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Eukaryotic genomic origins, parasites, and the essential nature of mitochondria

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Conflicting phylogenies for early land plants are caused by composition biases among synonymous substitutions
Publication . Cox, C. J.; Li, Blaise; Foster, P. G.; Embley, T. M.; Civáň, Peter
Plants are the primary producers of the terrestrial ecosystems that dominate much of the natural environment. Occurring approximately 480 Ma (Sanderson 2003; Kenrick et al. 2012), the evolutionary transition of plants from an aquatic to a terrestrial environment was accompanied by several major developmental innovations. The freshwater charophyte ancestors of land plants have a haplobiontic life cycle with a single haploid multicellular stage, whereas land plants, which include the bryophytes (liverworts, hornworts, and mosses) and tracheophytes (also called vascular plants, namely, lycopods, ferns, and seed plants), exhibit a marked alternation of generations with a diplobiontic life cycle with both haploid and diploid multicellular stages and where the embryo remains attached to, and is nourished by, the gametophyte (Haig 2008).
A congruent phylogenomic signal places eukaryotes within the Archaea
Publication . Williams, T. A.; Foster, P. G.; Nye, T. M. W.; Cox, C. J.; Martin Embley, T.
Determining the relationships among the major groups of cellular life is important for understanding the evolution of biological diversity, but is difficult given the enormous time spans involved. In the textbook ‘three domains’ tree based on informational genes, eukaryotes and Archaea share a common ancestor to the exclusion of Bacteria. However, some phylogenetic analyses of the same data have placed eukaryotes within the Archaea, as the nearest relatives of different archaeal lineages. We compared the support for these competing hypotheses using sophisticated phylogenetic methods and an improved sampling of archaeal biodiversity. We also employed both new and existing tests of phylogenetic congruence to explore the level of uncertainty and conflict in the data. Our analyses suggested that much of the observed incongruence is weakly supported or associated with poorly fitting evolutionary models. All of our phylogenetic analyses, whether on small subunit and large subunit ribosomal RNA or concatenated protein-coding genes, recovered a monophyletic group containing eukaryotes and the TACK archaeal superphylum comprising the Thaumarchaeota, Aigarchaeota, Crenarchaeota and Korarchaeota. Hence, while our results provide no support for the iconic three-domain tree of life, they are consistent with an extended eocyte hypothesis whereby vital components of the eukaryotic nuclear lineage originated from within the archaeal radiation.
Analyses of charophyte chloroplast genomes help characterize theancestral chloroplastgenomeof land plants
Publication . Civáň, Peter; Foster, P. G.; Embley, T. M.; Séneca, A.; Cox, C. J.
Despitethesignificanceoftherelationshipsbetweenembryophytesandtheircharophytealgalancestorsindecipheringtheoriginand evolutionary success of land plants, few chloroplast genomes of the charophyte algae have been reconstructed to date. Here, we present new data for three chloroplast genomes of the freshwater charophytes Klebsormidium flaccidum (Klebsormidiophyceae), Mesotaenium endlicherianum (Zygnematophyceae), and Roya anglica (Zygnematophyceae).
Compositional biases among synonymous substitutions cause conflict between gene and protein trees for plastid origins
Publication . Li, Blaise; Lopes, J. S.; Foster, P. G.; Embley, T. M.; Cox, C. J.
Archaeplastida (=Kingdom Plantae) are primary plastid-bearing organisms that evolved via the endosymbiotic association of a heterotrophic eukaryote host cell and a cyanobacterial endosymbiont approximately 1,400 Ma. Here, we present analyses of cyanobacterial and plastid genomes that show strongly conflicting phylogenies based on 75 plastid (or nuclear plastid-targeted) protein-coding genes and their direct translations to proteins. The conflict between genes and proteins is largely robust to the use of sophisticated data- and tree-heterogeneous composition models. However, by using nucleotide ambiguity codes to eliminate synonymous substitutions due to codon-degeneracy, we identify a composition bias, and dependent codon-usage bias, resulting from synonymous substitutions at all third codon positions and first codon positions of leucine and arginine, as the main cause for the conflicting phylogenetic signals. We argue that the protein-coding gene data analyses are likely misleading due to artifacts induced by convergent composition biases at first codon positions of leucine and arginine and at all third codon positions. Our analyses corroborate previous studies based on gene sequence analysis that suggest Cyanobacteria evolved by the early paraphyletic splitting of Gloeobacter and a specific Synechococcus strain (JA33Ab), with all other remaining cyanobacterial groups, including both unicellular and filamentous species, forming the sister-group to the Archaeplastida lineage. In addition, our analyses using better-fitting models suggest (but without statistically strong support) an early divergence of Glaucophyta within Archaeplastida, with the Rhodophyta (red algae), and Viridiplantae (green algae and land plants) forming a separate lineage.

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European Commission

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FP7

Funding Award Number

268701

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