Abstract
BackgroundSensing 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.ResultsUsing 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.ConclusionsOur 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.
Highlights
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
Preliminary experiments showed that RNA turnover was faster at 27°C compared to 12°C (Figure S2b in Additional file 1), suggesting that temperature generally affected transcription rates
Because we can clearly show that regulation of transcription but not decay rates is central to the ambient temperature regulation of gene expression, we explored the possibility that key transcription factors or epigenetic states play a role in this process
Summary
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. The remaining genes either have rates buffered against changing temperatures, or passive increases in transcription rate must be offset by a balanced increase in decay rate, leading to higher turnover but static steady state levels. Despite this fundamental uncertainty, steady state transcriptomic responses to ambient temperature have been used to infer a role for chromatin modifications in temperature signaling [2,7]. We show that ambient temperature has large passive effects on both mRNA synthesis and decay rates, and that where temperature controls transcript abundance it does so by regulating transcription relative to decay and not vice versa. Our analysis suggests that transcription factor binding sites and epigenetic state combine to create a complex network of temperature responses in plants
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