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PMID: 16299223 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis.

The Plant cell ·Vol. 17 ·No. 12 ·2005-12-00 ·Pages 3257-81

Bläsing OE, Gibon Y, Günther M, Höhne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible WR, Stitt M

Abstract

The diurnal cycle strongly influences many plant metabolic and physiological processes. Arabidopsis thaliana rosettes were harvested six times during 12-h-light/12-h-dark treatments to investigate changes in gene expression using ATH1 arrays. Diagnostic gene sets were identified from published or in-house expression profiles of the response to light, sugar, nitrogen, and water deficit in seedlings and 4 h of darkness or illumination at ambient or compensation point [CO(2)]. Many sugar-responsive genes showed large diurnal expression changes, whose timing matched that of the diurnal changes of sugars. A set of circadian-regulated genes also showed large diurnal changes in expression. Comparison of published results from a free-running cycle with the diurnal changes in Columbia-0 (Col-0) and the starchless phosphoglucomutase (pgm) mutant indicated that sugars modify the expression of up to half of the clock-regulated genes. Principle component analysis identified genes that make large contributions to diurnal changes and confirmed that sugar and circadian regulation are the major inputs in Col-0 but that sugars dominate the response in pgm. Most of the changes in pgm are triggered by low sugar levels during the night rather than high levels in the light, highlighting the importance of responses to low sugar in diurnal gene regulation. We identified a set of candidate regulatory genes that show robust responses to alterations in sugar levels and change markedly during the diurnal cycle.

MeSH Terms
Arabidopsis/genetics Carbohydrates/physiology Circadian Rhythm Gene Expression Regulation, Plant/physiology Genes, Plant Mutation Nitrogen/physiology RNA, Messenger/genetics
Chemicals
Carbohydrates RNA, Messenger Nitrogen
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Bläsing Oliver E
Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, Germany. [email protected]
Gibon Yves
Günther Manuela
Höhne Melanie
Morcuende Rosa
Osuna Daniel
Thimm Oliver
Usadel Björn
Scheible Wolf-Rüdiger
Stitt Mark
References (53)
53 references, click to expand
  1. Sugar sensing and signalling networks in plants.
    Biochem Soc Trans. 2005 Feb;33(Pt 1):269-71 PMID: 15667323
  2. Transgenic plants changed in carbon allocation pattern display a shift in diurnal growth pattern.
    Plant J. 1998 Nov;16(4):497-503 PMID: 9881169
  3. Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana.
    Plant J. 2004 Jun;38(5):823-39 PMID: 15144383
  4. Molecular bases of circadian rhythms.
    Annu Rev Cell Dev Biol. 2001;17:215-53 PMID: 11687489
  5. Circadian clocks in daily and seasonal control of development.
    Science. 2003 Jul 18;301(5631):326-8 PMID: 12869749
  6. Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism.
    Plant Physiol. 2003 Jun;132(2):556-67 PMID: 12805587
  7. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock.
    Science. 2000 Dec 15;290(5499):2110-3 PMID: 11118138
  8. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes.
    Plant J. 2004 Mar;37(6):914-39 PMID: 14996223
  9. Diurnal changes in sucrose, nucleotides, starch synthesis and AGPS transcript in growing potato tubers that are suppressed by decreased expression of sucrose phosphate synthase.
    Plant J. 2000 Sep;23(6):795-806 PMID: 10998190
  10. A plant snoRNP complex containing snoRNAs, fibrillarin, and nucleolin-like proteins is competent for both rRNA gene binding and pre-rRNA processing in vitro.
    Mol Cell Biol. 2004 Aug;24(16):7284-97 PMID: 15282326
  11. Expression profiling of phyB mutant demonstrates substantial contribution of other phytochromes to red-light-regulated gene expression during seedling de-etiolation.
    Plant J. 2004 Jun;38(5):725-39 PMID: 15144375
  12. Shedding light on the circadian clock and the photoperiodic control of flowering.
    Curr Opin Plant Biol. 2003 Feb;6(1):13-9 PMID: 12495746
  13. Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period.
    Plant J. 2004 Sep;39(6):847-62 PMID: 15341628
  14. Genome-wide investigation of light and carbon signaling interactions in Arabidopsis.
    Genome Biol. 2004;5(2):R10 PMID: 14759260
  15. A proteomic study of the arabidopsis nuclear matrix.
    J Cell Biochem. 2003 Oct 1;90(2):361-78 PMID: 14505352
  16. Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of corresponding genes, and comparison with known responses.
    Plant Physiol. 2005 Jul;138(3):1195-204 PMID: 16009995
  17. Nitrate Acts as a Signal to Induce Organic Acid Metabolism and Repress Starch Metabolism in Tobacco.
    Plant Cell. 1997 May;9(5):783-798 PMID: 12237366
  18. Alterations in Growth, Photosynthesis, and Respiration in a Starchless Mutant of Arabidopsis thaliana (L.) Deficient in Chloroplast Phosphoglucomutase Activity.
    Plant Physiol. 1985 Sep;79(1):11-7 PMID: 16664354
  19. Identifying periodically expressed transcripts in microarray time series data.
    Bioinformatics. 2004 Jan 1;20(1):5-20 PMID: 14693803
  20. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias.
    Bioinformatics. 2003 Jan 22;19(2):185-93 PMID: 12538238
  21. A starch-accumulating mutant of Arabidopsis thaliana deficient in a chloroplastic starch-hydrolysing enzyme.
    Plant J. 1998 Aug;15(3):357-65 PMID: 9750347
  22. Functional identification of an Arabidopsis snf4 ortholog by screening for heterologous multicopy suppressors of snf4 deficiency in yeast.
    Plant J. 2000 Jul;23(1):115-22 PMID: 10929106
  23. Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen.
    Plant Physiol. 2004 Sep;136(1):2483-99 PMID: 15375205
  24. Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray.
    Plant J. 2002 Aug;31(3):279-92 PMID: 12164808
  25. Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana.
    Nature. 2003 Dec 4;426(6966):567-70 PMID: 14654842
  26. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression.
    Cell. 1998 Jun 26;93(7):1207-17 PMID: 9657153
  27. Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis.
    Plant Cell. 2001 Jan;13(1):113-23 PMID: 11158533
  28. AtGRP7, a nuclear RNA-binding protein as a component of a circadian-regulated negative feedback loop in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 1997 Aug 5;94(16):8515-20 PMID: 9238008
  29. TM4: a free, open-source system for microarray data management and analysis.
    Biotechniques. 2003 Feb;34(2):374-8 PMID: 12613259
  30. The role of ion channels in light-dependent stomatal opening.
    J Exp Bot. 2001 Oct;52(363):1959-67 PMID: 11559731
  31. The Arabidopsis ATR1 Myb transcription factor controls indolic glucosinolate homeostasis.
    Plant Physiol. 2005 Jan;137(1):253-62 PMID: 15579661
  32. Growth of tobacco in short-day conditions leads to high starch, low sugars, altered diurnal changes in the Nia transcript and low nitrate reductase activity, and inhibition of amino acid synthesis.
    Planta. 1998 Dec;207(1):27-41 PMID: 9951717
  33. Regulation of spinach SNF1-related (SnRK1) kinases by protein kinases and phosphatases is associated with phosphorylation of the T loop and is regulated by 5'-AMP.
    Plant J. 1999 Aug;19(4):433-9 PMID: 10504565
  34. Transcriptome profiling of the response of Arabidopsis suspension culture cells to Suc starvation.
    Plant Physiol. 2004 Aug;135(4):2330-47 PMID: 15310832
  35. Autophagic recycling: lessons from yeast help define the process in plants.
    Curr Opin Plant Biol. 2005 Apr;8(2):165-73 PMID: 15752997
  36. Diurnal changes in allocation of newly fixed carbon in exporting sugar beet leaves.
    Plant Physiol. 1985 Aug;78(4):753-7 PMID: 16664319
  37. Light-regulated translation mediates gated induction of the Arabidopsis clock protein LHY.
    EMBO J. 2003 Feb 17;22(4):935-44 PMID: 12574129
  38. Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis.
    Plant Cell. 2004 Aug;16(8):2128-50 PMID: 15273295
  39. Daylength and circadian effects on starch degradation and maltose metabolism.
    Plant Physiol. 2005 Aug;138(4):2280-91 PMID: 16055686
  40. Sensitive and high throughput metabolite assays for inorganic pyrophosphate, ADPGlc, nucleotide phosphates, and glycolytic intermediates based on a novel enzymic cycling system.
    Plant J. 2002 Apr;30(2):221-35 PMID: 12000458
  41. A Robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness.
    Plant Cell. 2004 Dec;16(12):3304-25 PMID: 15548738
  42. Tobacco mutants with a decreased number of functional nia genes compensate by modifying the diurnal regulation of transcription, post-translational modification and turnover of nitrate reductase.
    Planta. 1997;203(3):304-19 PMID: 9431679
  43. ADP-glucose pyrophosphorylase is activated by posttranslational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species.
    Plant Physiol. 2003 Oct;133(2):838-49 PMID: 12972664
  44. The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana.
    J Biol Chem. 2002 Sep 6;277(36):33105-14 PMID: 12070171
  45. Cullins 3a and 3b assemble with members of the broad complex/tramtrack/bric-a-brac (BTB) protein family to form essential ubiquitin-protein ligases (E3s) in Arabidopsis.
    J Biol Chem. 2005 May 13;280(19):18810-21 PMID: 15749712
  46. Control of Leaf Expansion Rate of Droughted Maize Plants under Fluctuating Evaporative Demand (A Superposition of Hydraulic and Chemical Messages?).
    Plant Physiol. 1997 Jul;114(3):893-900 PMID: 12223750
  47. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage.
    Science. 2005 Jul 22;309(5734):630-3 PMID: 16040710
  48. 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. 2004 Sep;136(1):2687-99 PMID: 15347792
  49. Circadian rhythms confer a higher level of fitness to Arabidopsis plants.
    Plant Physiol. 2002 Jun;129(2):576-84 PMID: 12068102
  50. CARBOHYDRATE-MODULATED GENE EXPRESSION IN PLANTS.
    Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47:509-540 PMID: 15012299
  51. Constitutive expression of nitrate reductase allows normal growth and development of Nicotiana plumbaginifolia plants.
    EMBO J. 1991 May;10(5):1027-35 PMID: 2022181
  52. Control of plant development and gene expression by sugar signaling.
    Curr Opin Plant Biol. 2005 Feb;8(1):93-102 PMID: 15653406
  53. The Brix domain protein family -- a key to the ribosomal biogenesis pathway?
    Trends Biochem Sci. 2001 Jun;26(6):345-7 PMID: 11406393
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2005-12-00
Epub
2005-00-18
Pages
3257-81
Language
English
Region
England
NLM ID
9208688
PMCID
PMC1315368
Subset
IM
Databases
OMIM
GSE3416, GSE3423, GSE3424
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