Abstract
tRNase Z is an essential endonuclease responsible for tRNA 3'-end maturation. tRNase Z exists in a short form (tRNase Z(S)) and a long form (tRNase Z(L)). Prokaryotes have only tRNase Z(S), whereas eukaryotes can have both forms of tRNase Z. Most eukaryotes characterized thus far, including Saccharomyces cerevisiae, Caenorhabditis elegans, Drosophila melanogaster, and humans, contain only one tRNase Z(L) gene encoding both nuclear and mitochondrial forms of tRNase Z(L). In contrast, Schizosaccharomyces pombe contains two essential tRNase Z(L) genes (trz1 and trz2) encoding two tRNase Z(L) proteins, which are targeted to the nucleus and mitochondria, respectively. Trz1 protein levels are notably higher than Trz2 protein levels. Here, using temperature-sensitive mutants of trz1 and trz2, we provide in vivo evidence that trz1 and trz2 are involved in nuclear and mitochondrial tRNA 3'-end processing, respectively. In addition, trz2 is also involved in generation of the 5'-ends of other mitochondrial RNAs, whose 5'-ends coincide with the 3'-end of tRNA. Thus, our results provide a rare example showing partitioning of the nuclear and mitochondrial tRNase Z(L) activities between two different proteins in S. pombe. The evolution of two tRNase Z(L) genes and their differential expression in fission yeast may avoid toxic off-target effects.
Highlights
Most eukaryotes contain only one tRNase Z gene involved in both nuclear and organellar tRNA 3Ј-end maturation
We found that, at the nonpermissive temperature, wild-type cells accumulated a weak band correincreased by 18 –20-fold. These results suggest that trz2 is involved in the maturation of the 5Ј-ends of mitochondrial mRNAs and noncoding RNAs except tRNAs, supporting the tRNA punctuation model for RNA processing in S. pombe mitochondria
Previous studies from our laboratory have shown that S. pombe contains two tRNase ZLs, one located in the nucleus and the other in the mitochondria [38, 39]
Summary
Most eukaryotes contain only one tRNase Z gene involved in both nuclear and organellar tRNA 3Ј-end maturation. Different eukaryotic organisms can have different numbers and forms of tRNase Z with different subcellular localizations, it has been suggested that a single tRNase ZL is responsible for the 3Ј-end processing of both nuclear and mitochondrial pre-tRNAs [27, 28, 35]. TRNase ZLs from some species, including S. cerevisiae [37], S. pombe [38], and A. thaliana [34], have been shown to possess tRNA 3Ј-end processing activity in vitro, their nuclear and mitochondrial tRNA 3Ј-end processing activity in vivo remains to be experimentally demonstrated. We have previously demonstrated that the two S. pombe tRNase ZLs (Trz and Trz2) are localized to the nucleus and mitochondria, respectively, and can endonucleolytically remove the 3Ј-extension from a human nuclear pre-tRNA in vitro [38]. We show that Trz plays a crucial role in 5Ј-end maturation of other types of RNAs in mitochondria
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