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 persistence to changing climate. The cellular response to heat shock, 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 shock can be quantitative (changing the magnitude of expression) or qualitative (differential usage of 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 shock at four post-stress timepoints (30 min, 1 h, 2 h, 24 h) in a splash pool 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. We observed that heat shock predominantly induced changes in gene expression in genes coding for chitin, HSPs, cellular growth, and differentiation. In contrast, we found that genes coding for peptidases showed both altered expression levels and exon usage. Genes associated with cellular metabolism and cytoskeletal elements primarily showed changes in exon usage. These ontology-specific response mechanisms provide new insights into the temporal landscape of HSR in Tigriopus and highlight the need to integrate qualitative and quantitative changes in gene expression to fully understand organismal responses to heat shock.