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Tracing the evolution of streptophyte algae and their mitochondrial genome.

Turmel M, Otis C, Lemieux C - Genome Biol Evol (2013)

Bottom Line: Our results indicate that important changes occurred at the levels of genome size, gene order, and intron content within the Zygnematales.In contrast, the two members of the Charales display an extremely conservative pattern of mtDNA evolution.Collectively, our analyses of gene order and gene content and the phylogenies we inferred from 40 mtDNA-encoded proteins failed to resolve the relationships among the Zygnematales, Coleochaetales, and Charales; however, they are consistent with previous phylogenomic studies in favoring that the morphologically complex Charales are not sister to land plants.

View Article: PubMed Central - PubMed

Affiliation: Institut de Biologie Intégrative et des Systèmes, Département de Biochimie, de Microbiologie et de Bio-Informatique, Université Laval, Québec, Canada.

ABSTRACT
Six monophyletic groups of charophycean green algae are recognized within the Streptophyta. Although incongruent with earlier studies based on genes from three cellular compartments, chloroplast and nuclear phylogenomic analyses have resolved identical relationships among these groups, placing the Zygnematales or the Zygnematales + Coleochaetales as sister to land plants. The present investigation aimed at determining whether this consensus view is supported by the mitochondrial genome and at gaining insight into mitochondrial DNA (mtDNA) evolution within and across streptophyte algal lineages and during the transition toward the first land plants. We present here the newly sequenced mtDNAs of representatives of the Klebsormidiales (Entransia fimbriata and Klebsormidium spec.) and Zygnematales (Closterium baillyanum and Roya obtusa) and compare them with their homologs in other charophycean lineages as well as in selected embryophyte and chlorophyte lineages. Our results indicate that important changes occurred at the levels of genome size, gene order, and intron content within the Zygnematales. Although the representatives of the Klebsormidiales display more similarity in genome size and intron content, gene order seems more fluid and gene losses more frequent than in other charophycean lineages. In contrast, the two members of the Charales display an extremely conservative pattern of mtDNA evolution. Collectively, our analyses of gene order and gene content and the phylogenies we inferred from 40 mtDNA-encoded proteins failed to resolve the relationships among the Zygnematales, Coleochaetales, and Charales; however, they are consistent with previous phylogenomic studies in favoring that the morphologically complex Charales are not sister to land plants.

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Majority-rule consensus tree inferred by PhyloBayes under the CATGTR + Γ4 model using a data set of 7,210 positions assembled from 40 mtDNA-encoded proteins. This data set was generated from the data set of 9,013 positions by removing 20% of the fastest evolving sites. BP support values are reported on various nodes: from top to bottom are shown the values for the PhyloBayes CATGTR + Γ4 and CAT + Γ4 analyses and for the RAxML GTR + Γ4 and LG + Γ4 analyses. Black dots indicate that the corresponding branches received 100% BP support in all four analyses. The scale bar denotes the estimated number of amino acid substitutions per site.
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evt135-F9: Majority-rule consensus tree inferred by PhyloBayes under the CATGTR + Γ4 model using a data set of 7,210 positions assembled from 40 mtDNA-encoded proteins. This data set was generated from the data set of 9,013 positions by removing 20% of the fastest evolving sites. BP support values are reported on various nodes: from top to bottom are shown the values for the PhyloBayes CATGTR + Γ4 and CAT + Γ4 analyses and for the RAxML GTR + Γ4 and LG + Γ4 analyses. Black dots indicate that the corresponding branches received 100% BP support in all four analyses. The scale bar denotes the estimated number of amino acid substitutions per site.

Mentions: We tested whether eliminating various proportions of the fastest evolving sites (i.e., the sites prone to yield a non-phylogenetic signal) from the amino acid data set has any effect on the robustness of the consensus tree and on the frequencies of the alternative topologies recovered. Five trimmed data sets, in which the sites with the highest rates of sequence evolution were deleted by 5% increment, were analyzed using the ML (LG-Γ4 model) and BI (CAT + Γ4 and CATGTR + Γ4 models) methods. As illustrated in figure 8, removal of the fastest evolving sites (5–25%) markedly lowered support for the placement of the Charales as sister to all land plants (i.e., the T1 topology) and concomitantly increased support for the sister group relationship of the Zygnematales to the land plants (i.e., T2 topology). For the data set lacking 20% of the fastest evolving sites, we also showed that it is much less saturated with substitutions than the original data set (supplementary fig. S6, Supplementary Material online). This reduced data set of 7,210 positions was further analyzed by bootstrapping using the ML and BI methods (fig. 9). The consensus trees derived from all four analyses uncovered identical relationships among the charophycean lineages, that is, the relationships corresponding to the T2 topology. The sister group relationship of the Zygnematales to the land plants received weak BP support (56–66%); however, the better fitting was the model of sequence evolution, the higher was the observed support level for this grouping. It is also worth noting that, as the fit of the model improved, the clade uniting the Charales, Zygnematales, and land plants received lowered support due to the increased frequencies of the T3 and T4 topologies (table 2).Fig. 8.—


Tracing the evolution of streptophyte algae and their mitochondrial genome.

Turmel M, Otis C, Lemieux C - Genome Biol Evol (2013)

Majority-rule consensus tree inferred by PhyloBayes under the CATGTR + Γ4 model using a data set of 7,210 positions assembled from 40 mtDNA-encoded proteins. This data set was generated from the data set of 9,013 positions by removing 20% of the fastest evolving sites. BP support values are reported on various nodes: from top to bottom are shown the values for the PhyloBayes CATGTR + Γ4 and CAT + Γ4 analyses and for the RAxML GTR + Γ4 and LG + Γ4 analyses. Black dots indicate that the corresponding branches received 100% BP support in all four analyses. The scale bar denotes the estimated number of amino acid substitutions per site.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3814193&req=5

evt135-F9: Majority-rule consensus tree inferred by PhyloBayes under the CATGTR + Γ4 model using a data set of 7,210 positions assembled from 40 mtDNA-encoded proteins. This data set was generated from the data set of 9,013 positions by removing 20% of the fastest evolving sites. BP support values are reported on various nodes: from top to bottom are shown the values for the PhyloBayes CATGTR + Γ4 and CAT + Γ4 analyses and for the RAxML GTR + Γ4 and LG + Γ4 analyses. Black dots indicate that the corresponding branches received 100% BP support in all four analyses. The scale bar denotes the estimated number of amino acid substitutions per site.
Mentions: We tested whether eliminating various proportions of the fastest evolving sites (i.e., the sites prone to yield a non-phylogenetic signal) from the amino acid data set has any effect on the robustness of the consensus tree and on the frequencies of the alternative topologies recovered. Five trimmed data sets, in which the sites with the highest rates of sequence evolution were deleted by 5% increment, were analyzed using the ML (LG-Γ4 model) and BI (CAT + Γ4 and CATGTR + Γ4 models) methods. As illustrated in figure 8, removal of the fastest evolving sites (5–25%) markedly lowered support for the placement of the Charales as sister to all land plants (i.e., the T1 topology) and concomitantly increased support for the sister group relationship of the Zygnematales to the land plants (i.e., T2 topology). For the data set lacking 20% of the fastest evolving sites, we also showed that it is much less saturated with substitutions than the original data set (supplementary fig. S6, Supplementary Material online). This reduced data set of 7,210 positions was further analyzed by bootstrapping using the ML and BI methods (fig. 9). The consensus trees derived from all four analyses uncovered identical relationships among the charophycean lineages, that is, the relationships corresponding to the T2 topology. The sister group relationship of the Zygnematales to the land plants received weak BP support (56–66%); however, the better fitting was the model of sequence evolution, the higher was the observed support level for this grouping. It is also worth noting that, as the fit of the model improved, the clade uniting the Charales, Zygnematales, and land plants received lowered support due to the increased frequencies of the T3 and T4 topologies (table 2).Fig. 8.—

Bottom Line: Our results indicate that important changes occurred at the levels of genome size, gene order, and intron content within the Zygnematales.In contrast, the two members of the Charales display an extremely conservative pattern of mtDNA evolution.Collectively, our analyses of gene order and gene content and the phylogenies we inferred from 40 mtDNA-encoded proteins failed to resolve the relationships among the Zygnematales, Coleochaetales, and Charales; however, they are consistent with previous phylogenomic studies in favoring that the morphologically complex Charales are not sister to land plants.

View Article: PubMed Central - PubMed

Affiliation: Institut de Biologie Intégrative et des Systèmes, Département de Biochimie, de Microbiologie et de Bio-Informatique, Université Laval, Québec, Canada.

ABSTRACT
Six monophyletic groups of charophycean green algae are recognized within the Streptophyta. Although incongruent with earlier studies based on genes from three cellular compartments, chloroplast and nuclear phylogenomic analyses have resolved identical relationships among these groups, placing the Zygnematales or the Zygnematales + Coleochaetales as sister to land plants. The present investigation aimed at determining whether this consensus view is supported by the mitochondrial genome and at gaining insight into mitochondrial DNA (mtDNA) evolution within and across streptophyte algal lineages and during the transition toward the first land plants. We present here the newly sequenced mtDNAs of representatives of the Klebsormidiales (Entransia fimbriata and Klebsormidium spec.) and Zygnematales (Closterium baillyanum and Roya obtusa) and compare them with their homologs in other charophycean lineages as well as in selected embryophyte and chlorophyte lineages. Our results indicate that important changes occurred at the levels of genome size, gene order, and intron content within the Zygnematales. Although the representatives of the Klebsormidiales display more similarity in genome size and intron content, gene order seems more fluid and gene losses more frequent than in other charophycean lineages. In contrast, the two members of the Charales display an extremely conservative pattern of mtDNA evolution. Collectively, our analyses of gene order and gene content and the phylogenies we inferred from 40 mtDNA-encoded proteins failed to resolve the relationships among the Zygnematales, Coleochaetales, and Charales; however, they are consistent with previous phylogenomic studies in favoring that the morphologically complex Charales are not sister to land plants.

Show MeSH
Related in: MedlinePlus