Highly dynamic transcriptional reprogramming and shorter isoform shifts under acute stresses during biological invasions

Phenotypic plasticity has been increasingly recognized for its importance in adaptation to novel environments, and initial rapid plastic response to acute stresses usually serves as the stepping stone for future adaptation. Differential gene expression and alternative splicing have been proposed as two underlying mechanisms for rapid plastic response to environmental stresses. Here, we used an invasive model species,Ciona savignyi, to investigate the temporary plastic changes under temperature stresses on gene expression and alternative splicing. Our results revealed rapid and highly dynamic gene expression reprogramming and alternative splicing switch under acute stresses. Distinct transcriptional response profiles were triggered by two types of temperature stresses, showing resilience recovery and increasing divergence under heat and cold challenges, respectively. Interestingly, alternative exons were more inclined to be skipped under both heat and cold stresses, leading to shorter isoforms but with maintained Open Reading Frames (ORFs). Although similar response patterns were observed between differential gene expression and alternative splicing, low overlap between Differentially Expressed Genes (DEGs) and Differentially Alternative Spliced Genes (DASGs) suggests that distinct gene sets and associated functions should be involved in temperature challenges. Thus, alternative splicing should offer an additional layer of plastic response to environmental challenges. Finally, we identified key plastic genes involved in both gene expression regulation and alternative splicing. The results obtained here shed light on adaptation and accommodation mechanisms during biological invasions, particularly for acute environmental changes at early stages of biological invasions such as transport and introduction.

Automated summary

The study revealed rapid and dynamic gene expression reprogramming and alternative splicing switch in response to acute temperature stresses in Ciona savignyi. Different transcriptional response profiles were triggered by heat and cold challenges, showing resilience recovery and increasing divergence, respectively. Alternative exons were more likely to be skipped under both heat and cold stresses.