The Plant Circadian Clock: From a Simple Timekeeper to a Complex Developmental Manager

Abstract

The plant circadian clock allows organisms to anticipate the predictable changes in the environment by adjusting their developmental and physiological traits. In the last few years, it was determined that responses known to be regulated by the oscillator are also able to modulate clock performance. These feedback loops and their multilayer communications create a complex web, and confer on the clock network a role that exceeds the measurement of time. In this article, we discuss the current knowledge of the wiring of the clock, including the interplay with metabolism, hormone, and stress pathways in the model species Arabidopsis thaliana We outline the importance of this system in crop agricultural traits, highlighting the identification of natural alleles that alter the pace of the timekeeper. We report evidence supporting the understanding of the circadian clock as a master regulator of plant life, and we hypothesize on its relevant role in the adaptability to the environment and the impact on the fitness of most organisms.

Figure 1.

Minimal architecture underlying the circadian clock of Arabidopsis thaliana. In this simplified model, only a subset of the pieces of the trascriptional–translational feedback loops is shown. The clockwork components are represented from left to right according to the time-of-day of their peak expression. White and gray background depict day and night, respectively. CCA1 and LHY are expressed in the morning and repress the expression of all clock components represented here. The “evening complex” (EC) is formed by LUX, ELF3, and ELF4, and induces CCA1/LHY. PRRs are repressed by TOC1, and PRR9 is also negatively regulated by the EC. TOC1 represses GI, which in turn induces CCA1/LHY by an unknown mechanism. All members of the PRR family are known to negatively regulate CCA1/LHY. Rectangles denote “functional groups,” either because the components are members of the same gene family (CCA/LHY and PRR9/PRR7/PRR5) or they act as a complex (EC). Despite PRR9, PRR7, and PRR5 being homologs of TOC1 (PRR1), the latter seems to have a different role in the oscillator. Arrowheads and perpendicular lines illustrate induction and repression of transcriptional activity, respectively. For references and a complete description, please refer to the main text.

Figure 2.

Interlocked communication between the central clock and different plant pathways. (A) The central clock modulates carbohydrate metabolism, nitrogen, calcium, iron, and copper homeostasis. In turn, all metabolic processes involving these nutrients feed back to the core oscillator. (B) The central clock modulates the hormone pathways illustrated in the figure: ABA, abscisic acid auxin; BRs, brassinosteroids; CK, cytokinin; ethylene; GA, gibberellin; JAs, jasmonates; SA, salicylic acid. All of these hormones with the exception of ethylene, GA, and JA contribute to the fine-tuning of the timekeeper. The outer arrows and circle reflect the clock independent interaction of these plant pathways, adding further complexity to the system as a whole.

Figure 3.

Schematic model of the circadian clock as the master regulator of plant life. The toroid represents all of the possible combinations of environmental parameters a plant can encounter through its life cycle. It comprises seasonal and diel changes of temperature and light, heat or cold stresses, water and mineral availability, and the presence of pathogens or herbivores, among others. Each slice of the toroid is therefore one particular combination of these external cues. For example, the bottom-right circle illustrates one hypothetical scenario. The different ellipses represent specific plant processes that interact with each other, converging in the center to feed the clock with exogenous and endogenous information, contributing to its synchronization. The central oscillator “interprets and translates” that information to determine an integrative and balanced response, which is then transmitted to the “outputs.” The interaction between the core clock and the outputs establishes the plant phenotype, represented in the figure by the edge of the circle. The two smaller circles depict other environmental interactions and scenarios. As the “input” cues differ in each example, the outcome is also different. In these examples, the change in the size of the ellipses represents that under certain conditions some physiological pathways are prevalent over others.