Complementary roles for differential gene expression and differential exon use in the heat shock response of an intertidal copepod

Understanding the mechanisms by which organisms adapt to variation in temperature is key to explaining their distribution across environments and to predicting their response to changing climate. The cellular response to heat stress, heat shock response (HSR), is a highly conserved mechanism for coping with elevated temperatures which functions through the upregulation of molecular chaperones like heat shock proteins (HSPs). Recent studies have also shown cellular response to heat stress can be quantitative (changing the magnitude of expression) or qualitative (expressing different exons originating from the same gene) . However, few studies have explored the time course of these two mechanisms in response to heat shock. We conducted a time-course experiment to examine the gene expression and exon usage changes in response to heat stress at four post-stress timepoints (30 minutes, 1 hour, 2 hours, 24 hours) in a splashpool copepod, Tigriopus californicus. We detected signatures of both gene expression and exon usage changes across all timepoints. The magnitude of this response was higher at timepoints closer to heat shock and decreased with time post-heat shock. Genes coding for heat shock proteins, cellular growth, and differentiation responded to heat stress predominantly through changing their expression levels, whereas genes coding for peptidases and chitin synthesis responded through changing expression levels and exon usage. Genes involved in cellular metabolism and cytoskeletal elements responded to heat shock primarily through changing exon usage. These ontology-specific response mechanisms provide new insights into temporal landscape of heat shock response in Tigriopus and highlight the need to integrate qualitative and quantitative changes in gene expression to fully understand the organismal response to heat stress.