Polynucleotide phosphorylase and the archaeal exosome as poly(A)-polymerases.
The addition of poly(A)-tails to RNA is a phenomenon common to almost all organisms. Not only homopolymeric poly(A)-tails, comprised exclusively of adenosines, but also heteropolymeric poly(A)-rich extensions, which include the other three nucleotides as well, have been observed in bacteria, archaea, chloroplasts, and human cells. Polynucleotide phosphorylase (PNPase) and the archaeal exosome, which bear strong similarities to one another, both functionally and structurally, were found to polymerize the heteropolymeric tails in bacteria, spinach chloroplasts, and archaea. As phosphorylases, these enzymes use diphosphate nucleotides as substrates and can reversibly polymerize or degrade RNA, depending on the relative concentrations of nucleotides and inorganic phosphate. A possible scenario, illustrating the evolution of RNA polyadenylation and its related functions, is presented, in which PNPase (or the archaeal exosome) was the first polyadenylating enzyme to evolve and the heteropolymeric tails that it produced, functioned in a polyadenylation-stimulated RNA degradation pathway. Only at a later stage in evolution, did the poly(A)-polymerases that use only ATP as a substrate, hence producing homopolymeric adenosine extensions, arise. Following the appearance of homopolymeric tails, a new role for polyadenylation evolved; RNA stability. This was accomplished by utilizing stable poly(A)-tails associated with the mature 3' ends of transcripts. Today, stable polyadenylation coexists with unstable heteropolymeric and homopolymeric tails. Therefore, the heteropolymeric poly(A)-rich tails, observed in bacteria, organelles, archaea, and human cells, represent an ancestral stage in the evolution of polyadenylation.
Slomovic
Shimyn
S
Department of Biology, Technion - Israel Institute of Technology, Haifa, Israel.
Portnoy
Victoria
V
Yehudai-Resheff
Shlomit
S
Bronshtein
Ela
E
Schuster
Gadi
G
D000818:Animals; D001105:Archaea / Q000201:enzymology / Q000235:genetics; D001419:Bacteria / Q000201:enzymology / Q000235:genetics; D002736:Chloroplasts / Q000201:enzymology / Q000235:genetics; D019143:Evolution, Molecular; D006801:Humans; D011061:Poly A / Q000235:genetics / Q000378:metabolism*; D011062:Polynucleotide Adenylyltransferase / Q000235:genetics / Q000378:metabolism*; D011117:Polyribonucleotide Nucleotidyltransferase / Q000235:genetics / Q000378:metabolism*; D018724:Spinacia oleracea / Q000201:enzymology / Q000235:genetics; D040681:Structural Homology, Protein
D011061:Poly A; D011062:Polynucleotide Adenylyltransferase; D011117:Polyribonucleotide Nucleotidyltransferase