The Library

Quantitative analysis of regulatory flexibility under changing environmental conditions

Tools

Edwards, Kieron D., Akman, Ozgur E., Knox, Kirsten, Lumsden, P. J., Thomson, Adrian W., Brown, Paul E., Pokhilko, Alexandra, Kozma-Bognar, Laszlo, Nagy, Ferenc, 1952-, Rand, D. A. (David A.) and Millar, A. J. (Andrew J.). (2010) Quantitative analysis of regulatory flexibility under changing environmental conditions. Molecular Systems Biology, Vol.6 (No.424). ISSN 1744-4292

PDF
WRAP_RAND_Quantitative_Analysis.pdf - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader
Download (491Kb)

Official URL: http://dx.doi.org/10.1038/msb.2010.81

Abstract

The circadian clock controls 24-h rhythms in many biological processes, allowing appropriate timing of biological rhythms relative to dawn and dusk. Known clock circuits include multiple, interlocked feedback loops. Theory suggested that multiple loops contribute the flexibility for molecular rhythms to track multiple phases of the external cycle. Clear dawn- and dusk-tracking rhythms illustrate the flexibility of timing in Ipomoea nil. Molecular clock components in Arabidopsis thaliana showed complex, photoperiod-dependent regulation, which was analysed by comparison with three contrasting models. A simple, quantitative measure, Dusk Sensitivity, was introduced to compare the behaviour of clock models with varying loop complexity. Evening-expressed clock genes showed photoperiod-dependent dusk sensitivity, as predicted by the three-loop model, whereas the one- and two-loop models tracked dawn and dusk, respectively. Output genes for starch degradation achieved dusk-tracking expression through light regulation, rather than a dusk-tracking rhythm. Model analysis predicted which biochemical processes could be manipulated to extend dusk tracking. Our results reveal how an operating principle of biological regulators applies specifically to the plant circadian clock.

Item Type:	Journal Article
Subjects:	Q Science > QK Botany
Divisions:	Faculty of Science > Centre for Systems Biology
Library of Congress Subject Headings (LCSH):	Circadian rhythms, Arabidopsis thaliana, Plant genetic regulation, Plant photoperiodism
Journal or Publication Title:	Molecular Systems Biology
Publisher:	Nature Publishing Group
ISSN:	1744-4292
Date:	2 November 2010
Volume:	Vol.6
Number:	No.424
Number of Pages:	11
Identification Number:	10.1038/msb.2010.81
Status:	Peer Reviewed
Access rights to Published version:	Open Access
Funder:	Engineering and Physical Sciences Research Council (EPSRC), Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), Sixth Framework Programme (European Commission) (FP6)
Grant number:	G19886 (BBSRC), E015263 (BBSRC), EUCLOCK (FP6), D019621 (EPSRC)
References:	Akman OE, Rand DA, Brown PE, Millar AJ (2010) Robustness from flexibility in the fungal circadian clock. BMC Syst Biol 4: 88 An H, Roussot C, Suarez-Lopez P, Corbesier L, Vincent C, Pineiro M, Hepworth S, Mouradov A, Justin S, Turnbull C, Coupland G (2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131: 3615–3626 Bell-Pedersen D, Cassone VM, Earnest DJ, Golden SS, Hardin PE, Thomas TL, Zoran MJ (2005) Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat Rev Genet 6: 544–556 Blasing OE, Gibon Y, Gunther M, Hohne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible WR, Stitt M (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17: 3257–3281 Bohlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312: 1040–1043 Chia T, Thorneycroft D, Chapple A, Messerli G, Chen J, Zeeman SC, Smith SM, Smith AM (2004) A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. Plant J 37: 853–863 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 Dodd AN, Gardner MJ, Hotta CT, Hubbard KE, Dalchau N, Love J, Assie JM, Robertson FC, Jakobsen MK, Goncalves J, Sanders D, Webb AA (2007) The Arabidopsis circadian clock incorporates a cADPR-based feedback loop. Science 318: 1789–1792 Dodd AN, Jakobsen MK, Baker AJ, Telzerow A, Hou SW, Laplaze L, Barrot L, Poethig RS, Haseloff J, Webb AA (2006) Time of day modulates low-temperature Ca signals in Arabidopsis. Plant J 48: 962–973 Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hibberd JM, Millar AJ, Webb AA (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309: 630–633 Doyle MR, Davis SJ, Bastow RM, McWatters HG, Kozma-Bognar L, Nagy F, Millar AJ, Amasino RM (2002) The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana. Nature 419: 74–77 Dunlap JC, Loros JJ, DeCoursey PJ (2004) Chronobiology: Biological Timekeeping. Sunderland, MA: Sinauer Associates Edwards KD, Anderson PE, Hall A, Salathia NS, Locke JC, Lynn JR, Straume M, Smith JQ, Millar AJ (2006) FLOWERING LOCUS C mediates natural variation in the high-temperature response of the Arabidopsis circadian clock. Plant Cell 18: 639–650 Edwards KD, Lynn JR, Gyula P, Nagy F, Millar AJ (2005) Natural allelic variation in the temperature-compensation mechanisms of the Arabidopsis thaliana circadian clock. Genetics 170: 387–400 Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Coupland G, Putterill J (1999) GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J 18: 4679–4688 Fowler SG, Cook D, Thomashow MF (2005) Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol 137: 961–968 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 Gould PD, Locke JC, Larue C, Southern MM, Davis SJ, Hanano S, Moyle R, Milich R, Putterill J, Millar AJ, Hall A (2006) The molecular basis of temperature compensation in the Arabidopsis circadian clock. Plant Cell 18: 1177–1187 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 USA 107: 9458–9463 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: 2110–2113 Hayama R, Agashe B, Luley E, King R, Coupland G (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 Hazen SP, Schultz TF, Pruneda-Paz JL, Borevitz JO, Ecker JR, Kay SA (2005) LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. Proc Natl Acad Sci USA 102: 10387–10392 Hazlerigg D, Loudon A (2008) New insights into ancient seasonal life timers. Curr Biol 18: R795–R804 Heide OM, King RW, Evans LT (1988) The semidian rhythm in flowering response of pharbitis-nil in relation to dark period time measurement and to a circadian-rhythm. Physiol Plant 73: 286–294 Imaizumi T, Kay SA (2006) Photoperiodic control of flowering: not only by coincidence. Trends Plant Sci 11: 550–558 Imaizumi T, Tran HG, Swartz TE, Briggs WR, Kay SA (2003) FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426: 302–306 Inagaki N, Honma S, Ono D, Tanahashi Y, Honma K (2007) Separate oscillating cell groups in mouse suprachiasmatic nucleus couple photoperiodically to the onset and end of daily activity. Proc Natl Acad Sci USA 104: 7664–7669 Ito S, Kawamura H, Niwa Y, Nakamichi N, Yamashino T, Mizuno T (2009) A genetic study of the Arabidopsis circadian clock with reference to the TIMING OF CAB EXPRESSION 1 (TOC1) gene. Plant Cell Physiol 50: 290–303 Jagota A, de la Iglesia HO, Schwartz WJ (2000) Morning and evening circadian oscillations in the suprachiasmatic nucleus in vitro. Nat Neurosci 3: 372–376 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 Khalsa SBS, Whitmore D, Block GD (1992) Stopping the circadian pacemaker with inhibitors of protein synthesis. Proc Natl Acad Sci USA 89: 10862–10866 Kitano H (2007) Towards a theory of biological robustness. Mol Syst Biol 3: 137 Kitayama Y, Nishiwaki T, Terauchi K, Kondo T (2008) Dual KaiC-based oscillations constitute the circadian system of cyanobacteria. Genes Dev 22: 1513–1521 Kolar C, Adam E, Schafer E, Nagy F (1995) Expression of tobacco genes for light-harvesting chlorophyll a/b binding proteins of photosystem II is controlled by two circadian oscillators in a developmentally regulated fashion. Proc Natl Acad Sci USA 92: 2174–2178 Locke JC, Kozma-Bognar L, Gould PD, Feher B, Kevei E, Nagy F, Turner MS, Hall A, Millar AJ (2006) Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Mol Syst Biol 2: 59 Locke JC, Millar AJ, Turner MS (2005a) Modelling genetic networks with noisy and varied experimental data: the circadian clock in Arabidopsis thaliana. J Theor Biol 234: 383–393 Locke JC, Southern MM, Kozma-Bognar L, Hibberd V, Brown PE, Turner MS, Millar AJ (2005b) Extension of a genetic network model by iterative experimentation and mathematical analysis. Mol Syst Biol 1: 13 Love J, Dodd AN, Webb AA (2004) Circadian and diurnal calcium oscillations encode photoperiodic information in Arabidopsis. Plant Cell 16: 956–966 Lumsden PJ, Youngs JA, Thomas B, Vince-Prue D (1995) Evidence that photoperiodic, dark time measurement in pharbitis-nil involves a circadian rather than a semidian rhythm. Plant Cell Environ 18: 1403–1410 Martin-Tryon EL, Kreps JA, Harmer SL (2007) GIGANTEA acts in blue light signaling and has biochemically separable roles in circadian clock and flowering time regulation. Plant Physiol 143: 473–486 McClung CR (2006) Plant circadian rhythms. Plant Cell 18: 792–803 McWatters HG, Bastow RM, Hall A, Millar AJ (2000) The ELF3 zeitnehmer regulates light signalling to the circadian clock. Nature 408: 716–720 McWatters HG, Kolmos E, Hall A, Doyle MR, Amasino RM, Gyula P, Nagy F, Millar AJ, Davis SJ (2007) ELF4 is required for oscillatory properties of the circadian clock. Plant Physiol 144: 391–401 Michael TP,Mockler TC, Breton G, McEntee C, Byer A, Trout JD, Hazen SP, Shen R, Priest HD, Sullivan CM, Givan SA, Yanovsky M, Hong F, Kay SA, Chory J (2008) Network discovery pipeline elucidates conserved time-of-day-specific cis-regulatory modules. PLoS Genet 4: e14 Millar AJ, Kay SA (1996) Integration of circadian and phototransduction pathways in the network controlling CAB gene transcription in Arabidopsis. Proc Natl Acad Sci USA 93: 15491–15496 Niittyla T, Comparot-Moss S, Lue WL, Messerli G, Trevisan M, Seymour MD, Gatehouse JA, Villadsen D, Smith SM, Chen J, Zeeman SC, Smith AM (2006) Similar protein phosphatases control starch metabolism in plants and glycogen metabolism in mammals. J Biol Chem 281: 11815–11818 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 Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, Hogenesch JB (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109: 307–320 Para A, Farre EM, Imaizumi T, Pruneda-Paz JL, Harmon FG, Kay SA (2007) PRR3 Is a vascular regulator of TOC1 stability in the Arabidopsis circadian clock. Plant Cell 19: 3462–3473 Perales M, Mas P (2007) A functional link between rhythmic changes in chromatin structure and the Arabidopsis biological clock. Plant Cell 19: 2111–2123 Pittendrigh CS, Daan S (1976) A functional analysis of circadian pacemakers in nocturnal rodents. V. A clock for all seasons. J Comp Physiol A 106: 333–355 Pruneda-Paz JL, Breton G, Para A, Kay SA (2009) A functional genomics approach reveals CHE as a component of the Arabidopsis circadian clock. Science 323: 1481–1485 Rand DA, Shulgin BV, Salazar D, Millar AJ (2004) Design principles underlying circadian clocks. J Roy Soc Interface 1: 119–130 Rand DA, Shulgin BV, Salazar JD, Millar AJ (2006) Uncovering the design principles of circadian clocks: mathematical analysis of flexibility and evolutionary goals. J Theor Biol 238: 616–635 Roenneberg T, Dragovic Z, Merrow M (2005) Demasking biological oscillators: properties and principles of entrainment exemplified by the Neurospora circadian clock. Proc Natl Acad Sci USA 102: 7742–7747 Smith SM, Fulton DC, Chia T, Thorneycroft D, Chapple A, Dunstan H, Hylton C, Zeeman SC, Smith AM (2004) Diurnal changes in the transcriptome encoding enzymes of starch metabolism provide evidence for both transcriptional and posttranscriptional regulation of starch metabolism in Arabidopsis leaves. Plant Physiol 136: 2687–2699 Stoleru D, Peng Y, Agosto J, Rosbash M (2004) Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431: 862–868 Thain SC, Hall A, Millar AJ (2000) Functional independence of circadian clocks that regulate plant gene expression. Curr Biol 10: 951–956 Thain SC, Murtas G, Lynn JR, McGrath RB, Millar AJ (2002) The circadian clock that controls gene expression in Arabidopsis is tissue specific. Plant Physiol 130: 102–110 Thomas B, Vince-Prue D (1997) Photoperiodism in Plants. San Diego, CA: Academic Press Troein C, Locke JC, Turner MS, Millar AJ (2009) Weather and seasons together demand complex biological clocks. Curr Biol 19: 1961–1964 Tsai TY, Choi YS, Ma W, Pomerening JR, Tang C, Ferrell Jr JE (2008) Robust, tunable biological oscillations from interlinked positive and negative feedback loops. Science 321: 126–129 Ueda HR, Chen W, Adachi A, Wakamatsu H, Hayashi S, Takasugi T, Nagano M, Nakahama K, Suzuki Y, Sugano S, Iino M, Shigeyoshi Y, Hashimoto S (2002) A transcription factor response element for gene expression during circadian night. Nature 418: 534–539 Usadel B, Blasing OE, Gibon Y, Retzlaff K, Hohne M, Gunther M, StittM (2008) Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis Rosettes. Plant Physiol 146: 1834–1861 Wilczek AM, Roe JL, Knapp MC, Cooper MD, Lopez-Gallego C, Martin LJ, Muir CD, Sim S, Walker A, Anderson J, Egan JF, Moyers BT, Petipas R, Giakountis A, Charbit E, Coupland G,Welch SM, Schmitt J (2009) Effects of genetic perturbation on seasonal life history plasticity. Science 323: 930–934 Yakir E, Hilman D, Hassidim M, Green RM (2007) CIRCADIAN CLOCK ASSOCIATED1 transcript stability and the entrainment of the circadian clock in Arabidopsis. Plant Physiol 145: 925–932 Zeeman SC, Smith SM, Smith AM (2007) The diurnal metabolism of leaf starch. Biochem J 401: 13–28 Zeilinger MN, Farre EM, Taylor SR, Kay SA, Doyle III FJ (2006) A novel computational model of the circadian clock in Arabidopsis that incorporates PRR7 and PRR9. Mol Syst Biol 2: 58
URI:	http://wrap.warwick.ac.uk/id/eprint/3969