RNA Polyadenylation in Prokaryotes and Organelles; Different Tails Tell Different Tales

Abstract

The addition of poly(A) tails to RNA is a phenomenon common to almost all organisms examined as of today. In eukaryotes, a stable poly(A) tail is added to the 3′ end of most nuclear-encoded mRNAs. This process is important for mRNA stability and translation initiation. In addition, polyadenylation of nuclear-encoded transcripts in yeast was recently reported to promote RNA degradation. In prokaryotes and organelles, RNA molecules are polyadenylated as part of a polyadenylation-dependent RNA degradation mechanism. This process consists sequentially of endonucleolytic cleavage, addition of degradation-inducing poly(A)-rich sequences to these cleavage products, and exonucleolytic degradation. In spinach chloroplasts the latter two steps, polyadenylation and exonucleolytic degradation, are performed by a single phosphorolytic and processive enzyme, polynucleotide phosphorylase (PNPase), while there is no equivalent to the E. coli poly(A)-polymerase enzyme. This was also found to be the case in cyanobacteria, a prokaryote believed to be related to the evolutionary ancestor of the chloroplast, and also in several other bacteria. No RNA polyadenylation was detected in the halophilic archaea Haloferax volcanii, which lacks the exosome complex, or in yeast mitochondria, which lack PNPase. Unlike other organelles, mammalian mitochondrial transcripts are known to include stable poly(A) tails at their 3′ ends, much like the case of nuclear-encoded mRNA. However, recent data have revealed that in addition to full-length, stably polyadenylated transcripts, nonabundant, truncated, polyadenylated RNA fragments are present in human mitochondria. These results suggest that the polyadenylation-dependent RNA degradation pathway is present in human mitochondria together with the addition of stable poly(A) tails at the mature 3′ end. We describe a possible scenario illustrating the evolution of RNA polyadenylation and its related functions found in bacteria, archaea, organelles, and eukaryotes.