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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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Coevolution of the plastidial RFs with the plastidial genetic code. The red and green backgrounds mark the red and green plastid lineages, respectively. The branching order is based on Marin et al. (2005) and Keeling (2010). Blue circles indicate a primary endosymbiosis and blue squares represent a secondary endosymbiosis event. Red font highlights the cases that represent exceptions to the coevolution of the RF with the plastidial genetic code, where the pRF2 is present in the genome, but TGA stop codons are not used. The star marks the possible “TGA-stop reinvention.” Question marks are used for uncertain data and two asterisks indicate no whole genome available. (See supplementary methods, Supplementary Materials online for details about the species used in making this figure.)
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mss157-F5: Coevolution of the plastidial RFs with the plastidial genetic code. The red and green backgrounds mark the red and green plastid lineages, respectively. The branching order is based on Marin et al. (2005) and Keeling (2010). Blue circles indicate a primary endosymbiosis and blue squares represent a secondary endosymbiosis event. Red font highlights the cases that represent exceptions to the coevolution of the RF with the plastidial genetic code, where the pRF2 is present in the genome, but TGA stop codons are not used. The star marks the possible “TGA-stop reinvention.” Question marks are used for uncertain data and two asterisks indicate no whole genome available. (See supplementary methods, Supplementary Materials online for details about the species used in making this figure.)

Mentions: We performed a systematic analysis of the organellar genetic code and the presence of mitochondrial and plastidial RF2 (figs. 4 and 5). Based on 95 currently sequenced nuclear genomes of organisms with annotated organellar genomes, the mitochondrial-type RF2 has been lost five times in evolution: in kinetoplastids, diatoms, alveolates, at the root of the opisthokonta and in the green algae lineage, whereas the usage of TGA as stop codon in mitochondrial genomes has been lost seven times: not only in the same diatoms, alveolata, opisthokonta, and green algae, but also in heterolobosea, rhizaria, and some amoebozoa (fig. 4).Fig. 5.


Evolution and diversification of the organellar release factor family.

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

Coevolution of the plastidial RFs with the plastidial genetic code. The red and green backgrounds mark the red and green plastid lineages, respectively. The branching order is based on Marin et al. (2005) and Keeling (2010). Blue circles indicate a primary endosymbiosis and blue squares represent a secondary endosymbiosis event. Red font highlights the cases that represent exceptions to the coevolution of the RF with the plastidial genetic code, where the pRF2 is present in the genome, but TGA stop codons are not used. The star marks the possible “TGA-stop reinvention.” Question marks are used for uncertain data and two asterisks indicate no whole genome available. (See supplementary methods, Supplementary Materials online for details about the species used in making this figure.)
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

mss157-F5: Coevolution of the plastidial RFs with the plastidial genetic code. The red and green backgrounds mark the red and green plastid lineages, respectively. The branching order is based on Marin et al. (2005) and Keeling (2010). Blue circles indicate a primary endosymbiosis and blue squares represent a secondary endosymbiosis event. Red font highlights the cases that represent exceptions to the coevolution of the RF with the plastidial genetic code, where the pRF2 is present in the genome, but TGA stop codons are not used. The star marks the possible “TGA-stop reinvention.” Question marks are used for uncertain data and two asterisks indicate no whole genome available. (See supplementary methods, Supplementary Materials online for details about the species used in making this figure.)
Mentions: We performed a systematic analysis of the organellar genetic code and the presence of mitochondrial and plastidial RF2 (figs. 4 and 5). Based on 95 currently sequenced nuclear genomes of organisms with annotated organellar genomes, the mitochondrial-type RF2 has been lost five times in evolution: in kinetoplastids, diatoms, alveolates, at the root of the opisthokonta and in the green algae lineage, whereas the usage of TGA as stop codon in mitochondrial genomes has been lost seven times: not only in the same diatoms, alveolata, opisthokonta, and green algae, but also in heterolobosea, rhizaria, and some amoebozoa (fig. 4).Fig. 5.

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
Related in: MedlinePlus