin 20-oxidase genes in phytochrome-regulated petiole elongation of Arabidopsis. Plant Physiol 138:1106–1116. doi:10.1104/pp.104.059055

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  48. Hornitschek P, Kohnen MV, Lorrain S, Rougemont J, Ljung K, Lopez-Vidriero I, Franco-Zorrilla JM et al (2012) Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J 71:699–711. doi:10.1111/j.1365-313X.2012.05033.x

    CAS  PubMed  Article  Google Scholar 

  49. Hsu PY, Harmer SL (2012) Circadian phase has profound effects on differential expression analysis. PLoS One 7:e49853. doi:10.1371/journal.pone.0049853

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  50. Hsu PY, Harmer SL (2014) Wheels within wheels: the plant circadian system. Trends Plant Sci 19:240–249. doi:10.1016/j.tplants.2013.11.007

    CAS  PubMed  Article  Google Scholar 

  51. 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 336:75–79. doi:10.1126/science.1219075

    CAS  PubMed  Article  Google Scholar 

  52. Ingle RA, Stoker C, Stone W, Adams N, Smith R, Grant M, Carre I et al (2015) Jasmonate signalling drives time-of-day differences in susceptibility of Arabidopsis to the fungal pathogen Botrytis cinerea. Plant J 84:937–948. doi:10.1111/tpj.13050

    CAS  PubMed  Article  Google Scholar 

  53. James AB, Monreal JA, Nimmo GA, Kelly CL, Herzyk P, Jenkins GI, Nimmo HG (2008) The circadian clock in Arabidopsis roots is a simplified slave version of the clock in shoots. Science 322:1832–1835. doi:10.1126/science.1161403

    CAS  PubMed  Article  Google Scholar 

  54. Janardhan KV, Vasudeva N, Gopel NH (1973) Diurnal variation of endogenous auxin in arabica coffee leaves. J Plant Crops 1:93–95

    Google Scholar 

  55. Jasoni RL, Cothren JT, Morgan PW, Sohan DE (2000) Circadian ethylene production in cotton. Plant Growth Regul 00:1–7

    Google Scholar 

  56. Jouve L, Gaspar T, Kevers C, Greppin H, Degli Agosti R (1999) Involvement of indole-3-acetic acid in the circadian growth of the first internode of Arabidopsis. Planta 209:136–142

    CAS  PubMed  Article  Google Scholar 

  57. Kapuya JL, Hall MA (1977) Diurnal variations in endogenous ethylene levels in plants. New Phytol 79:233–237

    CAS  Article  Google Scholar 

  58. Khan S, Rowe SC, Harmon FG (2010) Coordination of the maize transcriptome by a conserved circadian clock. BMC Plant Biol 10:126. doi:10.1186/1471-2229-10-126

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  59. Kim JS, Jung HJ, Lee HJ, Kim KA, Goh CH, Woo Y, Oh SH et al (2008) Glycine-rich RNA-binding protein 7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. Plant J 55:455–466. doi:10.1111/j.1365-313X.2008.03518.x

    CAS  PubMed  Article  Google Scholar 

  60. Kim SG, Yon F, Gaquerel E, Gulati J, Baldwin IT (2011) Tissue specific diurnal rhythms of metabolites and their regulation during herbivore attack in a native tobacco, Nicotiana attenuata. PloS One 6:e26214. doi:10.1371/journal.pone.0026214

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  61. Kinoshita T, Ono N, Hayashi Y, Morimoto S, Nakamura S, Soda M, Kato Y et al (2011) FLOWERING LOCUS T regulates stomatal opening. Curr Biol 21:1232–1238. doi:10.1016/j.cub.2011.06.025

    CAS  PubMed  Article  Google Scholar 

  62. Koini MA, Alvey L, Allen T, Tilley CA, Harberd NP, Whitelam GC, Franklin KA (2009) High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr Biol 19:408–413. doi:10.1016/j.cub.2009.01.046

    CAS  PubMed  Article  Google Scholar 

  63. 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. doi:10.1093/pcp/pcu092

    CAS  PubMed  Article  Google Scholar 

  64. Krekule J, Pavlova L, Souckova D, Machackova I (1985) Auxin in flowering of short-day and long-day Chenopodium species. Biol Plantarum 27:310–317

    CAS  Article  Google Scholar 

  65. 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. doi:10.1093/pcp/pcr076

    CAS  PubMed  Article  Google Scholar 

  66. Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331

    CAS  PubMed  Article  Google Scholar 

  67. Lecoq C, Koukkari WL, Brenner ML (1983) Rhythmic changes in abscisic acid (ABA) content of soybean leaves. Plant Physiol 72:52

    Google Scholar 

  68. Lee MH, Seo SW, Ota Y (1981) Diurnal variation in ethylene evolution in leaf and panicle. JPN J Crop Sci 50:396–400

    Article  Google Scholar 

  69. Lee IJ, Foster KR, Morgan PW (1998) Photoperiod control of gibberellin levels and flowering in sorghum. Plant Physiol 116:1003–1011

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  70. Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, Hartung W, Hwang I et al (2006) Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126:1109–1120. doi:10.1016/j.cell.2006.07.034

    CAS  PubMed  Article  Google Scholar 

  71. Lee HG, Mas P, Seo PJ (2016) MYB96 shapes the circadian gating of ABA signaling in Arabidopsis. Sci Rep 6:17754. doi:10.1038/srep17754

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  72. Lipe JA, Morgan PW (1973) Ethylene, a regulator of young fruit abscission. Plant Physiol 51:949–953

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  73. Liu T, Carlsson J, Takeuchi T, Newton L, Farre EM (2013) Direct regulation of abiotic responses by the Arabidopsis circadian clock component PRR7. Plant J 76:101–114. doi:10.1111/tpj.12276

    CAS  PubMed  Google Scholar 

  74. Liu D, Hu R, Palla KJ, Tuskan GA, Yang X (2016a) Advances and perspectives on the use of CRISPR/Cas9 systems in plant genomics research. Curr Opin Plant Biol 30:70–77. doi:10.1016/j.pbi.2016.01.007

    CAS  PubMed  Article  Google Scholar 

  75. Liu TL, Newton L, Liu MJ, Shiu SH, Farre EM (2016b) A G-box-like motif is necessary for transcriptional regulation by circadian pseudo-response regulators in Arabidopsis. Plant Physiol 170:528–539. doi:10.1104/pp.15.01562

    CAS  PubMed  Article  Google Scholar 

  76. Lund ST, Stall RE, Klee HJ (1998) Ethylene regulates the susceptible response to pathogen infection in tomato. Plant Cell 10:371–382

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  77. Machackova I, Chauvaux N, Dewitte W, Van Onckelen H (1997) Diurnal fluctuations in ethylene formation in Chenopodium rubrum. Plant Physiol 113:981–985

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Mano Y, Nemoto K (2012) The pathway of auxin biosynthesis in plants. J Exp Bot 63:2853–2872. doi:10.1093/jxb/ers091

    CAS  PubMed  Article  Google Scholar 

  79. McClung CR (2014) Wheels within wheels: new transcriptional feedback loops in the Arabidopsis circadian clock. F1000Prime Rep 6:2. doi:10.12703/P6-2

    PubMed  PubMed Central  Article  CAS  Google Scholar 

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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  81. Michael TP, Mockler TC, Breton G, McEntee C, Byer A, Trout JD, Hazen SP et al (2008b) Network discovery pipeline elucidates conserved time-of-day-specific cis-regulatory modules. PLoS Genet 4:e14. doi:10.1371/journal.pgen.0040014

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  82. Mir R, Hernandez ML, Abou-Mansour E, Martinez-Rivas JM, Mauch F, Metraux JP, Leon J (2013) Pathogen and Circadian Controlled 1 (PCC1) regulates polar lipid content, ABA-related responses, and pathogen defence in Arabidopsis thaliana. J Exp Bot 64:3385–3395. doi:10.1093/jxb/ert177

    CAS  PubMed  Article  Google Scholar 

  83. 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. doi:10.1093/pcp/pcn008

    CAS  PubMed  Article  Google Scholar 

  84. Mohawk JA, Green CB, Takahashi JS (2012) Central and peripheral circadian clocks in mammals. Annu Rev Neurosci 35:445–462. doi:10.1146/annurev-neuro-060909-153128

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  85. Morgan PW, He CJ, De Greef JA, De Proft MP (1990) Does water deficit stress promote ethylene synthesis by intact plants? Plant Physiol 94:1616–1624

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  86. Muller LM, von Korff M, Davis SJ (2014) Connections between circadian clocks and carbon metabolism reveal species-specific effects on growth control. J Exp Bot 65:2915–2923. doi:10.1093/jxb/eru117

    PubMed  Article  Google Scholar 

  87. Myster J, Junttila O, Lindgard B, Moe R (1997) Temperature alternations and the influence of gibberellins and indoleacetic acid on elongation growth and fowering of Begonia x hiemalis Fotsch. Plant Growth Regul 21:135–144

    CAS  Article  Google Scholar 

  88. Nagel DH, Doherty CJ, Pruneda-Paz JL, Schmitz RJ, Ecker JR, Kay SA (2015) Genome-wide identification of CCA1 targets uncovers an expanded clock network in Arabidopsis. Proc Natl Acad Sci USA. doi:10.1073/pnas.1513609112

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  90. Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126:467–475. doi:10.1016/j.cell.2006.05.050

    CAS  PubMed  Article  Google Scholar 

  91. Nicaise V, Joe A, Jeong BR, Korneli C, Boutrot F, Westedt I, Staiger D et al (2013) Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. EMBO J 32:701–712. doi:10.1038/emboj.2013.15

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  92. Nieto C, Lopez-Salmeron V, Daviere JM, Prat S (2015) ELF3-PIF4 interaction regulates plant growth independently of the Evening Complex. Curr Biol 25:187–193. doi:10.1016/j.cub.2014.10.070

    CAS  PubMed  Article  Google Scholar 

  93. Nose M, Watanabe A (2014) Clock genes and diurnal transcriptome dynamics in summer and winter in the gymnosperm Japanese cedar (Cryptomeria japonica (L.f.) D.Don). BMC Plant Biol 14:308. doi:10.1186/s12870-014-0308-1

    PubMed  PubMed Central  Google Scholar 

  94. Novakova M, Motyka V, Dobrev PI, Malbeck J, Gaudinova A, Vankova R (2005) Diurnal variation of cytokinin, auxin and abscisic acid levels in tobacco leaves. J Exp Bot 56:2877–2883. doi:10.1093/jxb/eri282

    CAS  PubMed  Article  Google Scholar 

  95. 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. doi:10.1038/nature05946

    CAS  PubMed  Article  Google Scholar 

  96. Nozue K, Harmer SL, Maloof JN (2011) Genomic analysis of circadian clock-, light-, and growth-correlated genes reveals PHYTOCHROME-INTERACTING FACTOR5 as a modulator of auxin signaling in Arabidopsis. Plant Physiol 156:357–372. doi:10.1104/pp.111.172684

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  97. Nusinow DA, Helfer A, Hamilton EE, King JJ, Imaizumi T, Schultz TF, Farre EM et al (2011) The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475:398–402. doi:10.1038/nature10182

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  98. Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci USA 95:8660–8664

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  99. Pavlova L, Krekule J (1984) Fluctuation of free IAA under inductive and non-inductive photoperiods in Chenopodium rubrum. Plant Growth Regul 2:91–98

    CAS  Article  Google Scholar 

  100. Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521. doi:10.1146/annurev-cellbio-092910-154055

    CAS  PubMed  Article  Google Scholar 

  101. Pokhilko A, Bou-Torrent J, Pulido P, Rodriguez-Concepcion M, Ebenhoh O (2015) Mathematical modelling of the diurnal regulation of the MEP pathway in Arabidopsis. New Phytol 206:1075–1085. doi:10.1111/nph.13258

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  103. Rieu I, Cristescu SM, Harren FJ, Huibers W, Voesenek LA, Mariani C, Vriezen WH (2005) RP-ACS1, a flooding-induced 1-aminocyclopropane-1-carboxylate synthase gene of Rumex palustris, is involved in rhythmic ethylene production. J Exp Bot 56:841–849. doi:10.1093/jxb/eri078

    CAS  PubMed  Article  Google Scholar 

  104. Ruiz-Sola MA, Rodriguez-Concepcion M (2012) Carotenoid biosynthesis in Arabidopsis: a colorful pathway. The Arabidopsis Book 10:e0158. doi:10.1199/tab.0158

    PubMed  PubMed Central  Article  Google Scholar 

  105. Ruts T, Matsubara S, Wiese-Klinkenberg A, Walter A (2012) Diel patterns of leaf and root growth: endogenous rhythmicity or environmental response? J Exp Bot 63:3339–3351. doi:10.1093/jxb/err334

    CAS  PubMed  Article  Google Scholar 

  106. Salome PA, To JP, Kieber JJ, McClung CR (2006) Arabidopsis response regulators ARR3 and ARR4 play cytokinin-independent roles in the control of circadian period. Plant Cell 18:55–69. doi:10.1105/tpc.105.037994

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  107. Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655–11660. doi:10.1073/pnas.97.21.11655

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  108. Shapiro DJ, Rodwell VW (1969) Diurnal variation and cholesterol regulation of hepatic HMG-CoA reductase activity. Biochem Biophys Res Commun 37:867–872

    CAS  PubMed  Article  Google Scholar 

  109. Shimizu H, Katayama K, Koto T, Torii K, Araki T, Endo M (2015) Decentralized circadian clocks process thermal and photoperiodic cues in specific tissues. Nat Plants. doi:10.1038/nplants.2015.163

    Google Scholar 

  110. Shin J, Heidrich K, Sanchez-Villarreal A, Parker JE, Davis SJ (2012) TIME FOR COFFEE represses accumulation of the MYC2 transcription factor to provide time-of-day regulation of jasmonate signaling in Arabidopsis. Plant Cell 24:2470–2482. doi:10.1105/tpc.111.095430

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  111. Song YH, Shim JS, Kinmonth-Schultz HA, Imaizumi T (2015) Photoperiodic flowering: time measurement mechanisms in leaves. Annu Rev Plant Biol 66:441–464. doi:10.1146/annurev-arplant-043014-115555

    CAS  PubMed  Article  Google Scholar 

  112. Spoelstra K, Wikelski M, Daan S, Loudon AS, Hau M (2016) Natural selection against a circadian clock gene mutation in mice. Proc Natl Acad Sci USA 113:686–691. doi:10.1073/pnas.1516442113

    CAS  PubMed  Article  Google Scholar 

  113. Stavang JA, Lindgard B, Erntsen A, Lid SE, Moe R, Olsen JE (2005) Thermoperiodic stem elongation involves transcriptional regulation of gibberellin deactivation in pea. Plant Physiol 138:2344–2353. doi:10.1104/pp.105.063149

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  114. Takahashi N, Hirata Y, Aihara K, Mas P (2015) A hierarchical multi-oscillator network orchestrates the Arabidopsis circadian system. Cell 163:148–159. doi:10.1016/j.cell.2015.08.062

    CAS  PubMed  Article  Google Scholar 

  115. Talon M, Zeevaart JA, Gage DA (1991) Identification of gibberellins in spinach and effects of light and darkness on their levels. Plant Physiol 97:1521–1526

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  116. Thain SC, Hall A, Millar AJ (2000) Functional independence of circadian clocks that regulate plant gene expression. Curr Biol 10:951–956

    CAS  PubMed  Article  Google Scholar 

  117. Thain SC, Vandenbussche F, Laarhoven LJ, Dowson-Day MJ, Wang ZY, Tobin EM, Harren FJ et al (2004) Circadian rhythms of ethylene emission in Arabidopsis. Plant Physiol 136:3751–3761. doi:10.1104/pp.104.042523

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  118. Thomma BPHJ, Penninckx IAMA, Cammue BPA, Broekaert WF (2001) The complexity of disease signaling in Arabidopsis. Curr Opin Immunol 13:63–68

    CAS  PubMed  Article  Google Scholar 

  119. Thompson AJ, Jackson AC, Parker RA, Morpeth DR, Burbidge A, Taylor IB (2000) Abscisic acid biosynthesis in tomato: regulation of zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase mRNAs by light/dark cycles, water stress and abscisic acid. Plant Mol Biol 42:833–845

    CAS  PubMed  Article  Google Scholar 

  120. Velho do Amaral LI, Santo HP, Rossatto DR, Buckeridge MS (2012) Diurnal changes in storage carbohydrate metabolism in cotyledons of the tropical tree Hymenaea courbaril L. (Leguminosae). Braz J Bot 35:347–355

    Article  Google Scholar 

  121. Vranova E, Coman D, Gruissem W (2013) Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu Rev Plant Biol 64:665–700. doi:10.1146/annurev-arplant-050312-120116

    CAS  PubMed  Article  Google Scholar 

  122. Wang KL, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14(Suppl):S131–S151

    CAS  PubMed  PubMed Central  Google Scholar 

  123. Wang W, Barnaby JY, Tada Y, Li H, Tor M, Caldelari D, Lee DU et al (2011) Timing of plant immune responses by a central circadian regulator. Nature 470:110–114. doi:10.1038/nature09766

    CAS  PubMed  Article  Google Scholar 

  124. Wang D, Mills ES, Deal RB (2012) Technologies for systems-level analysis of specific cell types in plants. Plant Sci 197:21–29. doi:10.1016/j.plantsci.2012.08.012

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  125. Wang G, Zhang C, Battle S, Lu H (2014) The phosphate transporter PHT4;1 is a salicylic acid regulator likely controlled by the circadian clock protein CCA1. Front Plant Sci 5:701. doi:10.3389/fpls.2014.00701

    PubMed  PubMed Central  Google Scholar 

  126. Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 111:1021–1058. doi:10.1093/aob/mct067

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  127. Webb AAR (1998) Stomatal rhythms. In: Lumsden PJ, Millar AJ (eds) Biological rhythms and photoperiodism in plants. BIOS Scientific Publishers, Oxford, pp 69–79

    Google Scholar 

  128. Wenden B, Toner DL, Hodge SK, Grima R, Millar AJ (2012) Spontaneous spatiotemporal waves of gene expression from biological clocks in the leaf. Proc Natl Acad Sci USA 109:6757–6762. doi:10.1073/pnas.1118814109

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  129. Went FW, Thimann KV (1937) Phytohormones. The Macmillan Company, New York

    Google Scholar 

  130. Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565. doi:10.1038/35107108

    CAS  PubMed  Article  Google Scholar 

  131. Xu ZY, Kim DH, Hwang I (2013) ABA homeostasis and signaling involving multiple subcellular compartments and multiple receptors. Plant Cell Rep 32:807–813. doi:10.1007/s00299-013-1396-3

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  133. Yates SA, Chernukhin I, Alvarez-Fernandez R, Bechtold U, Baeshen M, Baeshen N, Mutwakil MZ et al (2014) The temporal foliar transcriptome of the perennial C3 desert plant Rhazya stricta in its natural environment. BMC Plant Biol 14:2. doi:10.1186/1471-2229-14-2

    PubMed  PubMed Central  Article  Google Scholar 

  134. Yue J, Hu X, Huang J (2014) Origin of plant auxin biosynthesis. Trends Plant Sci 19:764–770. doi:10.1016/j.tplants.2014.07.004

    CAS  PubMed  Article  Google Scholar 

  135. Zhang C, Xie Q, Anderson RG, Ng G, Seitz NC, Peterson T, McClung CR et al (2013) Crosstalk between the circadian clock and innate immunity in Arabidopsis. PLoS Pathog 9:e1003370. doi:10.1371/journal.ppat.1003370

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  136. Zhao B, Li J (2012) Regulation of brassinosteroid biosynthesis and inactivation. J Integr Plant Biol 54:746–759. doi:10.1111/j.1744-7909.2012.01168.x

    CAS  PubMed  Article  Google Scholar 

  137. Zhao X, Yu X, Foo E, Symons GM, Lopez J, Bendehakkalu KT, Xiang J et al (2007) A study of gibberellin homeostasis and cryptochrome-mediated blue light inhibition of hypocotyl elongation. Plant Physiol 145:106–118. doi:10.1104/pp.107.099838

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  138. Zheng B, Deng Y, Mu J, Ji Z, Xiang T, Niu Q-W, Chua N-H et al (2006) Cytokinin affects circadian-clock oscillation in a phytochrome B- and Arabidopsis response regulator 4-dependent manner. Physiol Plant 127:277–292

    CAS  Article  Google Scholar 

  139. Zheng XY, Zhou M, Yoo H, Pruneda-Paz JL, Spivey NW, Kay SA, Dong X (2015) Spatial and temporal regulation of biosynthesis of the plant immune signal salicylic acid. Proc Natl Acad Sci USA 112:9166–9173. doi:10.1073/pnas.1511182112

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  140. Zhou M, Wang W, Karapetyan S, Mwimba M, Marques J, Buchler NE, Dong X (2015) Redox rhythm reinforces the circadian clock to gate immune response. Nature 523:472–476. doi:10.1038/nature14449

    PubMed  PubMed Central  Article  CAS  Google Scholar 

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Acknowledgments

Work in the Harmer laboratory is supported by Grants R01 GM 069418 from the National Institutes of Health and IOS 1238040 from the National Science Foundation.

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H.S.A and S.L.H both contributed to the writing of this manuscript.

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Correspondence to Stacey L. Harmer.

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Atamian, H.S., Harmer, S.L. Circadian regulation of hormone signaling and plant physiology. Plant Mol Biol 91, 691–702 (2016). https://doi.org/10.1007/s11103-016-0477-4

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Keywords

  • Circadian clock
  • Hormone
  • Signaling
  • Growth
  • Immunity
  • Adaptation