Photosynthetic entrainment of the arabidopsis thaliana circadian clock

ABSTRACT Circadian clocks provide a competitive advantage in an environment that is heavily influenced by the rotation of the Earth1,2, by driving daily rhythms in behaviour, physiology and

metabolism in bacteria, fungi, plants and animals3,4. 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 environment3. The production of sugars by photosynthesis is a key metabolic output of the circadian clock in plants2,5. 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

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Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS ASCHOFF’S RULE ON CIRCADIAN RHYTHMS ORCHESTRATED BY BLUE LIGHT SENSOR CRY2 AND CLOCK COMPONENT PRR9 Article Open access 05

October 2022 LOW-TEMPERATURE AND CIRCADIAN SIGNALS ARE INTEGRATED BY THE SIGMA FACTOR SIG5 Article Open access 30 March 2023 CENTRAL TRANSCRIPTIONAL REGULATOR CONTROLS PHOTOSYNTHETIC GROWTH

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ACKNOWLEDGEMENTS This work was supported by BBSRC grant BB/H006826/1. We thank J. O’Neill, J. Davies and J. Hibberd for comments on the manuscript. AUTHOR INFORMATION Author notes * Michael

J. Haydon & Fiona C. Robertson Present address: Present addresses: Department of Biology, University of York, York YO10 5DD, UK (M.J.H.); Department of Biochemistry, University of

Zimbabwe, PO Box MP45, Harare, Zimbabwe (F.C.R.)., AUTHORS AND AFFILIATIONS * Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, UK, Michael J. Haydon, Olga

Mielczarek, Fiona C. Robertson, Katharine E. Hubbard & Alex A. R. Webb Authors * Michael J. Haydon View author publications You can also search for this author inPubMed Google Scholar *

Olga Mielczarek View author publications You can also search for this author inPubMed Google Scholar * Fiona C. Robertson View author publications You can also search for this author

inPubMed Google Scholar * Katharine E. Hubbard View author publications You can also search for this author inPubMed Google Scholar * Alex A. R. Webb View author publications You can also

search for this author inPubMed Google Scholar CONTRIBUTIONS M.J.H. and A.A.R.W. designed the research. M.J.H., O.M., F.C.R. and K.E.H. performed the experiments and analysed the data.

M.J.H. and A.A.R.W. prepared the manuscript. CORRESPONDING AUTHOR Correspondence to Alex A. R. Webb. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing financial

interests. EXTENDED DATA FIGURES AND TABLES EXTENDED DATA FIGURE 1 A MODEL FOR ENTRAINMENT OF THE _A. THALIANA_ CIRCADIAN CLOCK BY PHOTOSYNTHETICALLY DERIVED SUGARS. From dawn, light

activates _PRR7_ and drives photosynthesis. The concentrations of simple sugars produced by photosynthesis accumulate within the plant during the day (red dashed line), peaking around 4–8 h

after dawn. High endogenous sugar concentrations lead to suppression of the _PRR7_ promoter, contributing to the phase of _PRR7_ rhythms. PRR7 is a transcriptional repressor of the circadian

clock component CCA1. Thus, the rhythms of endogenous sugars derived from photosynthesis contribute to circadian entrainment through PRR7. We propose that the timing of these events

represents a ‘metabolic dawn’. Dawn is a time-dependent gradient of light intensity, whereas ‘metabolic dawn’ represents a gradient of increasing metabolite concentration. The metabolic

gradient lags behind that of light and contributes to the setting of the circadian clock. In the model, previously established relationships are shown by black connectors, and novel

relationships proposed in this study are shown by orange connectors. EXTENDED DATA FIGURE 2 EFFECTS OF EXOGENOUS SUCROSE AND PHOTOSYNTHESIS INHIBITION ON CIRCADIAN RHYTHMS. A, B, Period

estimates for the rhythms of the promoter:LUC reporters in continuous low light (A) or continuous light (B) in plants grown in media with or without sucrose (mean ± s.d.; _n_ = 4). C, D,

Promoter:LUC reporter rhythms (mean ± s.e.m.) and relative amplitude error versus period plots for seedlings in media in the presence or absence of DCMU in continuous low light (C) or

continuous light (D) (_n_ = 4). * _P_ < 0.05; ** _P_ < 0.01; *** _P_ < 0.001; compared with untreated plants by two-tailed Student’s _t_-test. _n_ refers to number of biological

replicates. EXTENDED DATA FIGURE 3 THE RHYTHMS OF ENDOGENOUS SUGARS PEAK IN THE MORNING AND ARE REDUCED BY INHIBITION OF PHOTOSYNTHESIS. A, Leaf sucrose and glucose concentrations in

10-day-old seedlings growing in 12 h light and 12 h dark cycles (mean ± s.d.; _n_ = 3). B, Glucose, fructose and sucrose concentrations 4 h after subjective dawn in 13-day-old seedlings

grown in CO2-free air or ambient air in continuous low light for 5 days (mean ± s.d.; _n_ = 3). C, Glucose concentration in 10-day-old seedlings growing in a light–dark cycle at 12–36 h

after transfer to DCMU or control media at dusk (mean ± s.d.; _n_ = 3). * _P_ < 0.05; ** _P_ < 0.01 by two-tailed Student’s _t_-test compared with ZT0 in A and compared with control

conditions in B and C. _n_ refers to number of biological replicates. EXTENDED DATA FIGURE 4 EFFECTS OF DCMU, NORFLURAZON OR LINCOMYCIN ON _CCA1:LUC_ RHYTHMS IN THE PRESENCE OR ABSENCE OF

EXOGENOUS SUCROSE. A, _CCA1:LUC_ rhythms in continuous low light for seedlings transferred to media containing DCMU in the presence of the indicated exogenous sucrose concentrations compared

with control media (mean ± s.e.m.; _n_ = 4). B, _CCA1:LUC_ rhythms in continuous light for seedlings transferred to media containing DCMU, norflurazon or lincomycin in the absence (left) or

presence (right) of exogenous sucrose (mean ± s.e.m.; _n_ = 4). _n_ refers to number of biological replicates. EXTENDED DATA FIGURE 5 ALTERING REACTIVE OXYGEN SPECIES (ROS) PRODUCTION DOES

NOT INFLUENCE CIRCADIAN RHYTHMS. A, _CAB2:LUC_ rhythms in seedlings transferred to continuous light and treated with 1 mM glutathione or 5 mM ascorbate. The short-period mutant _toc1-1_ and

long-period mutant _ztl-1_ were included as positive controls (means ± s.d.; _n_ = 2–3). B, Relative amplitude error versus period plot for leaf movement rhythms in wild-type plants and

NADPH oxidase _rbohD,F_ mutants45 in continuous light (mean ± s.e.m.). C, Promoter:LUC rhythms and relative amplitude error versus period plots for seedlings grown in continuous light or

continuous low light and treated with 10 µM diphenyleneiodonium (DPI) or 0.1% (v/v) dimethylsulphoxide (DMSO) at 0 h (mean ± s.e.m.; _n_ = 4). _n_ refers to number of biological replicates.

EXTENDED DATA FIGURE 6 METABOLICALLY ACTIVE SUGARS SUSTAIN CIRCADIAN RHYTHMS IN DARKNESS. A, _CCA1:LUC_ rhythms in continuous dark in seedlings grown in media containing the indicated sugars

or control treatments (mean ± s.e.m.; _n_ = 4). B, Promoter:LUC rhythms (mean ± s.e.m.; _n_ = 4) and relative amplitude error versus period plots (_n_ = 4–8) for seedlings grown in

continuous dark in media with or without sucrose. Note that rhythms could not be detected in seedlings grown without sucrose for the morning-expressed _CCA1:LUC_ or _PRR9:LUC_ but could be

detected for the evening-expressed _GI:LUC_ and _TOC1:LUC_, despite the small amplitude. _n_ refers to number of biological replicates. EXTENDED DATA FIGURE 7 EXOGENOUS SUGAR CAN SET THE

CIRCADIAN PHASE IN DARK-ADAPTED SEEDLINGS. A, Time to the first circadian peak of promoter:LUC reporters in seedlings treated with sucrose after 72 h (subjective dawn, CT0) or 84 h

(subjective dusk, CT12) in continuous dark (mean ± s.d.; _n_ = 4). B, Promoter:LUC rhythms of seedlings after sucrose or mannitol treatment as in A (mean ± s.e.m.; _n_ = 4). C, _CCA1_

transcript level relative to _UBQ10_ in seedlings treated with sucrose or mannitol after 72 h in continuous dark (mean ± s.d.; _n_ = 3). ** _P_ < 0.01; *** _P_ < 0.001 by two-tailed

Student’s _t_-test. _n_ refers to number of biological replicates. EXTENDED DATA FIGURE 8 PHASE SETTING BY SUGAR AND LIGHT. A, Change in the period of _CCA1:LUC_ after pulses of sucrose

compared with control seedlings in continuous low light (mean ± s.d.; _n_ = 8). B, Phase response of _TOC1:LUC_ to pulses of sucrose for seedlings in continuous low light (mean ± s.d.; _n_ =

8). C, Phase response of _CCA1:LUC_ to pulses of mannitol (mean ± s.d.; _n_ = 8). D, LUC reporter rhythms (mean ± s.e.m.), time to the circadian peak (mean ± s.d.) and period estimates

(mean ± s.d.) in seedlings grown in continuous darkness for 72 h then transferred to continuous light or continuous low light (_n_ = 4). E, _CCA1:LUC_ rhythms (mean ± s.e.m.) and time to the

circadian peak in seedlings following transfer to continuous light or continuous low light in control media, medium containing DCMU, or medium containing DCMU and sucrose after 72 h in

continuous dark (_n_ = 4). * _P_ < 0.05; *** _P_ < 0.001 by two-tailed Student’s _t_-test. _n_ refers to number of biological replicates. EXTENDED DATA FIGURE 9 REGULATION OF THE

CIRCADIAN CLOCK BY SUGAR REQUIRES PRR7. A, Change in _PRR7:LUC_ luminescence after 3 h treatment with sucrose relative to untreated plants (mean ± s.d.; _n_ = 4). The data were normalized

across the time series, and the change relative to untreated plants was plotted. B, Change in _CCA1:LUC_ luminescence in wild-type plants and _prr7-11_ mutants after 3 h treatment with

sucrose relative to untreated plants (mean ± s.d.; _n_ = 8). The data were normalized across the time series, and the change relative to untreated plants of the appropriate genotype was

plotted. C, Period estimates of rhythms of delayed fluorescence in wild-type and mutant seedlings in continuous low light in media with or without exogenous sucrose (mean ± s.d.; _n_ = 4).

D, Phase response of _CCA1:LUC_ to pulses of sucrose in _prr7-11_ seedlings in continuous low light (mean ± s.d.; _n_ = 8). Compare this with the sucrose PRC for _CCA1:LUC_ in wild-type

seedlings in Fig. 2c. * _P_ < 0.05; ** _P_ < 0.01; *** _P_ < 0.001 by Student’s two-tailed _t_-test compared with controls in A and C and compared with wild-type plants in B. _n_

refers to number of biological replicates. EXTENDED DATA FIGURE 10 EFFECT OF EXOGENOUS SUCROSE ON CIRCADIAN PERIOD IN CIRCADIAN, SUGAR-INSENSITIVE AND LIGHT-SIGNALLING MUTANTS. LUC reporter

rhythms in circadian, sugar-insensitive and light-signalling mutants in continuous low light in media with or without exogenous sucrose (mean ± s.e.m.; _n_ = 4). The reporter is _CCA1:LUC_

in all lines except for Ws, _cca1-11_ (_CAB2:LUC_) and _toc1-21_ (_CCR2:LUC_). Period estimates are shown in blue (control) and red (sucrose) for each line (mean ± s.d.; _n_ = 8). _n_ refers

to number of biological replicates. POWERPOINT SLIDES POWERPOINT SLIDE FOR FIG. 1 POWERPOINT SLIDE FOR FIG. 2 POWERPOINT SLIDE FOR FIG. 3 POWERPOINT SLIDE FOR FIG. 4 RIGHTS AND PERMISSIONS

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