Dynamic regulation of genome-wide pre-mRNA splicing and stress tolerance by the Sm-like protein LSm5 in Arabidopsis

TLDR

Sm‑like proteins, core components of the U6 snRNP, are conserved across eukaryotes and participate in pre‑mRNA splicing, yet their specific regulatory roles in splicing remain largely unexplored. Loss of the Arabidopsis Sm‑like protein LSm5 (SAD1) increases genome‑wide alternative splicing, whereas its overexpression enhances splice‑site precision, suppresses alternative splicing, and improves salt tolerance by modulating stress‑responsive transcripts.

Abstract

Abstract Background Sm-like proteins are highly conserved proteins that form the core of the U6 ribonucleoprotein and function in several mRNA metabolism processes, including pre-mRNA splicing. Despite their wide occurrence in all eukaryotes, little is known about the roles of Sm-like proteins in the regulation of splicing. Results Here, through comprehensive transcriptome analyses, we demonstrate that depletion of the Arabidopsis supersensitive to abscisic acid and drought 1 gene ( SAD1 ), which encodes Sm-like protein 5 (LSm5), promotes an inaccurate selection of splice sites that leads to a genome-wide increase in alternative splicing. In contrast, overexpression of SAD1 strengthens the precision of splice-site recognition and globally inhibits alternative splicing. Further, SAD1 modulates the splicing of stress-responsive genes, particularly under salt-stress conditions. Finally, we find that overexpression of SAD1 in Arabidopsis improves salt tolerance in transgenic plants, which correlates with an increase in splicing accuracy and efficiency for stress-responsive genes. Conclusions We conclude that SAD1 dynamically controls splicing efficiency and splice-site recognition in Arabidopsis , and propose that this may contribute to SAD1 -mediated stress tolerance through the metabolism of transcripts expressed from stress-responsive genes. Our study not only provides novel insights into the function of Sm-like proteins in splicing, but also uncovers new means to improve splicing efficiency and to enhance stress tolerance in a higher eukaryote.