Short Poly(A) Tails are a Conserved Feature of Highly Expressed Genes

Poly(A) tails are important elements in mRNA translation and stability. However, recent genome-wide studies concluded that poly(A) tail length was generally not associated with translational efficiency in non-embryonic cells. To investigate if poly(A) tail size might be coupled to gene expression in an intact organism, we used an adapted TAIL-seq protocol to measure poly(A) tails in Caenorhabditis elegans. Surprisingly, we found that well-expressed transcripts contain relatively short, well-defined tails. This attribute appears dependent on translational efficiency, as transcripts enriched for optimal codons and ribosome association had the shortest tail sizes, while non-coding RNAs retained long tails. Across eukaryotes, short tails were a feature of abundant and well-translated mRNAs. Although this seems to contradict the dogma that deadenylation induces translational inhibition and mRNA decay, it instead suggests that well-expressed mRNAs accumulate with pruned tails that accommodate a minimal number of poly(A) binding proteins, which may be ideal for protective and translational functions.