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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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Distribution of mitochondrial gene/pseudogene pairs that are shared by at least two charophycean and two chlorophyte taxa, by at least three charophycean taxa, or by at least one charophycean and two bryophyte lineages. The presence of a gene pair is denoted by a dark blue box. A light green box refers to a gene pair in which at least one gene is missing in some lineages due to gene loss. Ancestral gene pairs, that is, gene pairs common to chlorophytes and streptophytes, are presented first. The yellow, orange, and brown colors on the left of the figure refer to derived gene pairs (synapomorphies) supporting the three current hypotheses concerning the sister group of land plants: yellow, Charales; orange, Zygnematales; brown, Coleochaetales + Zygnematales. The blue color on the left of the figure refers to the gene pairs supporting the alternative hypothesis that the Coleochaetales are sister to the Charales, Zygnematales, and land plants. Note that the 3′yejV–5′yejU pair was considered to be an ancestral linkage because it is found in the few protist lineages that have retained these genes, more specifically in the bacteria-like and gene-rich mitochondrial genomes of jakobids (Burger et al. 2013).
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evt135-F5: Distribution of mitochondrial gene/pseudogene pairs that are shared by at least two charophycean and two chlorophyte taxa, by at least three charophycean taxa, or by at least one charophycean and two bryophyte lineages. The presence of a gene pair is denoted by a dark blue box. A light green box refers to a gene pair in which at least one gene is missing in some lineages due to gene loss. Ancestral gene pairs, that is, gene pairs common to chlorophytes and streptophytes, are presented first. The yellow, orange, and brown colors on the left of the figure refer to derived gene pairs (synapomorphies) supporting the three current hypotheses concerning the sister group of land plants: yellow, Charales; orange, Zygnematales; brown, Coleochaetales + Zygnematales. The blue color on the left of the figure refers to the gene pairs supporting the alternative hypothesis that the Coleochaetales are sister to the Charales, Zygnematales, and land plants. Note that the 3′yejV–5′yejU pair was considered to be an ancestral linkage because it is found in the few protist lineages that have retained these genes, more specifically in the bacteria-like and gene-rich mitochondrial genomes of jakobids (Burger et al. 2013).

Mentions: To compare the gene organizations of the charophycean and bryophyte mtDNAs in our study group, we examined the gene pairs and gene clusters they share and also inferred a scenario of genome rearrangements. Figure 5 presents one of the two gene-pair analyses that we performed. The mtDNAs of four green algae representing early diverging lineages of the Chlorophyta (i.e., three members of the Prasinophyceae and Prototheca wickerhamii, a representative of the Trebouxiophyceae) were included in this analysis in an attempt to distinguish conserved gene clusters that predate the divergence of chlorophytes and streptophytes (i.e., ancestral clusters) from those that arose during charophycean evolution. The ancestral gene pairs appear to be more prevalent in the Klebsormidiales and Charales than in the other streptophyte lineages. With regard to the gene pairs that are streptophyte-specific, they are most abundant in the Zygnematales and Charales and their proportions in these lineages are comparable to those observed in liverworts and mosses. We identified the streptophyte-specific gene pairs (synapomorphies) that are shared exclusively between the Charales and bryophytes; between the Coleochaetales, Zygnematales, and bryophytes; and also between the Zygnematales and bryophytes in order to evaluate which of the three current hypotheses concerning the identity of the charophycean lineage(s) being sister to land plants is best supported (fig. 5, compare the gene pairs shown in different colors). The hypothesis that the Coleochaetales + Zygnematales are sister to the land plant lineage received the strongest support. In this context, it is worth pointing out that several gene pairs are uniquely shared between the Charales, Zygnematales, and land plants (fig. 5), thus providing support for a basal position of the Coleochaetales relative to these lineages. In a separate analysis, we assembled a data set of 134 gene pairs from 16 streptophytes (128 phylogenetically informative characters), in which the gene pairs were coded as binary Dollo characters (presence/absence), and used this data set to infer a phylogeny using MP (fig. 6). The majority-rule consensus tree of the bootstrap replicates resolved with weak bootstrap (BP) support the Coleochaetales and Zygnematales as sister to land plants and the Charales as sister to the Coleochaetales + Zygnematales + land plants.Fig. 5.—


Tracing the evolution of streptophyte algae and their mitochondrial genome.

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

Distribution of mitochondrial gene/pseudogene pairs that are shared by at least two charophycean and two chlorophyte taxa, by at least three charophycean taxa, or by at least one charophycean and two bryophyte lineages. The presence of a gene pair is denoted by a dark blue box. A light green box refers to a gene pair in which at least one gene is missing in some lineages due to gene loss. Ancestral gene pairs, that is, gene pairs common to chlorophytes and streptophytes, are presented first. The yellow, orange, and brown colors on the left of the figure refer to derived gene pairs (synapomorphies) supporting the three current hypotheses concerning the sister group of land plants: yellow, Charales; orange, Zygnematales; brown, Coleochaetales + Zygnematales. The blue color on the left of the figure refers to the gene pairs supporting the alternative hypothesis that the Coleochaetales are sister to the Charales, Zygnematales, and land plants. Note that the 3′yejV–5′yejU pair was considered to be an ancestral linkage because it is found in the few protist lineages that have retained these genes, more specifically in the bacteria-like and gene-rich mitochondrial genomes of jakobids (Burger et al. 2013).
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

evt135-F5: Distribution of mitochondrial gene/pseudogene pairs that are shared by at least two charophycean and two chlorophyte taxa, by at least three charophycean taxa, or by at least one charophycean and two bryophyte lineages. The presence of a gene pair is denoted by a dark blue box. A light green box refers to a gene pair in which at least one gene is missing in some lineages due to gene loss. Ancestral gene pairs, that is, gene pairs common to chlorophytes and streptophytes, are presented first. The yellow, orange, and brown colors on the left of the figure refer to derived gene pairs (synapomorphies) supporting the three current hypotheses concerning the sister group of land plants: yellow, Charales; orange, Zygnematales; brown, Coleochaetales + Zygnematales. The blue color on the left of the figure refers to the gene pairs supporting the alternative hypothesis that the Coleochaetales are sister to the Charales, Zygnematales, and land plants. Note that the 3′yejV–5′yejU pair was considered to be an ancestral linkage because it is found in the few protist lineages that have retained these genes, more specifically in the bacteria-like and gene-rich mitochondrial genomes of jakobids (Burger et al. 2013).
Mentions: To compare the gene organizations of the charophycean and bryophyte mtDNAs in our study group, we examined the gene pairs and gene clusters they share and also inferred a scenario of genome rearrangements. Figure 5 presents one of the two gene-pair analyses that we performed. The mtDNAs of four green algae representing early diverging lineages of the Chlorophyta (i.e., three members of the Prasinophyceae and Prototheca wickerhamii, a representative of the Trebouxiophyceae) were included in this analysis in an attempt to distinguish conserved gene clusters that predate the divergence of chlorophytes and streptophytes (i.e., ancestral clusters) from those that arose during charophycean evolution. The ancestral gene pairs appear to be more prevalent in the Klebsormidiales and Charales than in the other streptophyte lineages. With regard to the gene pairs that are streptophyte-specific, they are most abundant in the Zygnematales and Charales and their proportions in these lineages are comparable to those observed in liverworts and mosses. We identified the streptophyte-specific gene pairs (synapomorphies) that are shared exclusively between the Charales and bryophytes; between the Coleochaetales, Zygnematales, and bryophytes; and also between the Zygnematales and bryophytes in order to evaluate which of the three current hypotheses concerning the identity of the charophycean lineage(s) being sister to land plants is best supported (fig. 5, compare the gene pairs shown in different colors). The hypothesis that the Coleochaetales + Zygnematales are sister to the land plant lineage received the strongest support. In this context, it is worth pointing out that several gene pairs are uniquely shared between the Charales, Zygnematales, and land plants (fig. 5), thus providing support for a basal position of the Coleochaetales relative to these lineages. In a separate analysis, we assembled a data set of 134 gene pairs from 16 streptophytes (128 phylogenetically informative characters), in which the gene pairs were coded as binary Dollo characters (presence/absence), and used this data set to infer a phylogeny using MP (fig. 6). The majority-rule consensus tree of the bootstrap replicates resolved with weak bootstrap (BP) support the Coleochaetales and Zygnematales as sister to land plants and the Charales as sister to the Coleochaetales + Zygnematales + land plants.Fig. 5.—

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