Abstract
Circadian rhythms are daily biological oscillations driven by an endogenous mechanism known as circadian clock. The protein kinase CK2 is one of the few clock components that is evolutionary conserved among different taxonomic groups. CK2 regulates the stability and nuclear localization of essential clock proteins in mammals, fungi, and insects. Two CK2 regulatory subunits, CKB3 and CKB4, have been also linked with the Arabidopsis thaliana circadian system. However, the biological relevance and the precise mechanisms of CK2 function within the plant clockwork are not known. By using ChIP and Double–ChIP experiments together with in vivo luminescence assays at different temperatures, we were able to identify a temperature-dependent function for CK2 modulating circadian period length. Our study uncovers a previously unpredicted mechanism for CK2 antagonizing the key clock regulator CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1). CK2 activity does not alter protein accumulation or subcellular localization but interferes with CCA1 binding affinity to the promoters of the oscillator genes. High temperatures enhance the CCA1 binding activity, which is precisely counterbalanced by the CK2 opposing function. Altering this balance by over-expression, mutation, or pharmacological inhibition affects the temperature compensation profile, providing a mechanism by which plants regulate circadian period at changing temperatures. Therefore, our study establishes a new model demonstrating that two opposing and temperature-dependent activities (CCA1-CK2) are essential for clock temperature compensation in Arabidopsis.
Highlights
Circadian rhythms are daily biological oscillations driven by an endogenous mechanism known as circadian clock
This is a property known as clock temperature compensation, and despite its importance for circadian function, we know few details about the mechanisms responsible for the temperature-dependent regulation of circadian period length
We have identified that the activity of two key plant clock components (CK2 and CLOCK-ASSOCIATED 1 (CCA1)) is regulated by temperature
Summary
Circadian rhythms are daily biological oscillations driven by an endogenous mechanism known as circadian clock. The phase of the rhythms is synchronized by environmental cues, mostly changes in light and temperature, that occur during the 24-hour day/night cycle. Synchronization ensures adequate timing and allows the rhythmic activities to occur at the most appropriate phase relationships with the environment [1,2,3,4,5]. The reciprocal regulation among key clock genes and proteins sustains molecular oscillations that are translated into metabolic and behavioral rhythms [6,7,8]. Additional mechanisms involving chromatin remodeling [9,10] and post-translational regulation of clock components [11,12] contribute to circadian rhythmicity. Despite the conservation of clock mechanisms, the actual molecular components responsible for circadian function are not conserved among phylogenetic kingdoms. A remarkable exception is the protein kinase CK2 (formerly casein kinase 2) with an important function within the plant, fungi, insect and mammalian circadian systems [13]
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