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Open Access Research

Direct measurement of transcription rates reveals multiple mechanisms for configuration of the Arabidopsis ambient temperature response

Kate Sidaway-Lee1, Maria J Costa2, David A Rand23, Bärbel Finkenstadt4 and Steven Penfield1*

Author Affiliations

1 Biosciences, College of Life and Environmental Sciences, University of Exeter, Geoffrey Pope Building, Stocker Road, Exeter EX4 4QD, UK

2 Systems Biology Centre, University of Warwick, Coventry CV4 7AL, UK

3 Mathematics Institute, University of Warwick, Coventry CV4 7AL, UK

4 Department of Statistics, University of Warwick, Coventry CV4 7AL, UK

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Genome Biology 2014, 15:R45  doi:10.1186/gb-2014-15-3-r45

Published: 3 March 2014

Abstract

Background

Sensing and responding to ambient temperature is important for controlling growth and development of many organisms, in part by regulating mRNA levels. mRNA abundance can change with temperature, but it is unclear whether this results from changes in transcription or decay rates, and whether passive or active temperature regulation is involved.

Results

Using a base analog labelling method, we directly measured the temperature coefficient, Q10, of mRNA synthesis and degradation rates of the Arabidopsis transcriptome. We show that for most genes, transcript levels are buffered against passive increases in transcription rates by balancing passive increases in the rate of decay. Strikingly, for temperature-responsive transcripts, increasing temperature raises transcript abundance primarily by promoting faster transcription relative to decay and not vice versa, suggesting a global transcriptional process exists that controls mRNA abundance by temperature. This is partly accounted for by gene body H2A.Z which is associated with low transcription rate Q10, but is also influenced by other marks and transcription factor activities.

Conclusions

Our data show that less frequent chromatin states can produce temperature responses simply by virtue of their rarity and the difference between their thermal properties and those of the most common states, and underline the advantages of directly measuring transcription rate changes in dynamic systems, rather than inferring rates from changes in mRNA abundance.