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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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Schematic eukaryotic phylogeny displaying, per lineage, the coevolution of the mitochondrial genetic code with the codon-specific RFs. The red circle indicates the unique primary endosymbiosis event that originated the mitochondrion. The green algae stop-codon reinvention hypothesis is detailed in the gray “zoom-in” area. Species relationships were assembled from two studies: the main tree is based on the consensus tree depicting the six main eukaryotic groups from Simpson and Roger (2004) and the green algae lineage is based on the 18S rRNA gene tree published by Worden et al. (2009). Branching order is meaningful, but not branch length. Red font highlights the exceptions to the coevolution discussed in the text. The star marks the “TGA-stop reinvention” with pRF2 relocalization hypothesis in the green lineage. Question marks are used for uncertain data, and two asterisks indicate no mitochondrial genome available. (See supplementary methods, Supplementary Materials online for details about the species used in making this figure).
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mss157-F4: Schematic eukaryotic phylogeny displaying, per lineage, the coevolution of the mitochondrial genetic code with the codon-specific RFs. The red circle indicates the unique primary endosymbiosis event that originated the mitochondrion. The green algae stop-codon reinvention hypothesis is detailed in the gray “zoom-in” area. Species relationships were assembled from two studies: the main tree is based on the consensus tree depicting the six main eukaryotic groups from Simpson and Roger (2004) and the green algae lineage is based on the 18S rRNA gene tree published by Worden et al. (2009). Branching order is meaningful, but not branch length. Red font highlights the exceptions to the coevolution discussed in the text. The star marks the “TGA-stop reinvention” with pRF2 relocalization hypothesis in the green lineage. Question marks are used for uncertain data, and two asterisks indicate no mitochondrial genome available. (See supplementary methods, Supplementary Materials online for details about the species used in making this figure).

Mentions: The mitochondrial mtRF2a has a relatively narrow phylogenetic distribution, when compared to its mtRF1a counterpart. It has been lost at least five times during the eukaryotic evolution (fig. 4), coevolving together with the mitochondrial genetic code (see section II. Release factors and the evolution of the genetic code). It is only consistently found in streptophytes (land plants), red algae, dictyosteliida, and some stramenopiles (namely in brown algae, oomycetes and Blastocystis). It is absent from animals, fungi and excavata, with the exception of the heterolobosean Naegleria gruberi (supplementary table 1, Supplementary Material online).


Evolution and diversification of the organellar release factor family.

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

Schematic eukaryotic phylogeny displaying, per lineage, the coevolution of the mitochondrial genetic code with the codon-specific RFs. The red circle indicates the unique primary endosymbiosis event that originated the mitochondrion. The green algae stop-codon reinvention hypothesis is detailed in the gray “zoom-in” area. Species relationships were assembled from two studies: the main tree is based on the consensus tree depicting the six main eukaryotic groups from Simpson and Roger (2004) and the green algae lineage is based on the 18S rRNA gene tree published by Worden et al. (2009). Branching order is meaningful, but not branch length. Red font highlights the exceptions to the coevolution discussed in the text. The star marks the “TGA-stop reinvention” with pRF2 relocalization hypothesis in the green lineage. Question marks are used for uncertain data, and two asterisks indicate no mitochondrial 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-F4: Schematic eukaryotic phylogeny displaying, per lineage, the coevolution of the mitochondrial genetic code with the codon-specific RFs. The red circle indicates the unique primary endosymbiosis event that originated the mitochondrion. The green algae stop-codon reinvention hypothesis is detailed in the gray “zoom-in” area. Species relationships were assembled from two studies: the main tree is based on the consensus tree depicting the six main eukaryotic groups from Simpson and Roger (2004) and the green algae lineage is based on the 18S rRNA gene tree published by Worden et al. (2009). Branching order is meaningful, but not branch length. Red font highlights the exceptions to the coevolution discussed in the text. The star marks the “TGA-stop reinvention” with pRF2 relocalization hypothesis in the green lineage. Question marks are used for uncertain data, and two asterisks indicate no mitochondrial genome available. (See supplementary methods, Supplementary Materials online for details about the species used in making this figure).
Mentions: The mitochondrial mtRF2a has a relatively narrow phylogenetic distribution, when compared to its mtRF1a counterpart. It has been lost at least five times during the eukaryotic evolution (fig. 4), coevolving together with the mitochondrial genetic code (see section II. Release factors and the evolution of the genetic code). It is only consistently found in streptophytes (land plants), red algae, dictyosteliida, and some stramenopiles (namely in brown algae, oomycetes and Blastocystis). It is absent from animals, fungi and excavata, with the exception of the heterolobosean Naegleria gruberi (supplementary table 1, Supplementary Material online).

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