Long mRNAs coding for yeast mitochondrial proteins of prokaryotic origin preferentially localize to the vicinity of mitochondria

Abstract

BACKGROUND: Subcellular messenger RNA localization is important in most eukaryotic cells, even in unicellular organisms like yeast for which this process has been underestimated. Microarrays are rarely used to study subcellular mRNA localization at whole-genome level, but can be adapted to that purpose. This work focuses on studying the repartition of yeast nuclear transcripts encoding mitochondrial proteins between free cytosolic polysomes and polysomes bound to the mitochondrial outer membrane. RESULTS: Combining biochemical fractionations with oligonucleotide array analyses permits clustering of genes on the basis of the subcellular sites of their mRNA translation. A large fraction of yeast nuclear transcripts known to encode mitochondrial proteins is found in mitochondrial outer-membrane-bound fractions. These results confirm and extend a previous analysis conducted with partial genomic microarrays. Interesting statistical relations among mRNA localization, gene origin and mRNA lengths were found: longer and older mRNAs are more prone to be localized to the vicinity of mitochondria. These observations are included in a refined model of mitochondrial protein import. CONCLUSIONS: Mitochondrial biogenesis requires concerted expression of the many genes whose products make up the organelle. In the absence of any clear transcriptional program, coordinated mRNA localization could be an important element of the time-course of organelle construction. We have built a 'MitoChip' localization database from our results which allows us to identify interesting genes whose mRNA localization might be essential for mitochondrial biogenesis in most eukaryotic cells. Moreover, many components of the experimental and data-analysis strategy implemented here are of general relevance in global transcription studies.