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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 group II introns among the chlorophyte and streptophyte mtDNAs examined in this study. The presence of a cis-spliced intron containing an ORF is denoted by a dark blue box, whereas the presence of a cis-spliced intron lacking an ORF is denoted by a lighter blue box. Trans-spliced introns are represented by purple boxes. Intron insertion sites in protein-coding and tRNA genes are given relative to the corresponding genes in Mesostigma mtDNA; insertion sites in rns and rnl are given relative to the Escherichia coli 16S and 23S rRNAs, respectively. For each insertion site, the position corresponding to the nucleotide immediately preceding the intron is reported.
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evt135-F4: Distribution of group II introns among the chlorophyte and streptophyte mtDNAs examined in this study. The presence of a cis-spliced intron containing an ORF is denoted by a dark blue box, whereas the presence of a cis-spliced intron lacking an ORF is denoted by a lighter blue box. Trans-spliced introns are represented by purple boxes. Intron insertion sites in protein-coding and tRNA genes are given relative to the corresponding genes in Mesostigma mtDNA; insertion sites in rns and rnl are given relative to the Escherichia coli 16S and 23S rRNAs, respectively. For each insertion site, the position corresponding to the nucleotide immediately preceding the intron is reported.

Mentions: In contrast to their land plant counterparts, charophycean mtDNAs are extremely variable in intron content (table 1 and figs. 3 and 4). All the introns identified so far in charophycean and bryophyte genomes, except for two group II introns in the tightly packed mtDNA of Mesostigma viride, are cis-spliced. Charophycean group I and group II introns lie at 37 and 44 distinct genomic sites (in 8 and 24 genes), respectively. Even within individual charophycean lineages, there are sharp differences in intron content. For instance, within the Zygnematales, the Closterium and Roya mtDNAs harbor as many as 31 introns and as few as two introns, respectively; the latter, which are both inserted into tRNA genes and belong to the group II family, are conserved between the two zygnematalean taxa and are also present in other charophycean or bryophyte lineages. Within the Klebsormidiales, the five Entransia and nine Klebsormidium introns share no homolog, although similar introns reside at identical insertion sites in other charophycean mtDNAs. Moreover, the mtDNAs of the charalean Chara (27 introns) and Nitella (20 introns), both of which contain numerous group I and group II introns, have in common a high proportion of group II introns but share only two group I introns at the same sites.Fig. 3.—


Tracing the evolution of streptophyte algae and their mitochondrial genome.

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

Distribution of group II introns among the chlorophyte and streptophyte mtDNAs examined in this study. The presence of a cis-spliced intron containing an ORF is denoted by a dark blue box, whereas the presence of a cis-spliced intron lacking an ORF is denoted by a lighter blue box. Trans-spliced introns are represented by purple boxes. Intron insertion sites in protein-coding and tRNA genes are given relative to the corresponding genes in Mesostigma mtDNA; insertion sites in rns and rnl are given relative to the Escherichia coli 16S and 23S rRNAs, respectively. For each insertion site, the position corresponding to the nucleotide immediately preceding the intron is reported.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

evt135-F4: Distribution of group II introns among the chlorophyte and streptophyte mtDNAs examined in this study. The presence of a cis-spliced intron containing an ORF is denoted by a dark blue box, whereas the presence of a cis-spliced intron lacking an ORF is denoted by a lighter blue box. Trans-spliced introns are represented by purple boxes. Intron insertion sites in protein-coding and tRNA genes are given relative to the corresponding genes in Mesostigma mtDNA; insertion sites in rns and rnl are given relative to the Escherichia coli 16S and 23S rRNAs, respectively. For each insertion site, the position corresponding to the nucleotide immediately preceding the intron is reported.
Mentions: In contrast to their land plant counterparts, charophycean mtDNAs are extremely variable in intron content (table 1 and figs. 3 and 4). All the introns identified so far in charophycean and bryophyte genomes, except for two group II introns in the tightly packed mtDNA of Mesostigma viride, are cis-spliced. Charophycean group I and group II introns lie at 37 and 44 distinct genomic sites (in 8 and 24 genes), respectively. Even within individual charophycean lineages, there are sharp differences in intron content. For instance, within the Zygnematales, the Closterium and Roya mtDNAs harbor as many as 31 introns and as few as two introns, respectively; the latter, which are both inserted into tRNA genes and belong to the group II family, are conserved between the two zygnematalean taxa and are also present in other charophycean or bryophyte lineages. Within the Klebsormidiales, the five Entransia and nine Klebsormidium introns share no homolog, although similar introns reside at identical insertion sites in other charophycean mtDNAs. Moreover, the mtDNAs of the charalean Chara (27 introns) and Nitella (20 introns), both of which contain numerous group I and group II introns, have in common a high proportion of group II introns but share only two group I introns at the same sites.Fig. 3.—

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