Codon Usage and Splicing Jointly Influence mRNA Localization

Cell Syst. 2020 Apr 22;10(4):351-362.e8. doi: 10.1016/j.cels.2020.03.001. Epub 2020 Apr 9.

Abstract

In the human genome, most genes undergo splicing, and patterns of codon usage are splicing dependent: guanine and cytosine (GC) content is the highest within single-exon genes and within first exons of multi-exon genes. However, the effects of codon usage on gene expression are typically characterized in unspliced model genes. Here, we measured the effects of splicing on expression in a panel of synonymous reporter genes that varied in nucleotide composition. We found that high GC content increased protein yield, mRNA yield, cytoplasmic mRNA localization, and translation of unspliced reporters. Splicing did not affect the expression of GC-rich variants. However, splicing promoted the expression of AT-rich variants by increasing their steady-state protein and mRNA levels, in part through promoting cytoplasmic localization of mRNA. We propose that splicing promotes the nuclear export of AU-rich mRNAs and that codon- and splicing-dependent effects on expression are under evolutionary pressure in the human genome.

Keywords: codon usage; evolution; mRNA export; saturation mutagenesis; splicing; synthetic biology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus / genetics
  • Alternative Splicing / genetics
  • Alternative Splicing / physiology
  • Base Composition / genetics
  • Codon / genetics
  • Codon Usage / genetics*
  • Exons / genetics
  • Gene Expression / genetics
  • Genome, Human / genetics
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • RNA Splicing / genetics
  • RNA Transport / genetics*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism*

Substances

  • Codon
  • RNA, Messenger