Multidimensional plasticity jointly contributes to rapid acclimation to environmental challenges during biological invasions

Rapid plastic response to environmental changes, which involves extremely complex underlying mechanisms, is crucial for organismal survival during many ecological and evolutionary processes such as those in global change and biological invasions. Gene expression is among the most studied molecular plasticity, while co- or post-transcriptional mechanisms are still largely unexplored. Using a model invasive ascidian Ciona savignyi, we studied multidimensional short-term plasticity in response to hyper- and hypo-salinity stresses, covering the physiological adjustment, gene expression, alternative splicing (AS), and alternative polyadenylation (APA) regulations. Our results demonstrated that rapid plastic response varied with environmental context, timescales, and molecular regulatory levels. Gene expression, AS, and APA regulations independently acted on different gene sets and corresponding biological functions, highlighting their non-redundant roles in rapid environmental adaptation. Stress-induced gene expression changes illustrated the use of a strategy of accumulating free amino acid under high salinity and losing/reducing them during low salinity to maintain the osmotic homoeostasis. Genes with more exons were inclined to use AS regulations, and isoform switches in functional genes such as SLC2a5 and Cyb5r3 resulted in enhanced transporting activities by upregulating the isoforms with more transmembrane regions. The extensive 3-untranslated region (3UTR) shortening through APA was induced by both salinity stresses, and APA regulation predominated transcriptomic changes at some stages of stress response. The findings here provide evidence for complex plastic mechanisms to environmental changes, and thereby highlight the importance of systemically integrating different levels of regulation mechanisms in studying initial plasticity in evolutionary trajectories.