The circadian clock coordinates plant development through specificity at the tissue and cellular level
Introduction
Many organisms have evolved a genetic circuit, known as the circadian clock, in order to coordinate processes over the day-night cycle. The clock uses environmental signals, such as light and temperature, to set, or entrain, the clock to the environment. An organism can then use the clock to time key processes to the appropriate time of day. In plants, the clock is particularly influential and regulates not only daily events but also important developmental transitions during the life cycle of the plant, including when to flower. The advantage gained from the clock’s diurnal and seasonal timing is large; plants with a functional clock matching the day–night cycle fix more carbon and grow faster than those without [1,2].
Much effort has gone into building a molecular understanding of the clock, with a combination of mathematical modeling and experiment revealing a multiple feedback-loop network that generates a 24 hour oscillation in gene regulation [3,4]. Steadily, the number of processes known to be modulated by the clock has increased, as well as the number of signals that can entrain the clock [5,6]. Differences in clock period and phase have also been measured across the plant [7], which is perhaps unsurprising given that different parts of the plant are in very different environments.
This review will focus on recent research that has revealed how the clock can regulate plant physiology at multiple scales during development (Figure 1a). To do this, it appears clocks in different parts of the plant are sensitive to different environmental cues, run at different speeds, and regulate different outputs (Figure 1b). We do not provide a comprehensive review of the mechanism of the circadian clock, but instead use recent advances to explain how the clock can function as a developmental coordinator.
Section snippets
The circadian clock regulates at multiple scales during plant development
At the level of single cells, the clock can directly modulate cell division in plants in order to time division to a particular time of day. In developing Arabidopsis leaves, TIMING OF CAB EXPRESSION 1 (TOC1), a core protein of the clock network, binds to the promoter of the cell cycle gene CELL DIVISION CONTROL 6 (CDC6), repressing its expression [8••]. CDC6 promotes progression from the Gap 1 (G1) to the DNA Synthesis (S) stage of the cell cycle by licensing DNA for replication. Hence, when
Clocks in individual cells are sensitive to different environmental inputs and display different circadian phases and periods
As well as regulating multiple developmental processes, the plant clock’s period and phase are sensitive to a wide range of exogenous and endogenous signals. These include light, temperature, calcium [36], osmotic stress [37], humidity [38], and metabolic sugars [39,40]. It is these adjustments to phase, and likely also period [41,42] that match the clock to environmental cycles. At first it may seem unnecessary for the clock to be sensitive to such a range of cues, given that in the laboratory
Clocks in individual tissues regulate distinct developmental outputs
In addition to entraining to different environments, individual clocks must regulate a large number of different outputs. Previous work has revealed that the clock can regulate distinct sets of targets in different tissues to bring about appropriate changes in physiology. By isolating the individual tissues of the cotyledon enzymatically, it was shown that the clock in the vasculature oscillates with an earlier phase and greater robustness than the mesophyll clock (Figure 3a) [59,61••]. The
The coordination of the plant circadian clock
As discussed, rhythms across the plant have been shown to exhibit different phases and periods. This raises the question, are plants rhythms coordinated between cells and tissues at all? For many developmental processes, cells and tissues must act in a coordinated way. It is therefore likely that individual oscillations coordinate in order to time development. Whether and how clocks coordinate across the plant has thus been an active area of research in circadian biology.
Cell-to-cell
Conclusions and perspectives
As discussed, it is becoming increasingly clear that the clock both regulates and is regulated at multiple scales in plants. To further understand the role of the clock in coordinating development, it will be important to examine the clock at the appropriate scale. For example, by tracking TOC1 expression in individual cells during division, it will be possible to quantify the coupling between the clock and cell division, as has been done in other organisms [10,11,13]. Also, most molecular work
Conflict of interest statement
Nothing declared.
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
This work was supported by the Gatsby Charitable Foundation [grant number GAT3395/GLC]. We thank Dr Katie Abley and Dr Bruno Martins (University of Cambridge) for critical reading of the manuscript. We also thank contributors to the Plant Illustrations Repository [79] for graphics utilised in the figures.
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