MCB Accepts, published online ahead of print on 26 October 2009

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Mol. Cell. Biol. doi:10.1128/MCB.00651-09
Copyright (c) 2009, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved.

Tom20 mediates localization of mRNAs to mitochondria in a translation-dependent manner

Erez Eliyahu, Lilach Pnueli, Daniel Melamed, Tanja Scherrer, André P. Gerber, Ophry Pines, Doron Rapaport, and Yoav Arava^*

Department of Biology, Technion – Israel Institute of Technology, Haifa 32000, Israel; Department of Chemistry and Applied Biosciences, ETH Zurich, Switzerland; Department of Molecular Biology, The Hebrew University, Jerusalem 91120, Israel; Interfaculty Institute for Biochemistry, University of Tuebingen, 72076 Tuebingen, Germany

^* To whom correspondence should be addressed. Email: arava{at}tx.technion.ac.il.

mRNAs encoding mitochondrial proteins are enriched in the vicinity of mitochondria, presumably to facilitate protein transport. A possible mechanism for enrichment may involve interaction of the translocase of the mitochondrial outer membrane (TOM) complex with the precursor protein while it is translated, thereby leading to association of polysomal mRNAs with mitochondria. To test this hypothesis, we isolated mitochondrial fractions from yeast cells lacking the major import receptor, Tom20 and compared their mRNA repertoire to that of wild type cells by DNA microarrays. Most mRNAs encoding mitochondrial proteins were less associated with mitochondria, yet the extent of decrease varied among genes. Analysis of several mRNAs revealed that optimal association of Tom20-targets necessitates translating ribosomes and features within the encoded mitochondrial targeting signal. Recently, Puf3p was implicated in mRNAs' mitochondrial association through interaction with untranslated regions. We therefore constructed a tom20 puf3 double knockout strain, which demonstrated growth defects under conditions where fully functional mitochondria are required. Mislocalization effects for few tested mRNAs appeared stronger in the double knockout than in tom20. Taken together, our data reveals a large-scale mRNA association mode that involves interaction of Tom20p with the translated mitochondrial targeting sequence and may be assisted by Puf3p.