Evolution and Diversification of the Organellar Release Factor Family
Open Access
- 24 July 2012
- journal article
- research article
- Published by Oxford University Press (OUP) in Molecular Biology and Evolution
- Vol. 29 (11), 3497-3512
- https://doi.org/10.1093/molbev/mss157
Abstract
Translation termination is accomplished by proteins of the Class I release factor family (RF) that recognize stop codons and catalyze the ribosomal release of the newly synthesized peptide. Bacteria have two canonical RFs: RF1 recognizes UAA and UAG, RF2 recognizes UAA and UGA. Despite that these two release factor proteins are sufficient for de facto translation termination, the eukaryotic organellar RF protein family, which has evolved from bacterial release factors, has expanded considerably, comprising multiple subfamilies, most of which have not been functionally characterized or formally classified. Here, we integrate multiple sources of information to analyze the remarkable differentiation of the RF family among organelles. We document the origin, phylogenetic distribution and sequence structure features of the mitochondrial and plastidial release factors: mtRF1a, mtRF1, mtRF2a, mtRF2b, mtRF2c, ICT1, C12orf65, pRF1, and pRF2, and review published relevant experimental data. The canonical release factors (mtRF1a, mtRF2a, pRF1, and pRF2) and ICT1 are derived from bacterial ancestors, whereas the others have resulted from gene duplications of another release factor. These new RF family members have all lost one or more specific motifs relevant for bona fide release factor function but are mostly targeted to the same organelle as their ancestor. We also characterize the subset of canonical release factor proteins that bear nonclassical PxT/SPF tripeptide motifs and provide a molecular-model-based rationale for their retained ability to recognize stop codons. Finally, we analyze the coevolution of canonical RFs with the organellar genetic code. Although the RF presence in an organelle and its stop codon usage tend to coevolve, we find three taxa that encode an RF2 without using UGA stop codons, and one reverse scenario, where mamiellales green algae use UGA stop codons in their mitochondria without having a mitochondrial type RF2. For the latter, we put forward a “stop-codon reinvention” hypothesis that involves the retargeting of the plastid release factor to the mitochondrion.Keywords
This publication has 79 references indexed in Scilit:
- Mutations in C12orf65 in Patients with Encephalomyopathy and a Mitochondrial Translation DefectAmerican Journal of Human Genetics, 2010
- Recognition of the amber UAG stop codon by release factor RF1The EMBO Journal, 2010
- A functional peptidyl-tRNA hydrolase, ICT1, has been recruited into the human mitochondrial ribosomeThe EMBO Journal, 2010
- Improving physical realism, stereochemistry, and side‐chain accuracy in homology modeling: Four approaches that performed well in CASP8Proteins-Structure Function and Bioinformatics, 2009
- A Mitochondrial Protein Compendium Elucidates Complex I Disease BiologyCell, 2008
- mtRF1a Is a Human Mitochondrial Translation Release Factor Decoding the Major Termination Codons UAA and UAGMolecular Cell, 2007
- The Mechanisms of Codon Reassignments in Mitochondrial Genetic CodesJournal of Molecular Evolution, 2007
- Global analysis of protein localization in budding yeastNature, 2003
- Evidence for a Single Origin of the 35 kb Plastid DNA in ApicomplexansProtist, 1998
- A highly conserved eukaryotic protein family possessing properties of polypeptide chain release factorNature, 1994