Alternative mRNA editing in trypanosomes is extensive and may contribute to mitochondrial protein diversity.

Torsten Ochsenreiter,Michael Cipriano,Stephen L Hajduk,Michael Gray

doi:10.1371/journal.pone.0001566

Torsten Ochsenreiter, Michael Cipriano + Show 2 more

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https://doi.org/10.1371/journal.pone.0001566

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Abstract

The editing of trypanosome mitochondrial mRNAs produces transcripts necessary for mitochondrial functions including electron transport and oxidative phosphorylation. Precursor-mRNAs are often extensively edited by specific uridine insertion or deletion that is directed by small guide RNAs (gRNAs). Recently, it has been shown that cytochrome c oxidase subunit III (COXIII) mRNAs can be alternatively edited to encode a novel mitochondrial membrane protein composed of a unique hydrophilic N-terminal sequence of unknown function and the C-terminal hydrophobic segment of COXIII. To extend the analysis of alternative editing in Trypanosoma brucei we have constructed libraries with over 1100 full-length mitochondrial cDNAs and the sequences of over 1200 gRNA genes. Using this data, we show that alternative editing of COXIII, ATPase subunit 6 (A6), and NADH dehydrogenase subunits 7, 8 and 9 (ND7, 8, 9) mRNAs can produce novel open reading frames (ORFs). Several gRNAs potentially responsible for the alternative editing of these mRNAs were also identified. These findings show that alternative editing of mitochondrial mRNAs is common in T. brucei and expands the diversity of mitochondrial proteins in these organisms.

Highlights

RNA editing in trypanosome mitochondria is a posttranscriptional process of endonuclease cleavage, uridine insertion or deletion and ligation of mRNAs that is directed by small noncoding guide RNAs
Many mitochondrial mRNAs are so extensively edited that their gene sequences failed to reveal the open reading frames (ORFs) for conventional protein products
The recent discovery that alternative RNA editing of a c oxidase subunit III (COXIII) mRNA can create an mRNA that is translated to produce a novel protein, AEP-1, suggests that alternative editing may provide a powerful means to fine-tune and diversify trypanosome mitochondrial gene products [11]

Summary

Introduction

RNA editing in trypanosome mitochondria is a posttranscriptional process of endonuclease cleavage, uridine insertion or deletion and ligation of mRNAs that is directed by small noncoding guide RNAs (gRNAs) (reviewed in [1,2,3]). The genes encoding the trypanosome mitochondrial mRNAs are found on maxicircles, while gRNAs are largely encoded by genes located on minicircles. Uridine insertion/ deletion editing effectively combines information at the RNA level that is encoded separately, on minicircles and maxicircles in the mitochondrial genome of trypanosomes [7]. We have recently identified an alternatively edited COXIII mRNA and have shown its protein product associates in a high molecular weight complex in trypanosome mitochondrial membranes [11]

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