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Annual Review of Plant Biology

Volume 67, 2016

The Intracellular Dynamics of Circadian Clocks Reach for the Light of Ecology and Evolution

Abstract

A major challenge for biology is to extend our understanding of molecular regulation from the simplified conditions of the laboratory to ecologically relevant environments. Tractable examples are essential to make these connections for complex, pleiotropic regulators and, to go further, to link relevant genome sequences to field traits. Here, I review the case for the biological clock in higher plants. The gene network of the circadian clock drives pervasive, 24-hour rhythms in metabolism, behavior, and physiology across the eukaryotes and in some prokaryotes. In plants, the scope of chronobiology is now extending from the most tractable, intracellular readouts to the clock's many effects at the whole-organism level and across the life cycle, including biomass and flowering. I discuss five research areas where recent progress might be integrated in the future, to understand not only circadian functions in natural conditions but also the evolution of the clock's molecular mechanisms.

Keyword(s): Arabidopsis thaliana, biological clocks, circadian rhythms, flowering, plant photoperiodism, systems biology
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2016-04-29
2024-05-01
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Literature Cited

  1. Anderson SL, Teakle GR, Martino-Catt SJ, Kay SA. 1.  1994. Circadian clock- and phytochrome-regulated transcription is conferred by a 78 bp cis-acting domain of the Arabidopsis CAB2 promoter. Plant J. 6:457–70 [Google Scholar]
  2. Anwer MU, Boikoglou E, Herrero E, Hallstein M, Davis AM. 2.  et al. 2014. Natural variation reveals that intracellular distribution of ELF3 protein is associated with function in the circadian clock. eLife 3:e02206 [Google Scholar]
  3. Anwer MU, Davis SJ. 3.  2013. An overview of natural variation studies in the Arabidopsis thaliana circadian clock. Semin. Cell Dev. Biol. 24:422–29 [Google Scholar]
  4. Barneche F, Malapeira J, Mas P. 4.  2014. The impact of chromatin dynamics on plant light responses and circadian clock function. J. Exp. Bot. 65:2895–913 [Google Scholar]
  5. Beale A, Guibal C, Tamai TK, Klotz L, Cowen S. 5.  et al. 2013. Circadian rhythms in Mexican blind cavefish Astyanax mexicanus in the lab and in the field. Nat. Commun. 4:2769 [Google Scholar]
  6. Bieniawska Z, Espinoza C, Schlereth A, Sulpice R, Hincha DK, Hannah MA. 6.  2008. Disruption of the Arabidopsis circadian clock is responsible for extensive variation in the cold-responsive transcriptome. Plant Physiol. 147:263–79 [Google Scholar]
  7. Boden SA, Weiss D, Ross JJ, Davies NW, Trevaskis B. 7.  et al. 2014. EARLY FLOWERING3 regulates flowering in spring barley by mediating gibberellin production and FLOWERING LOCUS T expression. Plant Cell 26:1557–69 [Google Scholar]
  8. Bohlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S. 8.  et al. 2006. CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–43 [Google Scholar]
  9. Boikoglou E, Ma Z, von Korff M, Davis AM, Nagy F, Davis SJ. 9.  2011. Environmental memory from a circadian oscillator: The Arabidopsis thaliana clock differentially integrates perception of photic versus thermal entrainment. Genetics 189:655–64 [Google Scholar]
  10. Bouget FY, Lefranc M, Thommen Q, Pfeuty B, Lozano JC. 10.  et al. 2014. Transcriptional versus non-transcriptional clocks: a case study in Ostreococcus. Mar. Genomics 14:17–22 [Google Scholar]
  11. Bujdoso N, Davis SJ. 11.  2013. Mathematical modeling of an oscillating gene circuit to unravel the circadian clock network of Arabidopsis thaliana. Front. Plant Sci. 4:3 [Google Scholar]
  12. Calixto CP, Waugh R, Brown JW. 12.  2015. Evolutionary relationships among barley and Arabidopsis core circadian clock and clock-associated genes. J. Mol. Evol. 80:108–19 [Google Scholar]
  13. Campoli C, Pankin A, Drosse B, Casao CM, Davis SJ, von Korff M. 13.  2013. HvLUX1 is a candidate gene underlying the early maturity 10 locus in barley: phylogeny, diversity, and interactions with the circadian clock and photoperiodic pathways. New Phytol. 199:1045–59 [Google Scholar]
  14. Campoli C, Shtaya M, Davis SJ, von Korff M. 14.  2012. Expression conservation within the circadian clock of a monocot: Natural variation at barley Ppd-H1 affects circadian expression of flowering time genes, but not clock orthologs. BMC Plant Biol. 12:97 [Google Scholar]
  15. Carre I, Veflingstad SR. 15.  2013. Emerging design principles in the Arabidopsis circadian clock. Semin. Cell Dev. Biol. 24:393–98 [Google Scholar]
  16. Causton HC, Feeney KA, Ziegler CA, O'Neill JS. 16.  2015. Metabolic cycles in yeast share features conserved among circadian rhythms. Curr. Biol. 25:1056–62 [Google Scholar]
  17. Chen J, Kallman T, Ma X, Gyllenstrand N, Zaina G. 17.  et al. 2012. Disentangling the roles of history and local selection in shaping clinal variation of allele frequencies and gene expression in Norway spruce (Picea abies). Genetics 191:865–81 [Google Scholar]
  18. Chen J, Tsuda Y, Stocks M, Kallman T, Xu N. 18.  et al. 2014. Clinal variation at phenology-related genes in spruce: parallel evolution in FTL2 and Gigantea?. Genetics 197:1025–38 [Google Scholar]
  19. Chew YH, Wenden B, Flis A, Mengin V, Taylor J. 19.  et al. 2014. Multiscale digital Arabidopsis predicts individual organ and whole-organism growth. PNAS 111:E4127–36 [Google Scholar]
  20. Cho CS, Yoon HJ, Kim JY, Woo HA, Rhee SG. 20.  2014. Circadian rhythm of hyperoxidized peroxiredoxin II is determined by hemoglobin autoxidation and the 20S proteasome in red blood cells. PNAS 111:12043–48 [Google Scholar]
  21. Corbesier L, Vincent C, Jang S, Fornara F, Fan Q. 21.  et al. 2007. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–33 [Google Scholar]
  22. Corellou F, Schwartz C, Motta JP, Djouani-Tahri EB, Sanchez F, Bouget FY. 22.  2009. Clocks in the green lineage: comparative functional analysis of the circadian architecture of the picoeukaryote Ostreococcus. Plant Cell 21:3436–49 [Google Scholar]
  23. Covington MF, Maloof JN, Straume M, Kay SA, Harmer SL. 23.  2008. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol. 9:R130 [Google Scholar]
  24. Daan S. 24.  2010. A history of chronobiological concepts. Protein Rev. 12:1–35 [Google Scholar]
  25. Dally N, Xiao K, Holtgrawe D, Jung C. 25.  2014. The B2 flowering time locus of beet encodes a zinc finger transcription factor. PNAS 111:10365–70 [Google Scholar]
  26. Daniels BC, Chen YJ, Sethna JP, Gutenkunst RN, Myers CR. 26.  2008. Sloppiness, robustness, and evolvability in systems biology. Curr. Opin. Biotechnol. 19:389–95 [Google Scholar]
  27. Darrah C, Taylor BL, Edwards KD, Brown PE, Hall A, McWatters HG. 27.  2006. Analysis of phase of LUCIFERASE expression reveals novel circadian quantitative trait loci in Arabidopsis. Plant Physiol. 140:1464–74 [Google Scholar]
  28. Davey C, Ougham H, Millar A, Thomas H, Tindal C, Muetzelfeldt R. 28.  2009. PlaSMo: making existing plant and crop mathematical models available to plant systems biologists. Comp. Biochem. Physiol. A 153A:S225–26 [Google Scholar]
  29. de Dios VR, Roy J, Ferrio JP, Alday JG, Landais D. 29.  et al. 2015. Processes driving nocturnal transpiration and implications for estimating land evapotranspiration. Sci. Rep. 5:10975 [Google Scholar]
  30. de Montaigu A, Giakountis A, Rubin M, Toth R, Cremer F. 30.  et al. 2015. Natural diversity in daily rhythms of gene expression contributes to phenotypic variation. PNAS 112:905–10 [Google Scholar]
  31. Dixon LE, Hodge SK, van Ooijen G, Troein C, Akman OE, Millar AJ. 31.  2014. Light and circadian regulation of clock components aids flexible responses to environmental signals. New Phytol. 203:568–77 [Google Scholar]
  32. Dixon LE, Knox K, Kozma-Bognar L, Southern MM, Pokhilko A, Millar AJ. 32.  2011. Temporal repression of core circadian genes is mediated through EARLY FLOWERING 3 in Arabidopsis. Curr. Biol. 21:120–25 [Google Scholar]
  33. Dodd AN, Dalchau N, Gardner MJ, Baek SJ, Webb AA. 33.  2014. The circadian clock has transient plasticity of period and is required for timing of nocturnal processes in Arabidopsis. New Phytol. 201:168–79 [Google Scholar]
  34. Dodd AN, Kusakina J, Hall A, Gould PD, Hanaoka M. 34.  2014. The circadian regulation of photosynthesis. Photosynth. Res. 119:181–90 [Google Scholar]
  35. Dodd AN, Salathia N, Hall A, Kevei E, Toth R. 35.  et al. 2005. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–33 [Google Scholar]
  36. Domijan M, Rand DA. 36.  2011. Balance equations can buffer noisy and sustained environmental perturbations of circadian clocks. Interface Focus 1:177–86 [Google Scholar]
  37. Donohue K, Burghardt LT, Runcie D, Bradford KJ, Schmitt J. 37.  2015. Applying developmental threshold models to evolutionary ecology. Trends Ecol. Evol. 30:66–77 [Google Scholar]
  38. Dornbusch T, Michaud O, Xenarios I, Fankhauser C. 38.  2014. Differentially phased leaf growth and movements in Arabidopsis depend on coordinated circadian and light regulation. Plant Cell 26:3911–21 [Google Scholar]
  39. Doughty CE, Goulden ML, Miller SD, da Rocha HR. 39.  2006. Circadian rhythms constrain leaf and canopy gas exchange in an Amazonian forest. Geophys. Res. Lett. 33:L15404 [Google Scholar]
  40. Dunlap JC, Loros JJ, DeCoursey PJ. 40.  2003. Chronobiology: Biological Timekeeping Sunderland, MA: Sinauer
  41. Edwards KD, Akman OE, Knox K, Lumsden PJ, Thomson AW. 41.  et al. 2010. Quantitative analysis of regulatory flexibility under changing environmental conditions. Mol. Syst. Biol. 6:424 [Google Scholar]
  42. Edwards KD, Anderson PE, Hall A, Salathia NS, Locke JC. 42.  et al. 2006. FLOWERING LOCUS C mediates natural variation in the high-temperature response of the Arabidopsis circadian clock. Plant Cell 18:639–50 [Google Scholar]
  43. Edwards KD, Lynn JR, Gyula P, Nagy F, Millar AJ. 43.  2005. Natural allelic variation in the temperature-compensation mechanisms of the Arabidopsis thaliana circadian clock. Genetics 170:387–400 [Google Scholar]
  44. Eelderink-Chen Z, Mazzotta G, Sturre M, Bosman J, Roenneberg T, Merrow M. 44.  2010. A circadian clock in Saccharomyces cerevisiae. PNAS 107:2043–47 [Google Scholar]
  45. Endo M, Shimizu H, Nohales MA, Araki T, Kay SA. 45.  2014. Tissue-specific clocks in Arabidopsis show asymmetric coupling. Nature 515:419–22 [Google Scholar]
  46. Farre EM, Harmer SL, Harmon FG, Yanovsky MJ, Kay SA. 46.  2005. Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Curr. Biol. 15:47–54 [Google Scholar]
  47. Feillet C, Krusche P, Tamanini F, Janssens RC, Downey MJ. 47.  et al. 2014. Phase locking and multiple oscillating attractors for the coupled mammalian clock and cell cycle. PNAS 111:9828–33 [Google Scholar]
  48. Fenske MP, Hewett Hazelton KD, Hempton AK, Shim JS, Yamamoto BM. 48.  et al. 2015. Circadian clock gene LATE ELONGATED HYPOCOTYL directly regulates the timing of floral scent emission in Petunia. PNAS 112:9775–80 [Google Scholar]
  49. Flis A, Piñas Fernández A, Zielinski T, Mengin V, Sulpice R. 49.  et al. 2015. Defining the robust behaviour of the plant clock gene circuit with absolute RNA timeseries and open infrastructure. Open Biol 5:150042 [Google Scholar]
  50. Fogelmark K, Troein C. 50.  2014. Rethinking transcriptional activation in the Arabidopsis circadian clock. PLOS Comput. Biol. 10:e1003705 [Google Scholar]
  51. Franco-Zorrilla JM, Lopez-Vidriero I, Carrasco JL, Godoy M, Vera P, Solano R. 51.  2014. DNA-binding specificities of plant transcription factors and their potential to define target genes. PNAS 111:2367–72 [Google Scholar]
  52. Fukuda H, Ukai K, Oyama T. 52.  2012. Self-arrangement of cellular circadian rhythms through phase-resetting in plant roots. Phys. Rev. E 86:041917 [Google Scholar]
  53. Gawronski P, Ariyadasa R, Himmelbach A, Poursarebani N, Kilian B. 53.  et al. 2014. A distorted circadian clock causes early flowering and temperature-dependent variation in spike development in the Eps-3Am mutant of einkorn wheat. Genetics 196:1253–61 [Google Scholar]
  54. Gehan MA, Greenham K, Mockler TC, McClung CR. 54.  2015. Transcriptional networks—crops, clocks, and abiotic stress. Curr. Opin. Plant Biol. 24:39–46 [Google Scholar]
  55. Gendron JM, Pruneda-Paz JL, Doherty CJ, Gross AM, Kang SE, Kay SA. 55.  2012. Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor. PNAS 109:3167–72 [Google Scholar]
  56. Goodspeed D, Chehab EW, Min-Venditti A, Braam J, Covington MF. 56.  2012. Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior. PNAS 109:4674–77 [Google Scholar]
  57. Gould PD, Ugarte N, Domijan M, Costa M, Foreman J. 57.  et al. 2013. Network balance via CRY signalling controls the Arabidopsis circadian clock over ambient temperatures. Mol. Syst. Biol. 9:650 [Google Scholar]
  58. Graf A, Schlereth A, Stitt M, Smith AM. 58.  2010. Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. PNAS 107:9458–63 [Google Scholar]
  59. Gyllenstrand N, Karlgren A, Clapham D, Holm K, Hall A. 59.  et al. 2014. No time for spruce: rapid dampening of circadian rhythms in Picea abies (L. Karst). Plant Cell Physiol. 55:535–50 [Google Scholar]
  60. Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B. 60.  et al. 2000. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290:2110–13 [Google Scholar]
  61. Hayama R, Agashe B, Luley E, King R, Coupland G. 61.  2007. A circadian rhythm set by dusk determines the expression of FT homologs and the short-day photoperiodic flowering response in Pharbitis. Plant Cell 19:2988–3000 [Google Scholar]
  62. Haydon MJ, Hearn TJ, Bell LJ, Hannah MA, Webb AA. 62.  2013. Metabolic regulation of circadian clocks. Semin. Cell Dev. Biol. 24:414–21 [Google Scholar]
  63. Helfer A, Nusinow DA, Chow BY, Gehrke AR, Bulyk ML, Kay SA. 63.  2011. LUX ARRHYTHMO encodes a nighttime repressor of circadian gene expression in the Arabidopsis core clock. Curr. Biol. 21:126–33 [Google Scholar]
  64. Herrero E, Kolmos E, Bujdoso N, Yuan Y, Wang M. 64.  et al. 2012. EARLY FLOWERING4 recruitment of EARLY FLOWERING3 in the nucleus sustains the Arabidopsis circadian clock. Plant Cell 24:428–43 [Google Scholar]
  65. Highkin HR, Hanson JB. 65.  1954. Possible interactions between light-dark cycles and endogenous daily rhythms on the growth of tomato plants. Plant Physiol. 29:301–2 [Google Scholar]
  66. Hoyle NP, O'Neill JS. 66.  2015. Oxidation-reduction cycles of peroxiredoxin proteins and nontranscriptional aspects of timekeeping. Biochemistry 54:184–93 [Google Scholar]
  67. Hsu PY, Devisetty UK, Harmer SL. 67.  2013. Accurate timekeeping is controlled by a cycling activator in Arabidopsis. eLife 2:e00473 [Google Scholar]
  68. Hsu PY, Harmer SL. 68.  2014. Wheels within wheels: the plant circadian system. Trends Plant Sci. 19:240–49 [Google Scholar]
  69. Huang W, Perez-Garcia P, Pokhilko A, Millar AJ, Antoshechkin I. 69.  et al. 2012. Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 336:75–79 [Google Scholar]
  70. Ibáñez C, Kozarewa I, Johansson M, Ögren E, Rohde A, Eriksson ME. 70.  2010. Circadian clock components regulate entry and affect exit of seasonal dormancy as well as winter hardiness in Populus trees. Plant Physiol. 153:1823–33 [Google Scholar]
  71. Imaizumi T, Tran HG, Swartz TE, Briggs WR, Kay SA. 71.  2003. FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426:302–6 [Google Scholar]
  72. Izawa T, Mihara M, Suzuki Y, Gupta M, Itoh H. 72.  et al. 2011. Os-GIGANTEA confers robust diurnal rhythms on the global transcriptome of rice in the field. Plant Cell 23:1741–55 [Google Scholar]
  73. Johnson CH, Egli M. 73.  2014. Metabolic compensation and circadian resilience in prokaryotic cyanobacteria. Annu. Rev. Biochem. 83:221–47 [Google Scholar]
  74. Johnson CH, Elliott JA, Foster R. 74.  2003. Entrainment of circadian programs. Chronobiol. Int. 20:741–74 [Google Scholar]
  75. Johnson CH, Kyriacou CP. 75.  2005. Clock evolution and adaptation: whence and whither?. Annu. Plant Rev. 21:237–60 [Google Scholar]
  76. Jouffe C, Cretenet G, Symul L, Martin E, Atger F. 76.  et al. 2013. The circadian clock coordinates ribosome biogenesis. PLOS Biol. 11:e1001455 [Google Scholar]
  77. Kerwin RE, Jimenez-Gomez JM, Fulop D, Harmer SL, Maloof JN, Kliebenstein DJ. 77.  2011. Network quantitative trait loci mapping of circadian clock outputs identifies metabolic pathway-to-clock linkages in Arabidopsis. Plant Cell 23:471–85 [Google Scholar]
  78. Kim SG, Yon F, Gaquerel E, Gulati J, Baldwin IT. 78.  2011. Tissue specific diurnal rhythms of metabolites and their regulation during herbivore attack in a native tobacco, Nicotiana attenuata. PLOS ONE 6:e26214 [Google Scholar]
  79. Kim WY, Fujiwara S, Suh SS, Kim J, Kim Y. 79.  et al. 2007. ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449:356–60 [Google Scholar]
  80. Kusakina J, Dodd AN. 80.  2012. Phosphorylation in the plant circadian system. Trends Plant Sci. 17:575–83 [Google Scholar]
  81. Kusakina J, Gould PD, Hall A. 81.  2014. A fast circadian clock at high temperatures is a conserved feature across Arabidopsis accessions and likely to be important for vegetative yield. Plant Cell Environ. 37:327–40 [Google Scholar]
  82. Lau OS, Huang X, Charron JB, Lee JH, Li G, Deng XW. 82.  2011. Interaction of Arabidopsis DET1 with CCA1 and LHY in mediating transcriptional repression in the plant circadian clock. Mol. Cell 43:703–12 [Google Scholar]
  83. Li P, Filiault D, Box MS, Kerdaffrec E, van Oosterhout C. 83.  et al. 2014. Multiple FLC haplotypes defined by independent cis-regulatory variation underpin life history diversity in Arabidopsis thaliana. Genes Dev. 28:1635–40 [Google Scholar]
  84. Locke JC, Kozma-Bognar L, Gould PD, Feher B, Kevei E. 84.  et al. 2006. Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Mol. Syst. Biol. 2:59 [Google Scholar]
  85. Lu W, Meng QJ, Tyler NJ, Stokkan KA, Loudon AS. 85.  2010. A circadian clock is not required in an arctic mammal. Curr. Biol. 20:533–37 [Google Scholar]
  86. Ma XF, Hall D, Onge KR, Jansson S, Ingvarsson PK. 86.  2010. Genetic differentiation, clinal variation and phenotypic associations with growth cessation across the Populus tremula photoperiodic pathway. Genetics 186:1033–44 [Google Scholar]
  87. Matsuzaki J, Kawahara Y, Izawa T. 87.  2015. Punctual transcriptional regulation by the rice circadian clock under fluctuating field conditions. Plant Cell 27:633–48 [Google Scholar]
  88. McClung CR. 88.  2013. Beyond Arabidopsis: the circadian clock in non-model plant species. Semin. Cell Dev. Biol. 24:430–36 [Google Scholar]
  89. Michael TP, Mockler TC, Breton G, McEntee C, Byer A. 89.  et al. 2008. Network discovery pipeline elucidates conserved time-of-day-specific cis-regulatory modules. PLOS Genet 4:e14 [Google Scholar]
  90. Michael TP, Salomé PA, Yu HJ, Spencer TR, Sharp EL. 90.  et al. 2003. Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302:1049–53 [Google Scholar]
  91. Millar AJ. 91.  1999. Tansley review no. 103: biological clocks in Arabidopsis thaliana. New Phytol. 141:175–97 [Google Scholar]
  92. Mizuno N, Nitta M, Sato K, Nasuda S. 92.  2012. A wheat homologue of PHYTOCLOCK 1 is a candidate gene conferring the early heading phenotype to einkorn wheat. Genes Genet. Syst. 87:357–67 [Google Scholar]
  93. Mock T, Daines SJ, Geider R, Collins S, Metodiev M. 93.  et al. 2016. Bridging the gap between omics and Earth system science to better understand how environmental change impacts marine microbes. Glob. Change Biol. 2261–75
  94. Mockler TC, Michael TP, Priest HD, Shen R, Sullivan CM. 94.  et al. 2007. The Diurnal project: diurnal and circadian expression profiling, model-based pattern matching and promoter analysis. Cold Spring Harb. Symp. Quant. Biol. 72:353–63 [Google Scholar]
  95. Moore A, Zielinski T, Millar AJ. 95.  2014. Online period estimation and determination of rhythmicity in circadian data, using the BioDare data infrastructure. Methods Mol. Biol. 1158:13–44 [Google Scholar]
  96. Morant PE, Thommen Q, Pfeuty B, Vandermoere C, Corellou F. 96.  et al. 2010. A robust two-gene oscillator at the core of Ostreococcus tauri circadian clock. Chaos 20:045108 [Google Scholar]
  97. Moulager M, Monnier A, Jesson B, Bouvet R, Mosser J. 97.  et al. 2007. Light-dependent regulation of cell division in Ostreococcus: evidence for a major transcriptional input. Plant Physiol. 144:1360–69 [Google Scholar]
  98. Murphy RL, Klein RR, Morishige DT, Brady JA, Rooney WL. 98.  et al. 2011. Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum. PNAS 108:16469–74 [Google Scholar]
  99. Nagano AJ, Sato Y, Mihara M, Antonio BA, Motoyama R. 99.  et al. 2012. Deciphering and prediction of transcriptome dynamics under fluctuating field conditions. Cell 151:1358–69 [Google Scholar]
  100. Nakamichi N. 100.  2011. Molecular mechanisms underlying the Arabidopsis circadian clock. Plant Cell Physiol. 52:1709–18 [Google Scholar]
  101. Nakamichi N, Kiba T, Henriques R, Mizuno T, Chua NH, Sakakibara H. 101.  2010. PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell 22:594–605 [Google Scholar]
  102. Nikaido SS, Johnson CH. 102.  2000. Daily and circadian variation in survival from ultraviolet radiation in Chlamydomonas reinhardtii. Photochem. Photobiol. 71:758–65 [Google Scholar]
  103. Nolte C, Staiger D. 103.  2015. RNA around the clock—regulation at the RNA level in biological timing. Front. Plant Sci. 6:311 [Google Scholar]
  104. Noordally ZB, Millar AJ. 104.  2015. Clocks in algae. Biochemistry 54:171–83 [Google Scholar]
  105. Ocone A, Millar AJ, Sanguinetti G. 105.  2013. Hybrid regulatory models: a statistically tractable approach to model regulatory network dynamics. Bioinformatics 29:910–16 [Google Scholar]
  106. O'Neill JS, Reddy AB. 106.  2011. Circadian clocks in human red blood cells. Nature 469:498–503 [Google Scholar]
  107. O'Neill JS, van Ooijen G, Dixon LE, Troein C, Corellou F. 107.  et al. 2011. Circadian rhythms persist without transcription in a eukaryote. Nature 469:554–58 [Google Scholar]
  108. O'Neill JS, van Ooijen G, Le Bihan T, Millar AJ. 108.  2011. Circadian clock parameter measurement: characterization of clock transcription factors using surface plasmon resonance. J. Biol. Rhythms 26:91–98 [Google Scholar]
  109. Panchy N, Wu G, Newton L, Tsai CH, Chen J. 109.  et al. 2014. Prevalence, evolution, and cis-regulation of diel transcription in Chlamydomonas reinhardtii. G3 4:2461–71 [Google Scholar]
  110. Para A, Li Y, Marshall-Colon A, Varala K, Francoeur NJ. 110.  et al. 2014. Hit-and-run transcriptional control by bZIP1 mediates rapid nutrient signaling in Arabidopsis. PNAS 111:10371–76 [Google Scholar]
  111. Penfield S, Hall A. 111.  2009. A role for multiple circadian clock genes in the response to signals that break seed dormancy in Arabidopsis. Plant Cell 21:1722–32 [Google Scholar]
  112. Perez-Garcia P, Ma Y, Yanovsky MJ, Mas P. 112.  2015. Time-dependent sequestration of RVE8 by LNK proteins shapes the diurnal oscillation of anthocyanin biosynthesis. PNAS 112:5249–53 [Google Scholar]
  113. Pittendrigh CS. 113.  1993. Temporal organization: reflections of a Darwinian clock-watcher. Annu. Rev. Physiol. 55:16–54 [Google Scholar]
  114. Pittendrigh CS, Daan S. 114.  1976. A functional analysis of circadian pacemakers in nocturnal rodents. V. A clock for all seasons. J. Comp. Physiol. A 106:333–55 [Google Scholar]
  115. Pokhilko A, Fernandez AP, Edwards KD, Southern MM, Halliday KJ, Millar AJ. 115.  2012. The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Mol. Syst. Biol. 8:574 [Google Scholar]
  116. Pokhilko A, Hodge SK, Stratford K, Knox K, Edwards KD. 116.  et al. 2010. Data assimilation constrains new connections and components in a complex, eukaryotic circadian clock model. Mol. Syst. Biol. 6:416 [Google Scholar]
  117. Pokhilko A, Ramos JA, Holtan H, Maszle DR, Khanna R, Millar AJ. 117.  2011. Ubiquitin ligase switch in plant photomorphogenesis: a hypothesis. J. Theor. Biol. 270:31–41 [Google Scholar]
  118. Purcell O, Savery NJ, Grierson CS, di Bernardo M. 118.  2010. A comparative analysis of synthetic genetic oscillators. J. R. Soc. Interface 7:1503–24 [Google Scholar]
  119. Qiu Y, Li M, Pasoreck EK, Long L, Shi Y. 119.  et al. 2015. HEMERA couples the proteolysis and transcriptional activity of PHYTOCHROME INTERACTING FACTORs in Arabidopsis photomorphogenesis. Plant Cell 27:1409–27 [Google Scholar]
  120. Rawat R, Takahashi N, Hsu PY, Jones MA, Schwartz J. 120.  et al. 2011. REVEILLE8 and PSEUDO-REPONSE REGULATOR5 form a negative feedback loop within the Arabidopsis circadian clock. PLOS Genet. 7:e1001350 [Google Scholar]
  121. Roenneberg T, Merrow M. 121.  1999. Circadian systems and metabolism. J. Biol. Rhythms 14:449–59 [Google Scholar]
  122. Salathia N, Lynn JR, Millar AJ, King GJ. 122.  2007. Detection and resolution of genetic loci affecting circadian period in Brassica oleracea. Theor. Appl. Genet. 114:683–92 [Google Scholar]
  123. Salomé PA, McClung CR. 123.  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 [Google Scholar]
  124. Salomé PA, Michael TP, Kearns EV, Fett-Neto AG, Sharrock RA, McClung CR. 124.  2002. The out of phase 1 mutant defines a role for PHYB in circadian phase control in Arabidopsis. Plant Physiol. 129:1674–85 [Google Scholar]
  125. Salomé PA, Weigel D, McClung CR. 125.  2010. The role of the Arabidopsis morning loop components CCA1, LHY, PRR7, and PRR9 in temperature compensation. Plant Cell 22:3650–61 [Google Scholar]
  126. Scialdone A, Howard M. 126.  2015. How plants manage food reserves at night: quantitative models and open questions. Front. Plant Sci. 6:204 [Google Scholar]
  127. Seaton DD, Smith RW, Song YH, MacGregor DR, Stewart K. 127.  et al. 2015. Linked circadian outputs control elongation growth and flowering in response to photoperiod and temperature. Mol. Syst. Biol. 11:776 [Google Scholar]
  128. Seo PJ, Mas P. 128.  2014. Multiple layers of posttranslational regulation refine circadian clock activity in Arabidopsis. Plant Cell 26:79–87 [Google Scholar]
  129. Shi H, Wang X, Mo X, Tang C, Zhong S, Deng XW. 129.  2015. Arabidopsis DET1 degrades HFR1 but stabilizes PIF1 to precisely regulate seed germination. PNAS 112:3817–22 [Google Scholar]
  130. Sidaway-Lee K, Costa MJ, Rand DA, Finkenstadt B, Penfield S. 130.  2014. Direct measurement of transcription rates reveals multiple mechanisms for configuration of the Arabidopsis ambient temperature response. Genome Biol. 15:R45 [Google Scholar]
  131. Silverman SJ, Petti AA, Slavov N, Parsons L, Briehof R. 131.  et al. 2010. Metabolic cycling in single yeast cells from unsynchronized steady-state populations limited on glucose or phosphate. PNAS 107:6946–51 [Google Scholar]
  132. Sjodin A, Wissel K, Bylesjo M, Trygg J, Jansson S. 132.  2008. Global expression profiling in leaves of free-growing aspen. BMC Plant Biol. 8:61 [Google Scholar]
  133. Song YH, Shim JS, Kinmonth-Schultz HA, Imaizumi T. 133.  2015. Photoperiodic flowering: time measurement mechanisms in leaves. Annu. Rev. Plant Biol. 66:441–64 [Google Scholar]
  134. Sullivan AM, Arsovski AA, Lempe J, Bubb KL, Weirauch MT. 134.  et al. 2014. Mapping and dynamics of regulatory DNA and transcription factor networks in A. thaliana. Cell Rep. 8:2015–30 [Google Scholar]
  135. Tepperman JM, Hudson ME, Khanna R, Zhu T, Chang SH. 135.  et al. 2004. Expression profiling of phyB mutant demonstrates substantial contribution of other phytochromes to red-light-regulated gene expression during seedling de-etiolation. Plant J. 38:725–39 [Google Scholar]
  136. Toledo-Ortiz G, Johansson H, Lee KP, Bou-Torrent J, Stewart K. 136.  et al. 2014. The HY5-PIF regulatory module coordinates light and temperature control of photosynthetic gene transcription. PLOS Genet. 10:e1004416 [Google Scholar]
  137. Troein C, Corellou F, Dixon LE, van Ooijen G, O'Neill JS. 137.  et al. 2011. Multiple light inputs to a simple clock circuit allow complex biological rhythms. Plant J. 66:375–85 [Google Scholar]
  138. Troein C, Locke JC, Turner MS, Millar AJ. 138.  2009. Weather and seasons together demand complex biological clocks. Curr. Biol. 19:1961–64 [Google Scholar]
  139. Turner AS, Faure S, Zhang Y, Laurie DA. 139.  2013. The effect of day-neutral mutations in barley and wheat on the interaction between photoperiod and vernalization. Theor. Appl. Genet. 126:2267–77 [Google Scholar]
  140. Tyson JJ, Novak B. 140.  2010. Functional motifs in biochemical reaction networks. Annu. Rev. Phys. Chem. 61:219–40 [Google Scholar]
  141. van Ooijen G, Dixon LE, Troein C, Millar AJ. 141.  2011. Proteasome function is required for biological timing throughout the twenty-four hour cycle. Curr. Biol 21:869–75 [Google Scholar]
  142. van Ooijen G, Millar AJ. 142.  2012. Non-transcriptional oscillators in circadian timekeeping. Trends Biochem. Sci. 37:484–92 [Google Scholar]
  143. Voss U, Wilson MH, Kenobi K, Gould PD, Robertson FC. 143.  et al. 2015. The circadian clock rephases during lateral root organ initiation in Arabidopsis thaliana. Nat. Commun. 6:7641 [Google Scholar]
  144. Wang CQ, Sarmast MK, Jiang J, Dehesh K. 144.  2015. The transcriptional regulator BBX19 promotes hypocotyl growth by facilitating COP1-mediated EARLY FLOWERING3 degradation in Arabidopsis. Plant Cell 27:1128–39 [Google Scholar]
  145. Wang L, Kim J, Somers DE. 145.  2013. Transcriptional corepressor TOPLESS complexes with pseudoresponse regulator proteins and histone deacetylases to regulate circadian transcription. PNAS 110:761–66 [Google Scholar]
  146. Weiner J. 146.  1999. Time, Love, Memory: A Great Biologist and His Quest for the Origins of Behavior New York: Knopf
  147. Weirauch MT, Yang A, Albu M, Cote AG, Montenegro-Montero A. 147.  et al. 2014. Determination and inference of eukaryotic transcription factor sequence specificity. Cell 158:1431–43 [Google Scholar]
  148. Weller JL, Liew LC, Hecht VF, Rajandran V, Laurie RE. 148.  et al. 2012. A conserved molecular basis for photoperiod adaptation in two temperate legumes. PNAS 109:21158–63 [Google Scholar]
  149. Woelfle MA, Ouyang Y, Phanvijhitsiri K, Johnson CH. 149.  2004. The adaptive value of circadian clocks: an experimental assessment in cyanobacteria. Curr. Biol. 14:1481–86 [Google Scholar]
  150. Woolum JC. 150.  1991. A reexamination of the role of the nucleus in generating the circadian-rhythm in Acetabularia. J. Biol. Rhythms 6:129–36 [Google Scholar]
  151. Xie Q, Lou P, Hermand V, Aman R, Park HJ. 151.  et al. 2015. Allelic polymorphism of GIGANTEA is responsible for naturally occurring variation in circadian period in Brassica rapa. PNAS 112:3829–34 [Google Scholar]
  152. Yerushalmi S, Yakir E, Green RM. 152.  2011. Circadian clocks and adaptation in Arabidopsis. Mol. Ecol. 20:1155–65 [Google Scholar]
  153. Yon F, Seo PJ, Ryu JY, Park CM, Baldwin IT, Kim SG. 153.  2012. Identification and characterization of circadian clock genes in a native tobacco, Nicotiana attenuata. BMC Plant Biol. 12:172 [Google Scholar]
  154. Yoshida R, Fekih R, Fujiwara S, Oda A, Miyata K. 154.  et al. 2009. Possible role of EARLY FLOWERING 3 (ELF3) in clock-dependent floral regulation by SHORT VEGETATIVE PHASE (SVP) in Arabidopsis thaliana. New Phytol. 182:838–50 [Google Scholar]
  155. Young MW, Kay SA. 155.  2001. Time zones: a comparative genetics of circadian clocks. Nat. Rev. Genet. 2:702–15 [Google Scholar]
  156. Zakhrabekova S, Gough SP, Braumann I, Muller AH, Lundqvist J. 156.  et al. 2012. Induced mutations in circadian clock regulator Mat-a facilitated short-season adaptation and range extension in cultivated barley. PNAS 109:4326–31 [Google Scholar]
  157. Zhang EE, Liu AC, Hirota T, Miraglia LJ, Welch G. 157.  et al. 2009. A genome-wide RNAi screen for modifiers of the circadian clock in human cells. Cell 139:199–210 [Google Scholar]
  158. Zhou M, Wang W, Karapetyan S, Mwimba M, Marques J. 158.  et al. 2015. Redox rhythm reinforces the circadian clock to gate immune response. Nature 523:472–76 [Google Scholar]
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The Intracellular Dynamics of Circadian Clocks Reach for the Light of Ecology and Evolution
Annual Review of Plant Biology 67, 595 (2016); https://doi.org/10.1146/annurev-arplant-043014-115619
/content/journals/10.1146/annurev-arplant-043014-115619
/content/journals/10.1146/annurev-arplant-043014-115619
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