Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Orchestrated Transcription of Key Pathways in Arabidopsis by the Circadian Clock
Stacey L. Harmer,1John B. Hogenesch,2Marty Straume,3Hur-Song Chang,4Bin Han,4Tong Zhu,4Xun Wang,4Joel A. Kreps,4Steve A. Kay12*
Like most organisms, plants have endogenous biological
clocks that coordinate internal events with the external environment.We used high-density oligonucleotide microarrays to examine geneexpression in Arabidopsis and found that 6% of the more
than 8000genes on the array exhibited circadian changes in
steady-statemessenger RNA levels. Clusters of circadian-regulated
genes werefound in pathways involved in plant responses to light and
otherkey metabolic pathways. Computational analysis of cycling genesallowed the identification of a highly conserved promoter motifthat we
found to be required for circadian control of gene expression.Our
study presents a comprehensive view of the temporal
compartmentalizationof physiological pathways by the circadian clock
in a eukaryote.
1 Department of Cell Biology, Scripps Research
Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA.
2 Genomics Institute of the Novartis Research
Foundation, 3115 Merryfield Row, La Jolla, CA 92121, USA.
3 Center for Biomathematical Technology, NSF Center
for Biological Timing, Division of Endocrinology and Metabolism,
Department of Internal Medicine, University of Virginia,
Charlottesville, VA 22904, USA.
4 Novartis
Agricultural Discovery Institute, 3115 Merryfield Row, San Diego, CA
92121, USA.
*
To whom correspondence should be addressed. E-mail:
stevek{at}scripps.edu
The editors suggest the following Related Resources on Science sites:
In Science Magazine
NEWS FOCUS
Elizabeth Pennisi (15 December 2000) Science290 (5499), 2054.
[DOI: 10.1126/science.290.5499.2054] |Summary »|Full Text »
NEWS FOCUS
Elizabeth Pennisi (15 December 2000) Science290 (5499), 2055.
[DOI: 10.1126/science.290.5499.2055] |Summary »|Full Text »
NEWS FOCUS
Elizabeth Pennisi (15 December 2000) Science290 (5499), 2056.
[DOI: 10.1126/science.290.5499.2056] |Summary »|Full Text »
NEWS FOCUS
Christine Mlot (15 December 2000) Science290 (5499), 2057.
[DOI: 10.1126/science.290.5499.2057] |Summary »|Full Text »
EDITORIAL
Caroline Dean (15 December 2000) Science290 (5499), 2071.
[DOI: 10.1126/science.290.5499.2071] |Summary »
POLICY FORUM
Chris Somerville and Jeff Dangl (15 December 2000) Science290 (5499), 2077.
[DOI: 10.1126/science.290.5499.2077] |Summary »|Full Text »
RESEARCH ARTICLES
J. L. Riechmann, J. Heard, G. Martin, L. Reuber, C. -Z., Jiang, J. Keddie, L. Adam, O. Pineda, O. J. Ratcliffe, R. R. Samaha, R. Creelman, M. Pilgrim, P. Broun, J. Z. Zhang, D. Ghandehari, B. K. Sherman, and G. -L. Yu (15 December 2000) Science290 (5499), 2105.
[DOI: 10.1126/science.290.5499.2105] |Abstract »|Full Text »|PDF »|Supplemental Data »
RESEARCH ARTICLES
Todd J. Vision, Daniel G. Brown, and Steven D. Tanksley (15 December 2000) Science290 (5499), 2114.
[DOI: 10.1126/science.290.5499.2114] |Abstract »|Full Text »|PDF »
THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
SENSITIVE TO FREEZING6 Integrates Cellular and Environmental Inputs to the Plant Circadian Clock.
H. Knight, A. J.W. Thomson, and H. G. McWatters (2008)
Plant Physiology
148, 293-303
|Abstract »|Full Text »|PDF »
The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors.
D. Huang, W. Wu, S. R. Abrams, and A. J. Cutler (2008)
J. Exp. Bot.
59, 2991-3007
|Abstract »|Full Text »|PDF »
Sugar beet contains a large CONSTANS-LIKE gene family including a CO homologue that is independent of the early-bolting (B) gene locus.
T. Y. P. Chia, A. Muller, C. Jung, and E. S. Mutasa-Gottgens (2008)
J. Exp. Bot.
59, 2735-2748
|Abstract »|Full Text »|PDF »
Circadian Timekeeping during Early Arabidopsis Development.
P. A. Salome, Q. Xie, and C. R. McClung (2008)
Plant Physiology
147, 1110-1125
|Abstract »|Full Text »|PDF »
Disruption of the Arabidopsis Circadian Clock Is Responsible for Extensive Variation in the Cold-Responsive Transcriptome.
Z. Bieniawska, C. Espinoza, A. Schlereth, R. Sulpice, D. K. Hincha, and M. A. Hannah (2008)
Plant Physiology
147, 263-279
|Abstract »|Full Text »|PDF »
Distinct Light-Initiated Gene Expression and Cell Cycle Programs in the Shoot Apex and Cotyledons of Arabidopsis.
E. Lopez-Juez, E. Dillon, Z. Magyar, S. Khan, S. Hazeldine, S. M. de Jager, J. A.H. Murray, G. T.S. Beemster, L. Bogre, and H. Shanahan (2008)
PLANT CELL
20, 947-968
|Abstract »|Full Text »|PDF »
Global Transcript Levels Respond to Small Changes of the Carbon Status during Progressive Exhaustion of Carbohydrates in Arabidopsis Rosettes.
B. Usadel, O. E. Blasing, Y. Gibon, K. Retzlaff, M. Hohne, M. Gunther, and M. Stitt (2008)
Plant Physiology
146, 1834-1861
|Abstract »|Full Text »|PDF »
Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1.
R. A. Gutierrez, T. L. Stokes, K. Thum, X. Xu, M. Obertello, M. S. Katari, M. Tanurdzic, A. Dean, D. C. Nero, C. R. McClung, et al. (2008)
PNAS
105, 4939-4944
|Abstract »|Full Text »|PDF »
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.
Identification of Dynamin as an Interactor of Rice GIGANTEA by Tandem Affinity Purification (TAP).
M. Abe, M. Fujiwara, K.-i. Kurotani, S. Yokoi, and K. Shimamoto (2008)
Plant Cell Physiol.
49, 420-432
|Abstract »|Full Text »|PDF »
FIONA1 Is Essential for Regulating Period Length in the Arabidopsis Circadian Clock.
J. Kim, Y. Kim, M. Yeom, J.-H. Kim, and H. G. Nam (2008)
PLANT CELL
20, 307-319
|Abstract »|Full Text »|PDF »
Evolutionary Radiation Pattern of Novel Protein Phosphatases Revealed by Analysis of Protein Data from the Completely Sequenced Genomes of Humans, Green Algae, and Higher Plants.
D. Kerk, G. Templeton, and G. B.G. Moorhead (2008)
Plant Physiology
146, 351-367
|Abstract »|Full Text »|PDF »
The Clock Protein CCA1 and the bZIP Transcription Factor HY5 Physically Interact to Regulate Gene Expression in Arabidopsis.
C. Andronis, S. Barak, S. M. Knowles, S. Sugano, and E. M. Tobin (2008)
Mol Plant
1, 58-67
|Abstract »|Full Text »|PDF »
The Development of Protein Microarrays and Their Applications in DNA Protein and Protein Protein Interaction Analyses of Arabidopsis Transcription Factors.
W. Gong, K. He, M. Covington, S. P. Dinesh-Kumar, M. Snyder, S. L. Harmer, Y.-X. Zhu, and X. W. Deng (2008)
Mol Plant
1, 27-41
|Abstract »|Full Text »|PDF »
The Arabidopsis Circadian Clock Incorporates a cADPR-Based Feedback Loop.
A. N. Dodd, M. J. Gardner, C. T. Hotta, K. E. Hubbard, N. Dalchau, J. Love, J.-M. Assie, F. C. Robertson, M. K. Jakobsen, J. Goncalves, et al. (2007)
Science
318, 1789-1792
|Abstract »|Full Text »|PDF »
Circadian rhythms of superhelical status of DNA in cyanobacteria.
M. A. Woelfle, Y. Xu, X. Qin, and C. H. Johnson (2007)
PNAS
104, 18819-18824
|Abstract »|Full Text »|PDF »
STRESS RESPONSE SUPPRESSOR1 and STRESS RESPONSE SUPPRESSOR2, Two DEAD-Box RNA Helicases That Attenuate Arabidopsis Responses to Multiple Abiotic Stresses.
P. Kant, S. Kant, M. Gordon, R. Shaked, and S. Barak (2007)
Plant Physiology
145, 814-830
|Abstract »|Full Text »|PDF »
CIRCADIAN CLOCK ASSOCIATED1 Transcript Stability and the Entrainment of the Circadian Clock in Arabidopsis.
E. Yakir, D. Hilman, M. Hassidim, and R. M. Green (2007)
Plant Physiology
145, 925-932
|Abstract »|Full Text »|PDF »
Cyclic changes in metabolic state during the life of a yeast cell.
B. P. Tu, R. E. Mohler, J. C. Liu, K. M. Dombek, E. T. Young, R. E. Synovec, and S. L. McKnight (2007)
PNAS
104, 16886-16891
|Abstract »|Full Text »|PDF »
Move on up, it's time for change mobile signals controlling photoperiod-dependent flowering.
Measuring Daylength: Pharbitis Takes a Different Approach.
N. A. Eckardt (2007)
PLANT CELL
19, 2968-2969
|Full Text »|PDF »
A Circadian Rhythm Set by Dusk Determines the Expression of FT Homologs and the Short-Day Photoperiodic Flowering Response in Pharbitis.
R. Hayama, B. Agashe, E. Luley, R. King, and G. Coupland (2007)
PLANT CELL
19, 2988-3000
|Abstract »|Full Text »|PDF »
The CHLI1 Subunit of Arabidopsis thaliana Magnesium Chelatase Is a Target Protein of the Chloroplast Thioredoxin.
A. Ikegami, N. Yoshimura, K. Motohashi, S. Takahashi, P. G. N. Romano, T. Hisabori, K.-i. Takamiya, and T. Masuda (2007)
J. Biol. Chem.
282, 19282-19291
|Abstract »|Full Text »|PDF »
A Complex Genetic Interaction Between Arabidopsis thaliana TOC1 and CCA1/LHY in Driving the Circadian Clock and in Output Regulation.
Z. Ding, M. R. Doyle, R. M. Amasino, and S. J. Davis (2007)
Genetics
176, 1501-1510
|Abstract »|Full Text »|PDF »
A Functional Link between Rhythmic Changes in Chromatin Structure and the Arabidopsis Biological Clock.
Top-down Phenomics of Arabidopsis thaliana: METABOLIC PROFILING BY ONE- AND TWO-DIMENSIONAL NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY AND TRANSCRIPTOME ANALYSIS OF ALBINO MUTANTS.
C. Tian, E. Chikayama, Y. Tsuboi, T. Kuromori, K. Shinozaki, J. Kikuchi, and T. Hirayama (2007)
J. Biol. Chem.
282, 18532-18541
|Abstract »|Full Text »|PDF »
The glycine decarboxylase complex multienzyme family in Populus.
M. Rajinikanth, S. A. Harding, and C.-J. Tsai (2007)
J. Exp. Bot.
58, 1761-1770
|Abstract »|Full Text »|PDF »
TIME FOR COFFEE Encodes a Nuclear Regulator in the Arabidopsis thaliana Circadian Clock.
Z. Ding, A. J. Millar, A. M. Davis, and S. J. Davis (2007)
PLANT CELL
19, 1522-1536
|Abstract »|Full Text »|PDF »
GIGANTEA Regulates Phytochrome A-Mediated Photomorphogenesis Independently of Its Role in the Circadian Clock.
K. A. Oliverio, M. Crepy, E. L. Martin-Tryon, R. Milich, S. L. Harmer, J. Putterill, M. J. Yanovsky, and J. J. Casal (2007)
Plant Physiology
144, 495-502
|Abstract »|Full Text »|PDF »
Disturbed Diurnal Rhythm Alters Gene Expression and Exacerbates Cardiovascular Disease With Rescue by Resynchronization.
T. A. Martino, N. Tata, D. D. Belsham, J. Chalmers, M. Straume, P. Lee, H. Pribiag, N. Khaper, P. P. Liu, F. Dawood, et al. (2007)
Hypertension
49, 1104-1113
|Abstract »|Full Text »|PDF »
Rapid Classification of Phenotypic Mutants of Arabidopsis via Metabolite Fingerprinting.
G. Messerli, V. Partovi Nia, M. Trevisan, A. Kolbe, N. Schauer, P. Geigenberger, J. Chen, A. C. Davison, A. R. Fernie, and S. C. Zeeman (2007)
Plant Physiology
143, 1484-1492
|Abstract »|Full Text »|PDF »
Conservation, Convergence, and Divergence of Light-Responsive, Circadian-Regulated, and Tissue-Specific Expression Patterns during Evolution of the Arabidopsis GATA Gene Family.
I. W. Manfield, P. F. Devlin, C.-H. Jen, D. R. Westhead, and P. M. Gilmartin (2007)
Plant Physiology
143, 941-958
|Abstract »|Full Text »|PDF »
GIGANTEA Acts in Blue Light Signaling and Has Biochemically Separable Roles in Circadian Clock and Flowering Time Regulation.
E. L. Martin-Tryon, J. A. Kreps, and S. L. Harmer (2007)
Plant Physiology
143, 473-486
|Abstract »|Full Text »|PDF »
Circadian Rhythms of Isoprene Biosynthesis in Grey Poplar Leaves.
M. Loivamaki, S. Louis, G. Cinege, I. Zimmer, R. J. Fischbach, and J.-P. Schnitzler (2007)
Plant Physiology
143, 540-551
|Abstract »|Full Text »|PDF »
No Promoter Left Behind: Global Circadian Gene Expression in Cyanobacteria..
M. A. Woelfle and C. H. Johnson (2006)
J Biol Rhythms
21, 419-431
|Abstract »|PDF »
Systems Biology of Circadian Rhythms: An Outlook..
L. De Haro and S. Panda (2006)
J Biol Rhythms
21, 507-518
|Abstract »|PDF »
Large-Scale cis-Element Detection by Analysis of Correlated Expression and Sequence Conservation between Arabidopsis and Brassica oleracea.
G. Haberer, M. T. Mader, P. Kosarev, M. Spannagl, L. Yang, and K. F.X. Mayer (2006)
Plant Physiology
142, 1589-1602
|Abstract »|Full Text »|PDF »
Duplicate maize 13-lipoxygenase genes are differentially regulated by circadian rhythm, cold stress, wounding, pathogen infection, and hormonal treatments.
A. Nemchenko, S. Kunze, I. Feussner, and M. Kolomiets (2006)
J. Exp. Bot.
57, 3767-3779
|Abstract »|Full Text »|PDF »
Cloning and Characterization of Deoxymugineic Acid Synthase Genes from Graminaceous Plants.
K. Bashir, H. Inoue, S. Nagasaka, M. Takahashi, H. Nakanishi, S. Mori, and N. K. Nishizawa (2006)
J. Biol. Chem.
281, 32395-32402
|Abstract »|Full Text »|PDF »
Arabidopsis FHY3 Specifically Gates Phytochrome Signaling to the Circadian Clock.
T. Allen, A. Koustenis, G. Theodorou, D. E. Somers, S. A. Kay, G. C. Whitelam, and P. F. Devlin (2006)
PLANT CELL
18, 2506-2516
|Abstract »|Full Text »|PDF »
Circadian Clock Regulation of Starch Metabolism Establishes GBSSI as a Major Contributor to Amylopectin Synthesis in Chlamydomonas reinhardtii.
J.-P. Ral, C. Colleoni, F. Wattebled, D. Dauvillee, C. Nempont, P. Deschamps, Z. Li, M. K. Morell, R. Chibbar, S. Purton, et al. (2006)
Plant Physiology
142, 305-317
|Abstract »|Full Text »|PDF »
Arabidopsis SPA proteins regulate photoperiodic flowering and interact with the floral inducer CONSTANS to regulate its stability.
S. Laubinger, V. Marchal, J. Gentilhomme, S. Wenkel, J. Adrian, S. Jang, C. Kulajta, H. Braun, G. Coupland, and U. Hoecker (2006)
Development
133, 3213-3222
|Abstract »|Full Text »|PDF »
Two-component signaling provides the major output from the cyanobacterial circadian clock.
Twenty-Four-Hour Rhythmic Gene Expression in the Rhesus Macaque Adrenal Gland.
D. R. Lemos, J. L. Downs, and H. F. Urbanski (2006)
Mol. Endocrinol.
20, 1164-1176
|Abstract »|Full Text »|PDF »
Diurnal Regulation of the Brassinosteroid-Biosynthetic CPD Gene in Arabidopsis.
S. Bancos, A.-M. Szatmari, J. Castle, L. Kozma-Bognar, K. Shibata, T. Yokota, G. J. Bishop, F. Nagy, and M. Szekeres (2006)
Plant Physiology
141, 299-309
|Abstract »|Full Text »|PDF »
Isolation of cDNAs for R2R3-MYB, bHLH and WDR Transcriptional Regulators and Identification of c and ca Mutations Conferring White Flowers in the Japanese Morning Glory.
Y. Morita, M. Saitoh, A. Hoshino, E. Nitasaka, and S. Iida (2006)
Plant Cell Physiol.
47, 457-470
|Abstract »|Full Text »|PDF »
Analysis of Phase of LUCIFERASE Expression Reveals Novel Circadian Quantitative Trait Loci in Arabidopsis.
C. Darrah, B. L. Taylor, K. D. Edwards, P. E. Brown, A. Hall, and H. G. McWatters (2006)
Plant Physiology
140, 1464-1474
|Abstract »|Full Text »|PDF »
Diel patterns of leaf C export and of main shoot growth for Flaveria linearis with altered leaf sucrose-starch partitioning.
E. D. Leonardos, B. J. Micallef, M. C. Micallef, and B. Grodzinski (2006)
J. Exp. Bot.
57, 801-814
|Abstract »|Full Text »|PDF »
FLOWERING LOCUS C Mediates Natural Variation in the High-Temperature Response of the Arabidopsis Circadian Clock.
K. D. Edwards, P. E. Anderson, A. Hall, N. S. Salathia, J. C.W. Locke, J. R. Lynn, M. Straume, J. Q. Smith, and A. J. Millar (2006)
PLANT CELL
18, 639-650
|Abstract »|Full Text »|PDF »
AGRIS and AtRegNet. A Platform to Link cis-Regulatory Elements and Transcription Factors into Regulatory Networks.
S. K. Palaniswamy, S. James, H. Sun, R. S. Lamb, R. V. Davuluri, and E. Grotewold (2006)
Plant Physiology
140, 818-829
|Abstract »|Full Text »|PDF »
Real-Time Monitoring of Chloroplast Gene Expression by a Luciferase Reporter: Evidence for Nuclear Regulation of Chloroplast Circadian Period.
T. Matsuo, K. Onai, K. Okamoto, J. Minagawa, and M. Ishiura (2006)
Mol. Cell. Biol.
26, 863-870
|Abstract »|Full Text »|PDF »
Detecting periodic patterns in unevenly spaced gene expression time series using Lomb-Scargle periodograms.
E. F. Glynn, J. Chen, and A. R. Mushegian (2006)
Bioinformatics
22, 310-316
|Abstract »|Full Text »|PDF »
Sucrose-Specific Induction of the Anthocyanin Biosynthetic Pathway in Arabidopsis.
C. Solfanelli, A. Poggi, E. Loreti, A. Alpi, and P. Perata (2006)
Plant Physiology
140, 637-646
|Abstract »|Full Text »|PDF »
Systemic signalling of environmental cues in Arabidopsis leaves.
S. A. Coupe, B. G. Palmer, J. A. Lake, S. A. Overy, K. Oxborough, F. I. Woodward, J. E. Gray, and W. P. Quick (2006)
J. Exp. Bot.
57, 329-341
|Abstract »|Full Text »|PDF »
A Circadian Rhythm-Regulated Tomato Gene Is Induced by Arachidonic Acid and Phythophthora infestans Infection.
P. D. Weyman, Z. Pan, Q. Feng, D. G. Gilchrist, and R. M. Bostock (2006)
Plant Physiology
140, 235-248
|Abstract »|Full Text »|PDF »
Sugars and Circadian Regulation Make Major Contributions to the Global Regulation of Diurnal Gene Expression in Arabidopsis.
O. E. Blasing, Y. Gibon, M. Gunther, M. Hohne, R. Morcuende, D. Osuna, O. Thimm, B. Usadel, W.-R. Scheible, and M. Stitt (2005)
PLANT CELL
17, 3257-3281
|Abstract »|Full Text »|PDF »
A Model for the Circadian Oscillations in Expression and Activity of Nitrate Reductase in Higher Plants.
Differential Expression of Sucrose-Phosphate Synthase Isoenzymes in Tobacco Reflects Their Functional Specialization during Dark-Governed Starch Mobilization in Source Leaves.
S. Chen, M. Hajirezaei, and F. Bornke (2005)
Plant Physiology
139, 1163-1174
|Abstract »|Full Text »|PDF »
Functional Characterization of Phytochrome Interacting Factor 3 for the Arabidopsis thaliana Circadian Clockwork.
A. Viczian, S. Kircher, E. Fejes, A. J. Millar, E. Schafer, L. Kozma-Bognar, and F. Nagy (2005)
Plant Cell Physiol.
46, 1591-1602
|Abstract »|Full Text »|PDF »
Microarray Analysis Reveals Vegetative Molecular Phenotypes of Arabidopsis Flowering-time Mutants.
I. W. Wilson, G. C. Kennedy, J. W. Peacock, and E. S. Dennis (2005)
Plant Cell Physiol.
46, 1190-1201
|Abstract »|Full Text »|PDF »
Daylength and Circadian Effects on Starch Degradation and Maltose Metabolism.
Y. Lu, J. P. Gehan, and T. D. Sharkey (2005)
Plant Physiology
138, 2280-2291
|Abstract »|Full Text »|PDF »
Circadian Control of Messenger RNA Stability. Association with a Sequence-Specific Messenger RNA Decay Pathway.
P. Lidder, R. A. Gutierrez, P. A. Salome, C. R. McClung, and P. J. Green (2005)
Plant Physiology
138, 2374-2385
|Abstract »|Full Text »|PDF »
Plant Circadian Clocks Increase Photosynthesis, Growth, Survival, and Competitive Advantage.
A. N. Dodd, N. Salathia, A. Hall, E. Kevei, R. Toth, F. Nagy, J. M. Hibberd, A. J. Millar, and A. A. R. Webb (2005)
Science
309, 630-633
|Abstract »|Full Text »|PDF »
LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms.
S. P. Hazen, T. F. Schultz, J. L. Pruneda-Paz, J. O. Borevitz, J. R. Ecker, and S. A. Kay (2005)
PNAS
102, 10387-10392
|Abstract »|Full Text »|PDF »