Abstract
BackgroundPolyadenylation of RNA has a decisive influence on RNA stability. Depending on the organisms or subcellular compartment, it either enhances transcript stability or targets RNAs for degradation. In plant mitochondria, polyadenylation promotes RNA degradation, and polyadenylated mitochondrial transcripts are therefore widely considered to be rare and unstable. We followed up a surprising observation that a large number of mitochondrial transcripts are detectable in microarray experiments that used poly(A)-specific RNA probes, and that these transcript levels are significantly enhanced after heat treatment.Methodology/Principal FindingsAs the Columbia genome contains a complete set of mitochondrial genes, we had to identify polymorphisms to differentiate between nuclear and mitochondrial copies of a mitochondrial transcript. We found that the affected transcripts were uncapped transcripts of mitochondrial origin, which were polyadenylated at multiple sites within their 3′region. Heat-induced enhancement of these transcripts was quickly restored during a short recovery period.Conclusions/SignificanceOur results show that polyadenylated transcripts of mitochondrial origin are more stable than previously suggested, and that their steady-state levels can even be significantly enhanced under certain conditions. As many microarrays contain mitochondrial probes, due to the frequent transfer of mitochondrial genes into the genome, these effects need to be considered when interpreting microarray data.
Highlights
Polyadenylation of RNAs has a decisive role in the regulation of RNA stability
Much to our surprise when we analysed a group of microarray experiments, we found significant signals for a gene cluster on chromosome 2 that corresponds to the mitochondrial insertion, showing significant correlation with heat shock response genes and up-regulation in response to heat treatment
It was even more surprising that for a large number of mitochondrial genes, polyadenylated transcripts became more abundant after moderate heat treatment
Summary
Polyadenylation of RNAs has a decisive role in the regulation of RNA stability. In eukaryotes, it confers stability for nuclear mRNA, regulates export of processed mRNAs to the cytoplasm and promotes translation initiation [1]; [2]. As for prokaryotes, polyadenylation of mRNAs in chloroplasts serves as a RNA degradation signal [4] and it promotes mRNA degradation in plant mitochondria [5]; [6]. Plant mitochondrial PNPase degrades rRNA and tRNA maturation by-products, and removes highly transcribed non-functional RNAs and antisense transcripts, following their polyadenylation. Polyadenylation promotes RNA degradation, and polyadenylated mitochondrial transcripts are widely considered to be rare and unstable. We followed up a surprising observation that a large number of mitochondrial transcripts are detectable in microarray experiments that used poly(A)-specific RNA probes, and that these transcript levels are significantly enhanced after heat treatment
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