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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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Full release factor family neighbor-joining tree. This figure presents an overview of the nine RF subfamilies roughly separated by the NJ algorithm, recapturing the pattern of sequence motifs characteristic of each protein. It summarizes, in one image, the main sequence features presented by individual organisms. Each subfamily branch is highlighted with a different color following the exterior labels. Well-resolved branches from well-established taxa were collapsed to improve readability. In these collapsed branches, a representative domain and motif structure is displayed, slightly enlarged in order to stand out from other individual results. The following species were chosen as models for these representative domains: viridiplantae and land plants—Arabidopsis thaliana; metazoa, vertebrates, and mammals—Homo sapiens; insects—Drosophila melanogaster; and fungi—Saccharomyces cerevisiae. (Legend: Pfam domains displayed in front of each leaf: green hexagon—PCRF (peptide chain release factor) and dark-blue arrow—RF-1. Superimposed on the Pfam domains are the functionally characterized motifs: purple diamond—alpha5 helix; cyan oval—PxT motif, yellow oval—SPF motif, red oval—PExGxS motif; red diamond—RT insert; green diamond—GGQ motif; pink hexagon—C-terminal helix; and orange rectangle—ICT1-specific helix.)
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mss157-F1: Full release factor family neighbor-joining tree. This figure presents an overview of the nine RF subfamilies roughly separated by the NJ algorithm, recapturing the pattern of sequence motifs characteristic of each protein. It summarizes, in one image, the main sequence features presented by individual organisms. Each subfamily branch is highlighted with a different color following the exterior labels. Well-resolved branches from well-established taxa were collapsed to improve readability. In these collapsed branches, a representative domain and motif structure is displayed, slightly enlarged in order to stand out from other individual results. The following species were chosen as models for these representative domains: viridiplantae and land plants—Arabidopsis thaliana; metazoa, vertebrates, and mammals—Homo sapiens; insects—Drosophila melanogaster; and fungi—Saccharomyces cerevisiae. (Legend: Pfam domains displayed in front of each leaf: green hexagon—PCRF (peptide chain release factor) and dark-blue arrow—RF-1. Superimposed on the Pfam domains are the functionally characterized motifs: purple diamond—alpha5 helix; cyan oval—PxT motif, yellow oval—SPF motif, red oval—PExGxS motif; red diamond—RT insert; green diamond—GGQ motif; pink hexagon—C-terminal helix; and orange rectangle—ICT1-specific helix.)

Mentions: To provide an overview of the organellar release factor family, we first calculated a simple, yet comprehensive and illustrative tree of the nine distinct subfamilies (fig. 1). The figure shows congruence between tree topology, domain architecture, and the presence of functionally relevant motifs allowing the classification of each organisms’ RFs.Fig. 1.


Evolution and diversification of the organellar release factor family.

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

Full release factor family neighbor-joining tree. This figure presents an overview of the nine RF subfamilies roughly separated by the NJ algorithm, recapturing the pattern of sequence motifs characteristic of each protein. It summarizes, in one image, the main sequence features presented by individual organisms. Each subfamily branch is highlighted with a different color following the exterior labels. Well-resolved branches from well-established taxa were collapsed to improve readability. In these collapsed branches, a representative domain and motif structure is displayed, slightly enlarged in order to stand out from other individual results. The following species were chosen as models for these representative domains: viridiplantae and land plants—Arabidopsis thaliana; metazoa, vertebrates, and mammals—Homo sapiens; insects—Drosophila melanogaster; and fungi—Saccharomyces cerevisiae. (Legend: Pfam domains displayed in front of each leaf: green hexagon—PCRF (peptide chain release factor) and dark-blue arrow—RF-1. Superimposed on the Pfam domains are the functionally characterized motifs: purple diamond—alpha5 helix; cyan oval—PxT motif, yellow oval—SPF motif, red oval—PExGxS motif; red diamond—RT insert; green diamond—GGQ motif; pink hexagon—C-terminal helix; and orange rectangle—ICT1-specific helix.)
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

mss157-F1: Full release factor family neighbor-joining tree. This figure presents an overview of the nine RF subfamilies roughly separated by the NJ algorithm, recapturing the pattern of sequence motifs characteristic of each protein. It summarizes, in one image, the main sequence features presented by individual organisms. Each subfamily branch is highlighted with a different color following the exterior labels. Well-resolved branches from well-established taxa were collapsed to improve readability. In these collapsed branches, a representative domain and motif structure is displayed, slightly enlarged in order to stand out from other individual results. The following species were chosen as models for these representative domains: viridiplantae and land plants—Arabidopsis thaliana; metazoa, vertebrates, and mammals—Homo sapiens; insects—Drosophila melanogaster; and fungi—Saccharomyces cerevisiae. (Legend: Pfam domains displayed in front of each leaf: green hexagon—PCRF (peptide chain release factor) and dark-blue arrow—RF-1. Superimposed on the Pfam domains are the functionally characterized motifs: purple diamond—alpha5 helix; cyan oval—PxT motif, yellow oval—SPF motif, red oval—PExGxS motif; red diamond—RT insert; green diamond—GGQ motif; pink hexagon—C-terminal helix; and orange rectangle—ICT1-specific helix.)
Mentions: To provide an overview of the organellar release factor family, we first calculated a simple, yet comprehensive and illustrative tree of the nine distinct subfamilies (fig. 1). The figure shows congruence between tree topology, domain architecture, and the presence of functionally relevant motifs allowing the classification of each organisms’ RFs.Fig. 1.

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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