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

RNA Biol. 2021 Mar;18(3):340-353. doi: 10.1080/15476286.2020.1805904. Epub 2020 Aug 17.

Abstract

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.

Keywords: Biological invasion; alternative splicing; environmental challenge; gene expression plasticity; invasive ascidians.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological / genetics
  • Alternative Splicing*
  • Animals
  • Ciona / genetics*
  • Environment
  • Exons
  • Gene Expression Regulation*
  • Gene Regulatory Networks
  • Gene-Environment Interaction
  • Introduced Species*
  • Open Reading Frames
  • Stress, Physiological / genetics*
  • Temperature
  • Transcription, Genetic*

Grants and funding

This work was supported by the National Natural Science Foundation of China under Grant number 31772449.