Evolution of +1 programmed frameshifting signals and frameshift-regulating tRNAs in the order Saccharomycetales

J Mol Evol. 2006 Oct;63(4):545-61. doi: 10.1007/s00239-005-0311-0. Epub 2006 Jul 12.

Abstract

Programmed translational frameshifting is a ubiquitous but rare mechanism of gene expression in which mRNA sequences cause the translational machinery to shift reading frames with extreme efficiency, up to at least 50%. The mRNA sequences responsible are deceptively simple; the sequence CUU-AGG-C causes about 40% frameshifting when inserted into an mRNA in the yeast Saccharomyces cerevisiae. The high efficiency of this site depends on a set of S. cerevisiae tRNA isoacceptors that perturb the mechanism of translation to cause the programmed translational error. The simplicity of the system might suggest that it could evolve frequently and perhaps be lost as easily. We have investigated the history of programmed +1 frameshifting in fungi. We find that frameshifting has persisted in two structural genes in budding yeasts, ABP140 and EST3 for about 150 million years. Further, the tRNAs that stimulate the event are equally old. Species that diverged from the lineage earlier both do not employ frameshifting and have a different complement of tRNAs predicted to be inimical to frameshifting. The stability of the coevolution of protein coding genes and tRNAs suggests that frameshifting has been selected for during the divergence of these species.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acid Sequence
  • Base Sequence
  • Eukaryotic Cells / metabolism
  • Evolution, Molecular*
  • Frameshifting, Ribosomal / genetics*
  • Genes, Fungal
  • Microfilament Proteins / chemistry
  • Microfilament Proteins / genetics
  • Phylogeny
  • Point Mutation / genetics
  • RNA, Transfer / genetics
  • RNA, Transfer / metabolism*
  • Saccharomyces cerevisiae Proteins / chemistry
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomycetales / genetics*
  • Sequence Alignment
  • Synteny
  • Telomerase

Substances

  • ABP140 protein, S cerevisiae
  • Microfilament Proteins
  • Saccharomyces cerevisiae Proteins
  • RNA, Transfer
  • EST3 protein, S cerevisiae
  • Telomerase