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Time of day prioritizes the pool of translating mRNAs in response to heat stress

ABSTRACT: The circadian clock helps organisms to anticipate and coordinate gene regulatory responses to changes in environmental stimuli. Under growth limiting temperatures, time of day modulates the accumulation of polyadenylated mRNAs. In response to heat stress, plants will conserve energy and selectively translate mRNAs. How the clock and/or time of day regulates polyadenylated mRNAs bound by ribosomes in response to heat stress is unknown. In-depth analysis of Arabidopsis thaliana translating mRNAs found that time of day gates the response of approximately one-third of the circadian regulated heat responsive translatome. Specifically, time of day and heat stress interact to prioritize the pool of mRNAs in cue to be translated. For a subset of mRNAs, we observed a stronger gated response during the day, and preferentially before the peak of expression. We propose previously overlooked transcription factors (TFs) as regulatory nodes and show that the clock plays a role in the temperature response for select TFs. When the stress was removed, the redefined priorities for translation recovered within one-hour, though slower recovery was observed for abiotic stress regulators. Through hierarchical network connections between clock genes and prioritized TFs, our work provides a framework to target key nodes underlying heat stress tolerance throughout the day.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE158444 | GEO | 2021/04/21

REPOSITORIES: GEO

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Project description:Purpose: To understand time of day variation in Arabidopsis heat shock responses. We have observed significant differences in terms of plant survivability in response to a heat shock across various times of day. Because of this, we believe that transcriptional responses may be a significant underlying factor which contributes to the observed physiology and surivability after heat stress. Methods: Whole plant tissue mRNA profiles in Col-0 Arabidopsis were generated by deep sequencing using Illumina HiSeq 2500. Tissue samples of four replicates were collected at two times of day (Dawn and Dusk, ZT0/ZT12) and were either control or heat stressed (30oC) for 1 hour. An additional 4 samples were collected in constant light conditions (single replicate) to quantify circadian effects. Sequence reads from each sample were mapped to the TAIR10 reference genome with Tophat2 and counts were obtained using Htseq-count. Differential expression analysis was done using DeSeq2 to calculate differential expression levels of each gene in the dataset. Results: We identified 5512 differentially expressed transcripts with our DESeq2 based data analysis pipeline that involves characterizing gene expression profiles based on basal expression level, time of differential expression, and direction of differential expression. An additional interaction term analysis revealed 572 genes which showe time of day dependent responses to heat stress, meaning the response to heat stress differs depending on the time of day that the heat stress is perceived by the plant. Downstream analysis using gene ontology analysis tools (Pantherdb.org) and Cytoscape revealed strong differences in terms of response happening in the AM and PM gene expression networks. The significance of this work is that it is the first study to show that there is a significant difference in terms of transcriptional responses to heat stress in Arabidopsis where the differences were quantified by levels of mRNA expression.

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Time of day prioritizes the pool of translating mRNAs in response to heat stress

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