Photosynthetic Entrainment of the Arabidopsis Thaliana Circadian Clock

Overview

Journal Nature

Specialty Science

Date 2013 Oct 25

PMID 24153186

Citations 194

Authors

Michael J Haydon

Olga Mielczarek

Fiona C Robertson

Katharine E Hubbard

Alex A R Webb

Affiliations

Soon will be listed here.

Abstract

Circadian clocks provide a competitive advantage in an environment that is heavily influenced by the rotation of the Earth, by driving daily rhythms in behaviour, physiology and metabolism in bacteria, fungi, plants and animals. Circadian clocks comprise transcription-translation feedback loops, which are entrained by environmental signals such as light and temperature to adjust the phase of rhythms to match the local environment. The production of sugars by photosynthesis is a key metabolic output of the circadian clock in plants. Here we show that these rhythmic, endogenous sugar signals can entrain circadian rhythms in Arabidopsis thaliana by regulating the gene expression of circadian clock components early in the photoperiod, thus defining a 'metabolic dawn'. By inhibiting photosynthesis, we demonstrate that endogenous oscillations in sugar levels provide metabolic feedback to the circadian oscillator through the morning-expressed gene PSEUDO-RESPONSE REGULATOR 7 (PRR7), and we identify that prr7 mutants are insensitive to the effects of sucrose on the circadian period. Thus, photosynthesis has a marked effect on the entrainment and maintenance of robust circadian rhythms in A. thaliana, demonstrating that metabolism has a crucial role in regulation of the circadian clock.

Citing Articles

Modelling photosynthetic responses by day and night during initial water stress in Pulmonaria vallarsae.

Pupillo P, Sparla F, Melandri B, Trost P Physiol Plant. 2024; 176(6):e70004.

PMID: 39658793 PMC: 11632138. DOI: 10.1111/ppl.70004.

An Arabidopsis Cell Culture With Weak Circadian Rhythms Under Constant Light Compared With Constant Dark Can Be Rescued by ELF3.

Laosuntisuk K, Desai J, Doherty C Plant Direct. 2024; 8(11):1-16.

PMID: 39610858 PMC: 11603095. DOI: 10.1002/pld3.70028.

Interference of skeleton photoperiod in circadian clock and photosynthetic efficiency of tea plant: in-depth analysis of mathematical model.

Hu Z, Huang T, Zhang N, Chen C, Yang K, Sun M Hortic Res. 2024; 11(10):uhae226.

PMID: 39415971 PMC: 11480659. DOI: 10.1093/hr/uhae226.

Two KaiABC systems control circadian oscillations in one cyanobacterium.

Kobler C, Schmelling N, Wiegard A, Pawlowski A, Pattanayak G, Spat P Nat Commun. 2024; 15(1):7674.

PMID: 39227593 PMC: 11372060. DOI: 10.1038/s41467-024-51914-5.

Mitochondrial ATP Synthase -Subunit Affects Plastid Retrograde Signaling in .

Liu H, Liu Z, Qin A, Zhou Y, Sun S, Liu Y Int J Mol Sci. 2024; 25(14).

PMID: 39063070 PMC: 11277312. DOI: 10.3390/ijms25147829.

References

Nakamichi N, Kiba T, Henriques R, Mizuno T, Chua N, Sakakibara H . PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell. 2010; 22(3):594-605. PMC: 2861452. DOI: 10.1105/tpc.109.072892. View

Harmer S, Hogenesch J, Straume M, Chang H, Han B, Zhu T . Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science. 2000; 290(5499):2110-3. DOI: 10.1126/science.290.5499.2110. View

Ni M, Tepperman J, Quail P . PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell. 1998; 95(5):657-67. DOI: 10.1016/s0092-8674(00)81636-0. View

Fukushima A, Kusano M, Nakamichi N, Kobayashi M, Hayashi N, Sakakibara H . Impact of clock-associated Arabidopsis pseudo-response regulators in metabolic coordination. Proc Natl Acad Sci U S A. 2009; 106(17):7251-6. PMC: 2667372. DOI: 10.1073/pnas.0900952106. View

Harmer S . The circadian system in higher plants. Annu Rev Plant Biol. 2009; 60:357-77. DOI: 10.1146/annurev.arplant.043008.092054. View

Jarillo J, Capel J, Tang R, Yang H, Alonso J, Ecker J . An Arabidopsis circadian clock component interacts with both CRY1 and phyB. Nature. 2001; 410(6827):487-90. DOI: 10.1038/35068589. View

Xiong L, Ishitani M, Lee H, Zhu J . The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. Plant Cell. 2001; 13(9):2063-83. PMC: 139452. DOI: 10.1105/tpc.010101. View

Cho Y, Yoo S . Signaling role of fructose mediated by FINS1/FBP in Arabidopsis thaliana. PLoS Genet. 2011; 7(1):e1001263. PMC: 3017112. DOI: 10.1371/journal.pgen.1001263. View

Blasing O, Gibon Y, Gunther M, Hohne M, Morcuende R, Osuna D . Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell. 2005; 17(12):3257-81. PMC: 1315368. DOI: 10.1105/tpc.105.035261. View

10.

Dodd A, Salathia N, Hall A, Kevei E, Toth R, Nagy F . Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science. 2005; 309(5734):630-3. DOI: 10.1126/science.1115581. View

11.

Oyama T, Shimura Y, Okada K . The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev. 1997; 11(22):2983-95. PMC: 316701. DOI: 10.1101/gad.11.22.2983. View

12.

Johnson C, Kondo T, Hastings J . Action Spectrum for Resetting the Circadian Phototaxis Rhythm in the CW15 Strain of Chlamydomonas: II. Illuminated Cells. Plant Physiol. 1991; 97(3):1122-9. PMC: 1081131. DOI: 10.1104/pp.97.3.1122. View

13.

Dalchau N, Baek S, Briggs H, Robertson F, Dodd A, Gardner M . The circadian oscillator gene GIGANTEA mediates a long-term response of the Arabidopsis thaliana circadian clock to sucrose. Proc Natl Acad Sci U S A. 2011; 108(12):5104-9. PMC: 3064355. DOI: 10.1073/pnas.1015452108. View

14.

Knight H, Thomson A, McWatters H . Sensitive to freezing6 integrates cellular and environmental inputs to the plant circadian clock. Plant Physiol. 2008; 148(1):293-303. PMC: 2528108. DOI: 10.1104/pp.108.123901. View

15.

Reed J, Nagatani A, Elich T, Fagan M, Chory J . Phytochrome A and Phytochrome B Have Overlapping but Distinct Functions in Arabidopsis Development. Plant Physiol. 1994; 104(4):1139-1149. PMC: 159274. DOI: 10.1104/pp.104.4.1139. View

16.

Nakamichi N, Kita M, Ito S, Yamashino T, Mizuno T . PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol. 2005; 46(5):686-98. DOI: 10.1093/pcp/pci086. View

17.

Leung J, Bouvier-Durand M, Morris P, Guerrier D, Chefdor F, Giraudat J . Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science. 1994; 264(5164):1448-52. DOI: 10.1126/science.7910981. View

18.

James A, Monreal J, Nimmo G, Kelly C, Herzyk P, Jenkins G . The circadian clock in Arabidopsis roots is a simplified slave version of the clock in shoots. Science. 2008; 322(5909):1832-5. DOI: 10.1126/science.1161403. View

19.

Ahmad M, Cashmore A . HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature. 1993; 366(6451):162-6. DOI: 10.1038/366162a0. View

20.

Graf A, Schlereth A, Stitt M, Smith A . Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc Natl Acad Sci U S A. 2010; 107(20):9458-63. PMC: 2889127. DOI: 10.1073/pnas.0914299107. View