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Evolution and diversification of the organellar release factor family.

Duarte I, Nabuurs SB, Magno R, Huynen M - Mol. Biol. Evol. (2012)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Centre for Molecular and Biomolecular Informatics, Nijmegen Centre for Molecular Life Sciences, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands.

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.

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Bayesian RF2 phylogeny. The top branch, highlighted in yellow, groups known mitochondrial proteins (mtRF2a), several nonresolved bacterial RF2s and, highlighted with a checkerboard pattern, the mtRF2c branch (which has been experimentally shown to localize in the chloroplast). The bottom branch, highlighted in green, clusters the plastidial RF2s and mtRF2b (indicated by a vertical strip pattern). Alphaproteobacteria and cyanobacteria are highlighted in bold. (Colors for collapsed taxa: blue—bacteria; pink—alphaproteobacteria; green—viridiplantae; yellow—amoebozoa; brown—apicomplexa; and cyan—cyanobacteria). (Full noncollapsed tree available in supplementary figure 2, Supplementary Materials online.)
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mss157-F3: Bayesian RF2 phylogeny. The top branch, highlighted in yellow, groups known mitochondrial proteins (mtRF2a), several nonresolved bacterial RF2s and, highlighted with a checkerboard pattern, the mtRF2c branch (which has been experimentally shown to localize in the chloroplast). The bottom branch, highlighted in green, clusters the plastidial RF2s and mtRF2b (indicated by a vertical strip pattern). Alphaproteobacteria and cyanobacteria are highlighted in bold. (Colors for collapsed taxa: blue—bacteria; pink—alphaproteobacteria; green—viridiplantae; yellow—amoebozoa; brown—apicomplexa; and cyan—cyanobacteria). (Full noncollapsed tree available in supplementary figure 2, Supplementary Materials online.)

Mentions: The expected alphaproteobacterial ancestry of this protein, given the endosymbiotic origin of mitochondria, cannot be unequivocally established from our RF2 phylogeny (fig. 3). Most prokaryotic sequences present in this dataset do not form a monophyletic group, being instead all grouped in an unresolved branch, containing also most eukaryotic mitochondrial RF2s (fig. 3).Fig. 3.


Evolution and diversification of the organellar release factor family.

Duarte I, Nabuurs SB, Magno R, Huynen M - Mol. Biol. Evol. (2012)

Bayesian RF2 phylogeny. The top branch, highlighted in yellow, groups known mitochondrial proteins (mtRF2a), several nonresolved bacterial RF2s and, highlighted with a checkerboard pattern, the mtRF2c branch (which has been experimentally shown to localize in the chloroplast). The bottom branch, highlighted in green, clusters the plastidial RF2s and mtRF2b (indicated by a vertical strip pattern). Alphaproteobacteria and cyanobacteria are highlighted in bold. (Colors for collapsed taxa: blue—bacteria; pink—alphaproteobacteria; green—viridiplantae; yellow—amoebozoa; brown—apicomplexa; and cyan—cyanobacteria). (Full noncollapsed tree available in supplementary figure 2, Supplementary Materials online.)
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3472500&req=5

mss157-F3: Bayesian RF2 phylogeny. The top branch, highlighted in yellow, groups known mitochondrial proteins (mtRF2a), several nonresolved bacterial RF2s and, highlighted with a checkerboard pattern, the mtRF2c branch (which has been experimentally shown to localize in the chloroplast). The bottom branch, highlighted in green, clusters the plastidial RF2s and mtRF2b (indicated by a vertical strip pattern). Alphaproteobacteria and cyanobacteria are highlighted in bold. (Colors for collapsed taxa: blue—bacteria; pink—alphaproteobacteria; green—viridiplantae; yellow—amoebozoa; brown—apicomplexa; and cyan—cyanobacteria). (Full noncollapsed tree available in supplementary figure 2, Supplementary Materials online.)
Mentions: The expected alphaproteobacterial ancestry of this protein, given the endosymbiotic origin of mitochondria, cannot be unequivocally established from our RF2 phylogeny (fig. 3). Most prokaryotic sequences present in this dataset do not form a monophyletic group, being instead all grouped in an unresolved branch, containing also most eukaryotic mitochondrial RF2s (fig. 3).Fig. 3.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Centre for Molecular and Biomolecular Informatics, Nijmegen Centre for Molecular Life Sciences, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands.

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.

Show MeSH