Abstract

Correct daily phasing of transcription confers an adaptive advantage to almost all organisms, including higher plants. In this study, we describe a hypothesis-driven network discovery pipeline that identifies biologically relevant patterns in genome-scale data. To demonstrate its utility, we analyzed a comprehensive matrix of time courses interrogating the nuclear transcriptome of Arabidopsis thaliana plants grown under different thermocycles, photocycles, and circadian conditions. We show that 89% of Arabidopsis transcripts cycle in at least one condition and that most genes have peak expression at a particular time of day, which shifts depending on the environment. Thermocycles alone can drive at least half of all transcripts critical for synchronizing internal processes such as cell cycle and protein synthesis. We identified at least three distinct transcription modules controlling phase-specific expression, including a new midnight specific module, PBX/TBX/SBX. We validated the network discovery pipeline, as well as the midnight specific module, by demonstrating that the PBX element was sufficient to drive diurnal and circadian condition-dependent expression. Moreover, we show that the three transcription modules are conserved across Arabidopsis, poplar, and rice. These results confirm the complex interplay between thermocycles, photocycles, and the circadian clock on the daily transcription program, and provide a comprehensive view of the conserved genomic targets for a transcriptional network key to successful adaptation.

Highlights

  • The circadian clock functions to optimize physiology and metabolism to the correct time of the day and is crucial for fitness

  • Plants have adapted to these changes by timing physiological processes to specific times of the day or night

  • We discovered that almost all Arabidopsis genes cycle in at least one condition

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Summary

Introduction

The circadian clock functions to optimize physiology and metabolism to the correct time of the day and is crucial for fitness. Organisms experience the external environment as a dynamic relationship between daily changes in temperature (thermocycles) and light (photocycles) that vary by season and latitude (Figures S1 and S2). Environmental cycles and the circadian clock phase gene expression, metabolism, and physiology to the correct time of the day [4]. While much is known about how organisms sense light and integrate photocycles to synchronize the circadian clock, little is known of how ambient thermocycles are sensed and integrated. In Arabidopsis thaliana, thermocycles of 10 8C difference are dominant over photocycles for setting the phase of gene expression, consistent with the notion that multiple forms of the circadian oscillator may exist that have temperature- and light-specificity [7]. How and to what extent ambient thermocycles influence daily transcription remains unknown

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