The TRAMP complex shows tRNA editing activity in S. cerevisiae.

Transfer RNA (tRNA) editing is a widespread processing phenomenon that alters the sequence of primary transcripts by base substitutions as well as nucleotide deletions and insertions at internal or terminal transcript positions. In the corresponding tRNAs, these events are an important prerequisite for the generation of functional transcripts. Although many editing events are well characterized at the reaction level, it is unclear in most cases from which ancestral activities the modern editing enzymes evolved. Here, we show that in Saccharomyces cerevisiae, the noncanonical poly(A) polymerase Trf4p in the TRAMP complex can be recruited for such an editing reaction at an introduced tRNA transcript. As a distributive polymerase involved in RNA surveillance and quality control, it has a broad substrate spectrum and binds only transiently to the transcripts, limiting the number of added nucleotides at the editing position. These features exactly meet the criteria for an ancestral enzyme of a modern editing activity. Accordingly, our observations are a strong experimental support for the hypothesis that enzymatic promiscuity serves as an evolutionary starting point for the emergence of new functions and activities.