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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 CAT + Γ4 model using a data set of 9,013 positions assembled from 40 mtDNA-encoded proteins. 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 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.
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evt135-F7: Majority-rule consensus tree inferred by PhyloBayes under the CAT + Γ4 model using a data set of 9,013 positions assembled from 40 mtDNA-encoded proteins. 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 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.

Mentions: Regardless of the method of analysis and the model of sequence evolution used, we observed with high BP support that the Mesostigma + Chlorokybus clade occupies the first branch of the Streptophyta and that the clade formed by the two klebsormidialean green algae represents the second deepest divergence (fig. 7). In contrast, the relationships among the Coleochaetales, Zygnematales, and Charales were influenced by the model used. The ML analyses under the LG + Γ4 and GTR + Γ4 models as well as the BI phylogeny under the CAT + Γ4 model favored the placements of the Charales as sister to the land plants and of the Zygnematales as sister to the Charales + land plants clade (T1 topology). On the other hand, the BI analysis done under the CATGTR + Γ4 model favored a sister group relationship between the Zygnematales and land plants and placed the Charales just before the divergence of the Zygnematales (T2 topology), albeit BP support for these positions was weak. Use of the best-fitting model not only lowered the frequency with which the T1 topology was detected among the bootstrap pseudoreplicates but also increased the frequencies of the alternative topologies T3 and T4 in which the Charales diverged earlier than the Coleochaetales and Zygnematales (table 2). The sister group to all land plants is the Coleochaetales + Zygnematales clade in T3, whereas it is the Zygnematales in T4. Regarding the relationships among land plants, the method of analysis used was found to influence the branching order of the three major bryophyte lineages. Consistent with previously reported phylogenies inferred from multiple genes (Qiu et al. 2006), the liverworts are sister to all other land plants in the mitochondrial trees constructed with the BI method (CATGTR + Γ4 and CAT + Γ4 models); however, both the liverworts and the mosses are united in the same clade in the ML trees (GTR + Γ4 and LG + Γ4 models).Fig. 7.—


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 CAT + Γ4 model using a data set of 9,013 positions assembled from 40 mtDNA-encoded proteins. 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 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.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

evt135-F7: Majority-rule consensus tree inferred by PhyloBayes under the CAT + Γ4 model using a data set of 9,013 positions assembled from 40 mtDNA-encoded proteins. 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 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.
Mentions: Regardless of the method of analysis and the model of sequence evolution used, we observed with high BP support that the Mesostigma + Chlorokybus clade occupies the first branch of the Streptophyta and that the clade formed by the two klebsormidialean green algae represents the second deepest divergence (fig. 7). In contrast, the relationships among the Coleochaetales, Zygnematales, and Charales were influenced by the model used. The ML analyses under the LG + Γ4 and GTR + Γ4 models as well as the BI phylogeny under the CAT + Γ4 model favored the placements of the Charales as sister to the land plants and of the Zygnematales as sister to the Charales + land plants clade (T1 topology). On the other hand, the BI analysis done under the CATGTR + Γ4 model favored a sister group relationship between the Zygnematales and land plants and placed the Charales just before the divergence of the Zygnematales (T2 topology), albeit BP support for these positions was weak. Use of the best-fitting model not only lowered the frequency with which the T1 topology was detected among the bootstrap pseudoreplicates but also increased the frequencies of the alternative topologies T3 and T4 in which the Charales diverged earlier than the Coleochaetales and Zygnematales (table 2). The sister group to all land plants is the Coleochaetales + Zygnematales clade in T3, whereas it is the Zygnematales in T4. Regarding the relationships among land plants, the method of analysis used was found to influence the branching order of the three major bryophyte lineages. Consistent with previously reported phylogenies inferred from multiple genes (Qiu et al. 2006), the liverworts are sister to all other land plants in the mitochondrial trees constructed with the BI method (CATGTR + Γ4 and CAT + Γ4 models); however, both the liverworts and the mosses are united in the same clade in the ML trees (GTR + Γ4 and LG + Γ4 models).Fig. 7.—

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