Widespread use of poly(A) tail length control to accentuate expression of the yeast transcriptome

Abstract

Control of poly(A) tail length can affect translation and stability of eukaryotic mRNAs. Although well established for individual cases, it was not known to what extent this type of adjustable gene control is used to shape expression of eukaryotic transcriptomes. Here we report on microarray-based measurements of mRNA poly(A) tail lengths and association with the poly(A)-binding protein Pab1 in S. cerevisiae, revealing extensive correlation between tail length and other physical and functional mRNA characteristics. Gene ontology analyses and further directed experiments indicate coregulation of tail length on functionally and cytotopically related mRNAs to coordinate cell-cycle progression, ribosome biogenesis, and retrotransposon expression. We show that the 3′-untranslated region drives transcript-specific adenylation control and translational efficiency of multiple mRNAs. Our findings suggest a wide-spread interdependence between 3′-untranslated region-mediated poly(A) tail length control, Pab1 binding, and mRNA translation in budding yeast. They further provide a molecular explanation for deadenylase function in the cell cycle and suggest additional cellular processes that depend on control of mRNA polyadenylation.