Chemical Perturbation of Chloroplast-Related Processes Affects Circadian Rhythms of Gene Expression in Arabidopsis: Salicylic Acid Application Can Entrain the Clock

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.

Organelles and phytohormones: a network of interactions in plant stress responses

“…In addition, LHY overexpression represses the accumulation of ABA during drought. Perturbation of chloroplast-related functions by chemicals such as 3-(3,4-dichlorophenyl)-1,1-dimethylurea, paraquat, and ascorbate modifies the pace of nuclear-driven circadian oscillations ( Philippou et al , 2020 ), which led to the hypothesis that the circadian rhythm could act as an additional feedback mechanism from chloroplasts on ABA biosynthesis, due to connection of chloroplast functions and the circadian clock.…”

Chemical biology to dissect molecular mechanisms underlying plant circadian clocks

“…The inhibition of organelle activity and actin dynamics changes the circadian period in Arabidopsis (Toth et al ., 2012; Philippou et al ., 2020; Wang et al ., 2020; Table 2). Arabidopsis clock parameters are also influenced by oxidant, antioxidant and plant hormones (Hanano et al ., 2006; Zhang et al ., 2019; Gao et al ., 2020; Philippou et al ., 2020; see Table 2 for effect).…”

“…The modes of action of these molecules are diverse, but the inhibition of essential cellular processes such as transcription, translation, and protein degradation results in period lengthening(O'Neill et al, 2011;Ma et al, 2018;de Melo et al, 2021;Uehara et al, 2022; Table 2). The inhibition of organelle activity and actin dynamics changes the circadian period in Arabidopsis(Toth et al, 2012;Philippou et al, 2020;Wang et al, 2020; Table 2). Arabidopsis clock parameters are also influenced by oxidant, antioxidant and plant hormones(Hanano et al, 2006;Zhang et al, 2019;Gao et al, 2020;Philippou et al, 2020; see Table2for effect).Analyses using selective inhibitors reveal the specific enzymes that are involved in clock control (Table2).…”

“…The inhibition of organelle activity and actin dynamics changes the circadian period in Arabidopsis(Toth et al, 2012;Philippou et al, 2020;Wang et al, 2020; Table 2). Arabidopsis clock parameters are also influenced by oxidant, antioxidant and plant hormones(Hanano et al, 2006;Zhang et al, 2019;Gao et al, 2020;Philippou et al, 2020; see Table2for effect).Analyses using selective inhibitors reveal the specific enzymes that are involved in clock control (Table2). Inhibition of Casein Kinase 1 (CK1 in O. tauri and CKL in Arabidopsis), CK2, and Ca 2+ signalling lengthen periods in O. tauri and Arabidopsis…”

New Horizons in Plant Cell Signaling

“…Salicylic acid (SA), a phenolic plant hormone found in many plant species, functions as a critical signaling molecule in local and systemic disease resistance pathways [ 62 ]. Responding to a broad spectrum of pathogens and abiotic stresses, SA also crosstalks with many signaling pathways ranging from reactive oxygen species, lipids, and circadian clock to other hormones such as jasmonic acid and ethylene [ 63 , 64 , 65 , 66 , 67 ]. Plant defense signaling by SA is initiated when it binds to target proteins such as the nonexpresser of pathogenesis-related protein 1 (NPR1) which is a well-established transcriptional regulator of SA signaling [ 68 ].…”