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. 2014 Oct 1:14:211.
doi: 10.1186/s12862-014-0211-2.

Chloroplast phylogenomic analysis resolves deep-level relationships within the green algal class Trebouxiophyceae

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Chloroplast phylogenomic analysis resolves deep-level relationships within the green algal class Trebouxiophyceae

Claude Lemieux et al. BMC Evol Biol. .

Abstract

Background: The green algae represent one of the most successful groups of photosynthetic eukaryotes, but compared to their land plant relatives, surprisingly little is known about their evolutionary history. This is in great part due to the difficulty of recognizing species diversity behind morphologically similar organisms. The Trebouxiophyceae is a species-rich class of the Chlorophyta that includes symbionts (e.g. lichenized algae) as well as free-living green algae. Members of this group display remarkable ecological variation, occurring in aquatic, terrestrial and aeroterrestrial environments. Because a reliable backbone phylogeny is essential to understand the evolutionary history of the Trebouxiophyceae, we sought to identify the relationships among the major trebouxiophycean lineages that have been previously recognized in nuclear-encoded 18S rRNA phylogenies. To this end, we used a chloroplast phylogenomic approach.

Results: We determined the sequences of 29 chlorophyte chloroplast genomes and assembled amino acid and nucleotide data sets derived from 79 chloroplast genes of 61 chlorophytes, including 35 trebouxiophyceans. The amino acid- and nucleotide-based phylogenies inferred using maximum likelihood and Bayesian methods and various models of sequence evolution revealed essentially the same relationships for the trebouxiophyceans. Two major groups were identified: a strongly supported clade of 29 taxa (core trebouxiophyceans) that is sister to the Chlorophyceae + Ulvophyceae and a clade comprising the Chlorellales and Pedinophyceae that represents a basal divergence relative to the former group. The core trebouxiophyceans form a grade of strongly supported clades that include a novel lineage represented by the desert crust alga Pleurastrosarcina brevispinosa. The assemblage composed of the Oocystis and Geminella clades is the deepest divergence of the core trebouxiophyceans. Like most of the chlorellaleans, early-diverging core trebouxiophyceans are predominantly planktonic species, whereas core trebouxiophyceans occupying more derived lineages are mostly terrestrial or aeroterrestrial algae.

Conclusions: Our phylogenomic study provides a solid foundation for addressing fundamental questions related to the biology and ecology of the Trebouxiophyceae. The inferred trees reveal that this class is not monophyletic; they offer new insights not only into the internal structure of the class but also into the lifestyle of its founding members and subsequent adaptations to changing environments.

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Figures

Figure 1
Figure 1
Phylogeny of 61 chlorophytes inferred using a data set of 15,549 positions assembled from 79 cpDNA-encoded proteins. The tree presented here is the best-scoring ML tree inferred under the GTR + Γ4 model. Support values are reported on the nodes: from top to bottom, or from left to right, are shown the posterior probability (PP) values for the PhyloBayes CATGTR + Γ4 analyses and the bootstrap support (BS) values for the RAxML GTR + Γ4, LG4X and gcpREV + Γ4 analyses. Black dots indicate that the corresponding branches received BS and PP values of 100% in all four analyses. Shaded areas identify the clades that are well supported in 18S rDNA phylogenies. The histograms on the left indicate the proportion of missing data for each taxon. The scale bar denotes the estimated number of amino acid substitutions per site.
Figure 2
Figure 2
Correspondence analysis of amino acid usage in the data set of 15,549 positions. The members of the Chlorellales and Pedinophyceae are found within the circled area.
Figure 3
Figure 3
Influence of the Pedinophyceae on the placement of the Chlorellales. (A) Phylogeny of chlorophytes inferred under the GTR + Γ4 model using the amino acid data set of 15,549 positions after exclusion of the Pedinophyceae. The best-scoring RAxML tree is presented and support values are reported on the nodes, with black dots indicating 100% BS values. The scale bar denotes the estimated number of amino acid substitutions per site. (B) Confidence assessment of the three possible topologies (T1, T2 and T3) for the placement of the Chlorellales under the GTR + Γ4 model. The ΔlnL value indicates the difference in log likelihood relative to the best tree (T1). Local bootstrap probabilities were estimated by resampling of the estimated log-likelihood (RELL). pAU, P value for the approximately unbiased (AU) test [60] as implemented in CONSEL 0.20 [61].
Figure 4
Figure 4
Phylogeny of 61 chlorophytes inferred using nucleotide data sets assembled from 79 cpDNA-encoded genes. The tree presented here is the best-scoring ML tree inferred using the degen1 data set under the GTR + Γ4 model. Support values are reported on the nodes: from top to bottom, or from left to right, are shown the BS values for the analyses of the degen1 and nt1 + 2 data sets. Black dots indicate that the corresponding branches received BS values of 100% in the two analyses. Shaded areas identify the trebouxiophycean lineages uncovered in this study. Open and filled squares denote aquatic and terrestrial/aeroterrestrial habitats, respectively; an open square containing a star indicates that the taxon is a symbiont. The scale bar denotes the estimated number of nucleotide substitutions per site.

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