Abstract
The plant circadian system reciprocally interacts with metabolic processes. To investigate entrainment features in metabolic–circadian interactions, we used a chemical approach to perturb metabolism and monitored the pace of nuclear-driven circadian oscillations. We found that chemicals that alter chloroplast-related functions modified the circadian rhythms. Both vitamin C and paraquat altered the circadian period in a light-quality-dependent manner, whereas rifampicin lengthened the circadian period under darkness. Salicylic acid (SA) increased oscillatory robustness and shortened the period. The latter was attenuated by sucrose addition and was also gated, taking place during the first 3 h of the subjective day. Furthermore, the effect of SA on period length was dependent on light quality and genotype. Period lengthening or shortening by these chemicals was correlated to their inferred impact on photosynthetic electron transport activity and the redox state of plastoquinone (PQ). Based on these data and on previous publications on circadian effects that alter the redox state of PQ, we propose that the photosynthetic electron transport and the redox state of PQ participate in circadian periodicity. Moreover, coupling between chloroplast-derived signals and nuclear oscillations, as observed in our chemical and genetic assays, produces traits that are predicted by previous models. SA signaling or a related process forms a rhythmic input loop to drive robust nuclear oscillations in the context predicted by the zeitnehmer model, which was previously developed for Neurospora. We further discuss the possibility that electron transport chains (ETCs) are part of this mechanism.
Highlights
Stress events often occur at predictable times of the day given the environmentally rhythmic cycling of light, temperature, and humidity
A chemical approach was used to investigate the potential crosstalk between translational oscillations (TTOs) and metabolism in Arabidopsis thaliana
Redox-related chemicals were exogenously applied on seedlings and the effect of the chemicals on circadian promoter activity was monitored with the luciferase system
Summary
Stress events often occur at predictable times of the day given the environmentally rhythmic cycling of light, temperature, and humidity Within these cycles, light causes the accumulation of reactive oxygen species (ROS) (Pitzschke et al, 2006), while pathogen invasion is often favored at a given time of day (Shin et al, 2012; Korneli et al, 2014; Karapetyan and Dong, 2018; Li et al, 2018; Zhang et al, 2019). Given the predictable, timed nature of these abiotic and biotic stressors, the plant circadian clock provides timed sensitivity resistance to such agents This 24-h oscillator serves to prime a plant to be most capable of resisting stress when it is most likely to be encountered (Covington et al, 2008; Sánchez et al, 2011; Fornara et al, 2015; Grundy et al, 2015). This network is in constant cross-talking with plant physiology and the environment (McClung, 2019)
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