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Review
. 2023 Nov;116(3):650-668.
doi: 10.1111/tpj.16405. Epub 2023 Aug 2.

Circadian regulation of metabolism across photosynthetic organisms

Luíza Lane de Barros Dantas  1 , Bethany M Eldridge  1 , Jack Dorling  1 , Richard Dekeya  1 , Deirdre A Lynch  1 , Antony N Dodd  1
Affiliations
Review

Circadian regulation of metabolism across photosynthetic organisms

Luíza Lane de Barros Dantas et al. Plant J. 2023 Nov.

Abstract

Circadian regulation produces a biological measure of time within cells. The daily cycle in the availability of light for photosynthesis causes dramatic changes in biochemical processes in photosynthetic organisms, with the circadian clock having crucial roles in adaptation to these fluctuating conditions. Correct alignment between the circadian clock and environmental day-night cycles maximizes plant productivity through its regulation of metabolism. Therefore, the processes that integrate circadian regulation with metabolism are key to understanding how the circadian clock contributes to plant productivity. This forms an important part of exploiting knowledge of circadian regulation to enhance sustainable crop production. Here, we examine the roles of circadian regulation in metabolic processes in source and sink organ structures of Arabidopsis. We also evaluate possible roles for circadian regulation in root exudation processes that deposit carbon into the soil, and the nature of the rhythmic interactions between plants and their associated microbial communities. Finally, we examine shared and differing aspects of the circadian regulation of metabolism between Arabidopsis and other model photosynthetic organisms, and between circadian control of metabolism in photosynthetic and non-photosynthetic organisms. This synthesis identifies a variety of future research topics, including a focus on metabolic processes that underlie biotic interactions within ecosystems.

Keywords: Arabidopsis thaliana; Bacillus subtilis; Chlamydomonas reinhardtii; Ostreococcus tauri; Synechococcus elongatus PCC7942; circadian regulation; cyanobacteria; metabolism; rhizosphere; starch.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

Figure 1
Figure 1
Processes of circadian regulation. (a) Circadian rhythms are endogenous biological cycles that have a period of approximately 24 h under constant conditions. Under appropriate free‐running conditions, the rhythms persist in the absence of external cues such light or temperature. (b) The circadian oscillator of Arabidopsis is entrained to several environmental cues (known as zeitgebers) that align its phase with environmental fluctuations. The circadian oscillator produces an estimate of time, which is communicated to clock‐controlled processes through transcriptional and post‐transcriptional mechanisms. (c) A regulatory architecture underlying extensive circadian regulation of transcript abundance in the absence of equivalent extensive oscillations in protein abundance. Here, circadian oscillations of transcript accumulation permit oscillations of protein replacement, leading to proteostasis. (d) Circadian oscillations in the concentration of Mg2+ (Feeney et al., 2016) might lead to wide‐scale oscillations in ATP hydrolysis and translation rates, driving circadian rhythms of metabolism. (e) Circadian oscillations in the oxidation state of peroxiredoxin (PRX) (Edgar et al., 2012) might drive or be related to circadian rhythms of redox‐sensitive metabolism. In the hyperoxidized state, PRX has signaling and chaperone functions, and these oscillations might occur independently or semi‐independently from the transcription‐translation feedback loops (Edgar et al., 2012). In (c–e), the gray circular icon indicates points of circadian control.
Figure 2
Figure 2
Potential involvement of the circadian oscillator in rhythmic root exudation and rhizosphere interactions. (a) Circadian‐regulated rhythmicity in root metabolite biosynthesis and transport might directly or indirectly affect root exudation processes at the transcriptional, translational, and post‐translational scales. (b) The circadian oscillator is likely to contribute to diel fluctuations in root metabolite release into the rhizosphere. (c) Rhythmic changes in root exudation might affect microbial community composition, which could drive rhythmic metabolic feedback, shaping rhizosphere structure and function.
Figure 3
Figure 3
The circadian oscillator impacts metabolism across photosynthetic organisms. The diagram summarizes the times at which key metabolic processes occur in representative models for the investigation of circadian regulation in photosynthetic organisms. The diagram also indicates areas of similarity and differences between each group of organisms.
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References

    1. Abraham, P.E. , Yin, H. , Borland, A.M. , Weighill, D. , Lim, S.D. , De Paoli, H.C. et al. (2016) Transcript, protein and metabolite temporal dynamics in the CAM plant Agave . Nature Plants, 2, 16178. - PubMed
    1. Alabadí, D. , Oyama, T. , Yanovsky, M.J. , Harmon, F.G. , Más, P. & Kay, S.A. (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science, 293, 880–883. - PubMed
    1. Allard‐Massicotte, R. , Tessier, L. , Lécuyer, F. , Lakshmanan, V. , Lucier, J.‐F. , Garneau, D. et al. (2016) Bacillus subtilis early colonization of Arabidopsis thaliana roots involves multiple chemotaxis receptors. mBio, 7, e01664‐16. - PMC - PubMed
    1. Annunziata, M.G. , Apelt, F. , Carillo, P. , Krause, U. , Feil, R. , Koehl, K. et al. (2018) Response of Arabidopsis primary metabolism and circadian clock to low night temperature in a natural light environment. Journal of Experimental Botany, 69, 4881–4895. - PMC - PubMed
    1. Ansong, C. , Sadler, N.C. , Hill, E.A. , Lewis, M.P. , Zink, E.M. , Smith, R.D. et al. (2014) Characterization of protein redox dynamics induced during light‐to‐dark transitions and nutrient limitation in cyanobacteria. Frontiers in Microbiology, 5, 325. - PMC - PubMed

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