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Distribution and phylogeny of EFL and EF-1alpha in Euglenozoa suggest ancestral co-occurrence followed by differential loss.

Gile GH, Faktorová D, Castlejohn CA, Burger G, Lang BF, Farmer MA, Lukes J, Keeling PJ - PLoS ONE (2009)

Bottom Line: EF-1alpha was found to be widespread and monophyletic, suggesting it is ancestral in this group.EFL was found in some species belonging to each of the three euglenozoan lineages, diplonemids, kinetoplastids, and euglenids.Interestingly, the kinetoplastid EFL sequences are specifically related despite the fact that the lineages in which they are found are not sisters to one another, suggesting that EFL and EF-1alpha co-occurred in an early ancestor of kinetoplastids.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany, Canadian Institute for Advanced Research, University of British Columbia, Vancouver, British Columbia, Canada. ggile@interchange.ubc.ca

ABSTRACT

Background: The eukaryotic elongation factor EF-1alpha (also known as EF1A) catalyzes aminoacyl-tRNA binding by the ribosome during translation. Homologs of this essential protein occur in all domains of life, and it was previously thought to be ubiquitous in eukaryotes. Recently, however, a number of eukaryotes were found to lack EF-1alpha and instead encode a related protein called EFL (for EF-Like). EFL-encoding organisms are scattered widely across the tree of eukaryotes, and all have close relatives that encode EF-1alpha. This intriguingly complex distribution has been attributed to multiple lateral transfers because EFL's near mutual exclusivity with EF-1alpha makes an extended period of co-occurrence seem unlikely. However, differential loss may play a role in EFL evolution, and this possibility has been less widely discussed.

Methodology/principal findings: We have undertaken an EST- and PCR-based survey to determine the distribution of these two proteins in a previously under-sampled group, the Euglenozoa. EF-1alpha was found to be widespread and monophyletic, suggesting it is ancestral in this group. EFL was found in some species belonging to each of the three euglenozoan lineages, diplonemids, kinetoplastids, and euglenids.

Conclusions/significance: Interestingly, the kinetoplastid EFL sequences are specifically related despite the fact that the lineages in which they are found are not sisters to one another, suggesting that EFL and EF-1alpha co-occurred in an early ancestor of kinetoplastids. This represents the strongest phylogenetic evidence to date that differential loss has contributed to the complex distribution of EFL and EF-1alpha.

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Maximum likelihood phylogeny of EFL including Bayesian posterior probabilities.The tree was inferred under LG, RtREV, and CAT amino acids substitution models using 4 Γ categories plus invariable sites; the LG topology is displayed. Bootstrap support greater than 50% and Bayesian posterior probabilities greater than 0.8 are displayed at nodes, with LG/RtREV ML bootstrap values above and CAT model posterior probability below. Branches with hatch marks are displayed at one half their actual length. Euglenozoan taxa are boxed in red.
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pone-0005162-g002: Maximum likelihood phylogeny of EFL including Bayesian posterior probabilities.The tree was inferred under LG, RtREV, and CAT amino acids substitution models using 4 Γ categories plus invariable sites; the LG topology is displayed. Bootstrap support greater than 50% and Bayesian posterior probabilities greater than 0.8 are displayed at nodes, with LG/RtREV ML bootstrap values above and CAT model posterior probability below. Branches with hatch marks are displayed at one half their actual length. Euglenozoan taxa are boxed in red.

Mentions: EFL phylogenies were inferred using the same models used for EF-1α. While much of the tree remains unresolved in all analyses, as is typical of EFL trees [3], [4], [8]–[10], three features emerge that are pertinent to the origin and evolution of EFL in the Euglenozoa (Fig. 2). First, the three lineages of euglenozoan EFL, diplonemids, kinetoplastids, and P. cantuscygni, never branch together. However, their positions are not clearly resolved, none of the nodes that separate them are supported, and the relative branching order of the three euglenozoan EFL lineages, Goniomonas amphinema, Perkinsus marinus, red algae, and a group of opisthokonts, varies greatly depending on the dataset analyzed and evolutionary model employed. Second, diplonemid EFL sequences robustly branch together in all analyses, suggesting that EFL is ancestral in this group. Third, and most importantly, the two kinetoplastid EFL sequences branch together with complete support in all analyses, providing strong evidence that EFL was present in their common ancestor as well. This is significant because N. saliens and T. borreli are members of two different subgroups in organismal phylogenies of kinetoplastids [16], [20], [51], [52], [55], which therefore places EFL at least as far back as the common ancestor of all kinetoplastids save the earliest-branching lineage that includes P. amoebae (Fig. 3). Because the phylogeny of EF-1α suggests that this protein was also present in the ancestor of kinetoplastids, we infer that both genes must have co-existed through much of early kinetoplastid evolution, and it therefore appears that the complex distribution of EFL and EF-1α in the kinetoplastids is likely due to differential loss.


Distribution and phylogeny of EFL and EF-1alpha in Euglenozoa suggest ancestral co-occurrence followed by differential loss.

Gile GH, Faktorová D, Castlejohn CA, Burger G, Lang BF, Farmer MA, Lukes J, Keeling PJ - PLoS ONE (2009)

Maximum likelihood phylogeny of EFL including Bayesian posterior probabilities.The tree was inferred under LG, RtREV, and CAT amino acids substitution models using 4 Γ categories plus invariable sites; the LG topology is displayed. Bootstrap support greater than 50% and Bayesian posterior probabilities greater than 0.8 are displayed at nodes, with LG/RtREV ML bootstrap values above and CAT model posterior probability below. Branches with hatch marks are displayed at one half their actual length. Euglenozoan taxa are boxed in red.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2664479&req=5

pone-0005162-g002: Maximum likelihood phylogeny of EFL including Bayesian posterior probabilities.The tree was inferred under LG, RtREV, and CAT amino acids substitution models using 4 Γ categories plus invariable sites; the LG topology is displayed. Bootstrap support greater than 50% and Bayesian posterior probabilities greater than 0.8 are displayed at nodes, with LG/RtREV ML bootstrap values above and CAT model posterior probability below. Branches with hatch marks are displayed at one half their actual length. Euglenozoan taxa are boxed in red.
Mentions: EFL phylogenies were inferred using the same models used for EF-1α. While much of the tree remains unresolved in all analyses, as is typical of EFL trees [3], [4], [8]–[10], three features emerge that are pertinent to the origin and evolution of EFL in the Euglenozoa (Fig. 2). First, the three lineages of euglenozoan EFL, diplonemids, kinetoplastids, and P. cantuscygni, never branch together. However, their positions are not clearly resolved, none of the nodes that separate them are supported, and the relative branching order of the three euglenozoan EFL lineages, Goniomonas amphinema, Perkinsus marinus, red algae, and a group of opisthokonts, varies greatly depending on the dataset analyzed and evolutionary model employed. Second, diplonemid EFL sequences robustly branch together in all analyses, suggesting that EFL is ancestral in this group. Third, and most importantly, the two kinetoplastid EFL sequences branch together with complete support in all analyses, providing strong evidence that EFL was present in their common ancestor as well. This is significant because N. saliens and T. borreli are members of two different subgroups in organismal phylogenies of kinetoplastids [16], [20], [51], [52], [55], which therefore places EFL at least as far back as the common ancestor of all kinetoplastids save the earliest-branching lineage that includes P. amoebae (Fig. 3). Because the phylogeny of EF-1α suggests that this protein was also present in the ancestor of kinetoplastids, we infer that both genes must have co-existed through much of early kinetoplastid evolution, and it therefore appears that the complex distribution of EFL and EF-1α in the kinetoplastids is likely due to differential loss.

Bottom Line: EF-1alpha was found to be widespread and monophyletic, suggesting it is ancestral in this group.EFL was found in some species belonging to each of the three euglenozoan lineages, diplonemids, kinetoplastids, and euglenids.Interestingly, the kinetoplastid EFL sequences are specifically related despite the fact that the lineages in which they are found are not sisters to one another, suggesting that EFL and EF-1alpha co-occurred in an early ancestor of kinetoplastids.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany, Canadian Institute for Advanced Research, University of British Columbia, Vancouver, British Columbia, Canada. ggile@interchange.ubc.ca

ABSTRACT

Background: The eukaryotic elongation factor EF-1alpha (also known as EF1A) catalyzes aminoacyl-tRNA binding by the ribosome during translation. Homologs of this essential protein occur in all domains of life, and it was previously thought to be ubiquitous in eukaryotes. Recently, however, a number of eukaryotes were found to lack EF-1alpha and instead encode a related protein called EFL (for EF-Like). EFL-encoding organisms are scattered widely across the tree of eukaryotes, and all have close relatives that encode EF-1alpha. This intriguingly complex distribution has been attributed to multiple lateral transfers because EFL's near mutual exclusivity with EF-1alpha makes an extended period of co-occurrence seem unlikely. However, differential loss may play a role in EFL evolution, and this possibility has been less widely discussed.

Methodology/principal findings: We have undertaken an EST- and PCR-based survey to determine the distribution of these two proteins in a previously under-sampled group, the Euglenozoa. EF-1alpha was found to be widespread and monophyletic, suggesting it is ancestral in this group. EFL was found in some species belonging to each of the three euglenozoan lineages, diplonemids, kinetoplastids, and euglenids.

Conclusions/significance: Interestingly, the kinetoplastid EFL sequences are specifically related despite the fact that the lineages in which they are found are not sisters to one another, suggesting that EFL and EF-1alpha co-occurred in an early ancestor of kinetoplastids. This represents the strongest phylogenetic evidence to date that differential loss has contributed to the complex distribution of EFL and EF-1alpha.

Show MeSH