Have a personal or library account? Click to login
Heat the Clock: Entrainment and Compensation in Arabidopsis Circadian Rhythms Cover

Heat the Clock: Entrainment and Compensation in Arabidopsis Circadian Rhythms

Open Access
|May 2019

References

  1. 1Dodd, AN, Belbin, FE, Frank, A and Webb, AAR. Interactions between circadian clocks and photosynthesis for the temporal and spatial coordination of metabolism. Frontiers in Plant Science. 2015; 6: 245. DOI: 10.3389/fpls.2015.00245
  2. 2Grundy, J, Stoker, C and Carré, IA. Circadian regulation of abiotic stress tolerance in plants. Frontiers in Plant Science. 2015; 6: 115. DOI: 10.3389/fpls.2015.00648
  3. 3Yazdanbakhsh, N, Sulpice, R, Graf, A, Stitt, M and Fisahn, J. Circadian control of root elongation and C partitioning in Arabidopsis thaliana. Plant, Cell and Environment. 2011; 34: 877894. DOI: 10.1111/j.1365-3040.2011.02286.x
  4. 4Dodd, AN. Plant Circadian Clocks Increase Photosynthesis, Growth, Survival, and Competitive Advantage. Science. 2005; 309: 630633. DOI: 10.1126/science.1115581
  5. 5Green, RM, Tingay, S, Wang, ZY and Tobin, EM. Circadian rhythms confer a higher level of fitness to Arabidopsis plants. Plant physiology. 2002; 129: 576584. DOI: 10.1104/pp.004374
  6. 6Davis, SJ and Millar, AJ. Watching the hands of the Arabidopsis biological clock. Genome biology. 2001; 2: 1008.11008.4. DOI: 10.1186/gb-2001-2-3-reviews1008
  7. 7Turek, FW, Joshu, C, Kohsaka, A, Lin, E, Ivanova, G, Mcdearmon, E, et al. Obesity and Metabolic Syndrome in Circadian Clock Mutant Mice. Science. 2005; 308: 10431045. DOI: 10.1126/science.1108750
  8. 8Bell-Pedersen, D, Shinohara, ML, Loros, JJ and Dunlap, JC. Circadian clock controlled genes isolated from Neurospora crassa are late night to early morning-specific. Proceedings of the National Academy of Sciences. 1996; 93: 1309613101. DOI: 10.1073/pnas.93.23.13096
  9. 9Guo, F, Yu, J, Jung, HJ, Abruzzi, KC, Luo, W, Griffith, LC, et al. Circadian neuron feedback controls the Drosophila sleep-activity profile. Nature. 2016; 536: 292297. DOI: 10.1038/nature19097
  10. 10Welkie, DG, Rubin, BE, Chang, YG, Diamond, S, Rifkin, SA, LiWang, A, et al. Genome-wide fitness assessment during diurnal growth reveals an expanded role of the cyanobacterial circadian clock protein KaiA. Proceedings of the National Academy of Sciences. 2018; 115: E7174E7183. DOI: 10.1073/pnas.1802940115
  11. 11De Caluwé, J, Xiao, Q, Hermans, C, Verbruggen, N, Leloup, JC and Gonze, D. A Compact Model for the Complex Plant Circadian Clock. Frontiers in Plant Science. 2016; 7: 115. DOI: 10.3389/fpls.2016.00074
  12. 12Fogelmark, K and Troein, C. Rethinking Transcriptional Activation in the Arabidopsis Circadian Clock. PLoS Computational Biology. 2014; 10: e1003705. DOI: 10.1371/journal.pcbi.1003705
  13. 13Pokhilko, A, Mas, P and Millar, AJ. Modelling the widespread effects of TOC1 signalling on the plant circadian clock and its outputs. BMC Systems Biology. 2013; 7: 23. DOI: 10.1186/1752-0509-7-23
  14. 14Rust, MJ, Markson, JS, Lane, WS, Fisher, DS and O’Shea, EK. Ordered phospho rylation governs oscillation of a three-protein circadian clock. Science (New York, NY). 2007; 318: 80912. DOI: 10.1126/science.1148596
  15. 15Kurosawa, G, Aihara, K and Iwasa, Y. A Model for the Circadian Rhythm of Cyanobacteria that Maintains Oscillation without Gene Expression. Biophysical Journal. 2006; 91: 20152023. DOI: 10.1529/biophysj.105.076554
  16. 16Lerner, I, Bartok, O, Wolfson, V, Menet, JS, Weissbein, U, Afik, S, et al. Clk post-transcriptional control denoises circadian transcription both temporally and spatially. Nature Communications. 2015; 6: 7056. DOI: 10.1038/ncomms8056
  17. 17Fathallah-Shaykh, HM, Bona, JL and Kadener, S. Mathematical model of the Drosophila circadian clock: loop regulation and transcriptional integration. Biophysical journal. 2009; 97: 2399408. DOI: 10.1016/j.bpj.2009.08.018
  18. 18Bellman, J, Kim, JK, Lim, S and Hong, CI. Modeling Reveals a Key Mechanism for Light-Dependent Phase Shifts of Neurospora Circadian Rhythms. Biophysical Journal. 2018; 115: 10931102. DOI: 10.1016/j.bpj.2018.07.029
  19. 19Crosthwaite, SK, Loros, JJ and Dunlap, JC. Light-Induced Resetting of a Circadian Clock Is Mediated by a Rapid Increase in frequency Transcript. Cell. 1995; 81: 10031012. DOI: 10.1016/S0092-8674(05)80005-4
  20. 20Reló Gio, A, Westermark, PO, Wallach, T, Schellenberg, K and Kramer, A. Tuning the Mammalian Circadian Clock: Robust Synergy of Two Loops. PLoS Comput Biol. 2011; 7: e1002309. DOI: 10.1371/journal.pcbi.1002309
  21. 21Geier, F, Becker-Weimann, S, Kramer, A and Herzel, H. Entrainment in a Model of the Mammalian Circadian Oscillator. J Biol Rhythms. 2005; 20: 8393. DOI: 10.1177/0748730404269309
  22. 22Podkolodnaya, OA, Tverdokhleb, NN and Podkolodnyy, NL. Computational modeling of the cell-autonomous mammalian circadian oscillator. BMC Systems Biology. 2017; 11: 2742. DOI: 10.1186/s12918-016-0379-8
  23. 23Hevia, MA, Canessa, P and Larrondo, LF. Circadian clocks and the regulation of virulence in fungi: Getting up to speed. Seminars in Cell & Developmental Biology. 2016; 57: 147155. DOI: 10.1016/j.semcdb.2016.03.021
  24. 24Bujdoso, N and Davis, SJ. Mathematical modeling of an oscillating gene circuit to unravel the circadian clock network of Arabidopsis thaliana. Frontiers in Plant Science. 2013; 4: 18. DOI: 10.3389/fpls.2013.00003
  25. 25Hogenesch, JB and Ueda, HR. Understanding systems-level properties: Timely stories from the study of clocks. Nature Reviews Genetics. 2011; 12: 407416. DOI: 10.1038/nrg2972
  26. 26Bell-Pedersen, D, Cassone, VM, Earnest, DJ, Golden, SS, Hardin, PE, Thomas, TL, et al. Circadian rhythms from multiple oscillators: Lessons from diverse organisms. Nature Reviews Genetics. 2005; 6: 544556. DOI: 10.1038/nrg1633
  27. 27Pokhilko, A, Fernández, AP, Edwards, KD, Southern, MM, Halliday, KJ and Millar, AJ. The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Molecular Systems Biology. 2012; 8: 574. DOI: 10.1038/msb.2012.6
  28. 28Pokhilko, A, Hodge, SK, Stratford, K, Knox, K, Edwards, KD, Thomson, AW, et al. Data assimilation constrains new connections and components in a complex, eukaryotic circadian clock model. Molecular Systems Biology. 2010; 6: 416. DOI: 10.1038/msb.2010.69
  29. 29Herrero, E, Kolmos, E, Bujdoso, N, Yuan, Y, Wang, M, Berns, MC, et al. EARLY FLOWERING4 recruitment of EARLY FLOWERING3 in the nucleus sustains the Arabidopsis circadian clock. The Plant cell. 2012; 24: 42843. DOI: 10.1105/tpc.111.093807
  30. 30Kolmos, E, Nowak, M, Werner, M, Fischer, K, Schwarz, G, Mathews, S, et al. Integrating ELF4 into the circadian system through combined structural and functional studies. HFSP journal. 2009; 3: 35066. DOI: 10.2976/1.3218766
  31. 31Zeilinger, MN, Farré, EM, Taylor, SR, Kay, SA and Doyle, FJ. A novel computational model of the circadian clock in Arabidopsis that incorporates PRR7 and PRR9. Molecular Systems Biology. 2006; 2: 58. DOI: 10.1038/msb4100101
  32. 32Locke, JCW, Kozma-Bognár, L, Gould, PD, Fehér, B, Kevei, É, Nagy, F, et al. Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Molecular Systems Biology. 2006; 2: 59. DOI: 10.1038/msb4100102
  33. 33Locke, JCW, Southern, MM, Kozma-Bognár, L, Hibberd, V, Brown, PE, Turner, MS, et al. Extension of a genetic network model by iterative experimentation and mathematical analysis. Molecular Systems Biology. 2005; 1: 0013. DOI: 10.1038/msb4100018
  34. 34Locke, JCW, Millar, AJ and Turner, MS. Modelling genetic networks with noisy and varied experimental data: the circadian clock in Arabidopsis thaliana. Journal of Theoretical Biology. 2005; 234: 383393. DOI: 10.1016/j.jtbi.2004.11.038
  35. 35Shin, J and Davis, SJ. Recent advances in computational modeling as a conduit to understand the plant circadian clock. F1000 biology reports. 2010; 2: 58. DOI: 10.3410/B2-49
  36. 36Harmer, SL. The Circadian System in Higher Plants. Annual Review of Plant Biology. 2009; 60: 357377. DOI: 10.1146/annurev.arplant.043008.092054
  37. 37Johnson, CH, Elliott, JA and Foster, R. Entrainment of circadian programs. Chronobiology International. 2003; 20: 741774. DOI: 10.1081/CBI-120024211
  38. 38Millar, AJ. The Intracellular Dynamics of Circadian Clocks Reach for the Light of Ecology and Evolution. Annual Review of Plant Biology. 2016; 67: 595618. DOI: 10.1146/annurev-arplant-043014-115619
  39. 39Hsu, PY and Harmer, SL. Wheels within wheels: The plant circadian system. Trends in Plant Science. 2014; 19: 240249. DOI: 10.1016/j.tplants.2013.11.007
  40. 40Gould, PD, Locke, JCW, Larue, C, Southern, MM, Davis, SJ, Hanano, S, et al. The molecular basis of temperature compensation in the Arabidopsis circadian clock. Plant Cell. 2006; 18: 11771187. DOI: 10.1105/tpc.105.039990
  41. 41Edwards, K, Anderson, P, Hall, A, Salathia, N, Locke, J, Lynn, J, et al. FLOWERING LOCUS C Mediates Natural Variation in the High-Temperature Response of the Arabidopsis Circadian Clock. The Plant cell. 2006; 18: 639650. DOI: 10.1105/tpc.105.038315
  42. 42Jones, MA, Morohashi, K, Grotewold, E and Harmer, SL. Arabidopsis JMJD5/JMJ30 Acts Independently of LUX ARRHYTHMO Within the Plant Circadian Clock to Enable Temperature Compensation. Frontiers in Plant Science. 2019; 10: 57. DOI: 10.3389/fpls.2019.00057
  43. 43Gould, PD, Ugarte, N, Domijan, M, Costa, M, Foreman, J, MacGregor, D, et al. Network balance via CRY signalling controls the Arabidopsis circadian clock over ambient temperatures. Molecular Systems Biology. 2013; 9: 650. DOI: 10.1038/msb.2013.7
  44. 44Wigge, PA. Ambient temperature signalling in plants. 2013; 16: 661666. DOI: 10.1016/j.pbi.2013.08.004
  45. 45Akman, OE, Locke, JCW, Tang, S, Carré, I, Millar, AJ and Rand, DA. Isoform switching facilitates period control in the Neurospora crassa circadian clock. Molecular Systems Biology. 2008; 4: 164. DOI: 10.1038/msb.2008.28
  46. 46Ruoff, P, Zakhartsev, M and Westerhoff, HV. Temperature compensation through systems biology. FEBS Journal. 2007; 274: 940950. DOI: 10.1111/j.1742-4658.2007.05641.x
  47. 47Ruoff, P and Rensing, L. The temperature-compensated goodwin model simulates many circadian clock properties. Journal of Theoretical Biology. 1996; 179: 275285. DOI: 10.1006/jtbi.1996.0067
  48. 48Ruoff, P. Introducing temperature-compensation in any reaction kinetic oscillator model. Journal of Interdisiplinary Cycle Research. 1992; 23: 9299. DOI: 10.1080/09291019209360133
  49. 49Leloup, JC and Goldbeter, A. Temperature Compensation of Circadian Rhythms: Control of the Period in a Model for Circadian Oscillations of the Per Protein in Drosophila. Chronobiology International. 1997; 14: 511520. DOI: 10.3109/07420529709001472
  50. 50Nagao, R, Epstein, IR, Gonzalez, ER and Varela, H. Temperature (over)compensation in an oscillatory surface reaction. Journal of Physical Chemistry A. 2008; 112: 46174624. DOI: 10.1021/jp801361j
  51. 51Kolmos, E, Herrero, E, Bujdoso, N, Millar, AJ, Tóth, R, Gyula, P, et al. A Reduced-Function Allele Reveals That EARLY FLOWERING3 Repressive Action on the Circadian Clock Is Modulated by Phytochrome Signals in Arabidopsis. The Plant Cell. 2011; 23: 32303246. DOI: 10.1105/tpc.111.088195
  52. 52Ruoff, P, Vinsjevik, M and Rensing, L. Temperature compensation in biological oscillators: a challenge for joint experimental and theoretical analysis. Comments Theor Biol. 2000; 5: 361382.
  53. 53Salomé, PA, Weigel, D and McClung, CR. The role of the Arabidopsis morning loop components CCA1, LHY, PRR7, and PRR9 in temperature compensation. The Plant cell. 2010; 22: 365061. DOI: 10.1105/tpc.110.079087
  54. 54Sidaway-Lee, K, Costa, MJ, Rand, DA, Finkenstadt, B and Penfield, S. Direct measurement of transcription rates reveals multiple mechanisms for configuration of the Arabidopsis ambient temperature response. Genome Biology. 2014; 15: R45. DOI: 10.1186/gb-2014-15-3-r45
  55. 55Blair, EJ, Bonnot, T, Hummel, M, Hay, E, Marzolino, JM and Quijada, IA, et al. Contribution of time of day and the circadian clock to the heat stress responsive transcriptome in Arabidopsis. Scientific Reports. 2019; 9: 4814. DOI: 10.1038/s41598-019-41234-w
  56. 56Ripel, L, Wendell, M, Rognli, OA, Torre, S, Lee, Y and Olsen, JE. Thermoperiodic Control of Floral Induction Involves Modulation of the Diurnal FLOWERING LOCUS T Expression Pattern. Plant and Cell Physiology. 2017; 58: 466477. DOI: 10.1093/pcp/pcw221
  57. 57Bours, R, van Zanten, M, Pierik, R, Bouwmeester, H and van der Krol, A. Antiphase Light and Temperature Cycles Affect PHYTOCHROME B-Controlled Ethylene Sensitivity and Biosynthesis, Limiting Leaf Movement and Growth of Arabidopsis. 2013; 163: 882895. DOI: 10.1104/pp.113.221648
  58. 58De Caluwé, J, de Melo, JRF, Tosenberger, A, Hermans, C, Verbruggen, N, Leloup, JC, et al. Modeling the photoperiodic entrainment of the plant circadian clock. Journal of Theoretical Biology. 2017; 420: 220231. DOI: 10.1016/j.jtbi.2017.03.005
  59. 59Davis, AM, Ronald, J, Ma, Z, Wilkinson, AJ, Philippou, K, Shindo, T, et al. HSP90 Contributes to Entrainment of the Arabidopsis Circadian Clock via the Morning Loop. Genetics. 2018; 210: 13831390. DOI: 10.1534/genetics.118.301586
  60. 60Somers, DE, Webb, AA, Pearson, M and Kay, SA. The short-period mutant, toc1-1, alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana. 1998; 125: 485494.
  61. 61Boikoglou, E, Ma, Z, von Korff, M, Davis, AM, Nagy, F and Davis, SJ. Environmental Memory from a Circadian Oscillator: The Arabidopsis thaliana Clock Differentially Integrates Perception of Photic vs. Thermal Entrainment. 2011; 189: 655664. DOI: 10.1534/genetics.111.131417
  62. 62Salomé, PA and McClung, CR. PSEUDO-RESPONSE REGULATOR 7 and 9 are partially redundant genes essential for the temperature responsiveness of the Arabidopsis circadian clock. Plant Cell. 2005; 17: 791803. DOI: 10.1105/tpc.104.029504
DOI: https://doi.org/10.5334/jcr.179 | Journal eISSN: 1740-3391
Language: English
Submitted on: Feb 18, 2019
Accepted on: Apr 19, 2019
Published on: May 14, 2019
Published by: Ubiquity Press
In partnership with: Paradigm Publishing Services
Publication frequency: 1 issue per year

© 2019 Paula A. Avello, Seth J. Davis, James Ronald, Jonathan W. Pitchford, published by Ubiquity Press
This work is licensed under the Creative Commons Attribution 4.0 License.