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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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Total lengths of coding, intronic, and intergenic sequences in the streptophyte mtDNAs examined in this study. Note that intron-encoded genes were not considered as coding sequences but rather as intron sequences and that trans-spliced introns were not taken into account to estimate the total lengths of intron sequences because their sizes are usually not annotated in the GenBank accessions. Species names are abbreviated as in table 1.
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evt135-F1: Total lengths of coding, intronic, and intergenic sequences in the streptophyte mtDNAs examined in this study. Note that intron-encoded genes were not considered as coding sequences but rather as intron sequences and that trans-spliced introns were not taken into account to estimate the total lengths of intron sequences because their sizes are usually not annotated in the GenBank accessions. Species names are abbreviated as in table 1.

Mentions: All compared charophycean mitochondrial genomes, except the mtDNAs of Chlorokybus and of the zygnematelean Closterium, are smaller in size than their bryophyte counterparts (table 1 and fig. 1). Important differences in mitochondrial genome size are found among distinct charophycean lineages as well as within individual lineages, in particular the Mesostigma/Chlorokybus clade and the Zygnematales. In this regard, it is noteworthy that the two representatives of the Charales, Chara and Nitella, carry very similar mitochondrial genomes; these mtDNAs, which differ by only 12,447 bp, contain the same gene complement and display exactly the same gene order. Overall, the total lengths of both the intergenic and intronic regions in mtDNA changed substantially during charophycean evolution, even though the total lengths of coding regions remained similar (fig. 1). Repeated sequences account for less than 7.5% of the total mitochondrial genome size in charophyceans, the observed variation being comparable to that found in bryophyte mtDNAs (table 1).Fig. 1.—


Tracing the evolution of streptophyte algae and their mitochondrial genome.

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

Total lengths of coding, intronic, and intergenic sequences in the streptophyte mtDNAs examined in this study. Note that intron-encoded genes were not considered as coding sequences but rather as intron sequences and that trans-spliced introns were not taken into account to estimate the total lengths of intron sequences because their sizes are usually not annotated in the GenBank accessions. Species names are abbreviated as in table 1.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

evt135-F1: Total lengths of coding, intronic, and intergenic sequences in the streptophyte mtDNAs examined in this study. Note that intron-encoded genes were not considered as coding sequences but rather as intron sequences and that trans-spliced introns were not taken into account to estimate the total lengths of intron sequences because their sizes are usually not annotated in the GenBank accessions. Species names are abbreviated as in table 1.
Mentions: All compared charophycean mitochondrial genomes, except the mtDNAs of Chlorokybus and of the zygnematelean Closterium, are smaller in size than their bryophyte counterparts (table 1 and fig. 1). Important differences in mitochondrial genome size are found among distinct charophycean lineages as well as within individual lineages, in particular the Mesostigma/Chlorokybus clade and the Zygnematales. In this regard, it is noteworthy that the two representatives of the Charales, Chara and Nitella, carry very similar mitochondrial genomes; these mtDNAs, which differ by only 12,447 bp, contain the same gene complement and display exactly the same gene order. Overall, the total lengths of both the intergenic and intronic regions in mtDNA changed substantially during charophycean evolution, even though the total lengths of coding regions remained similar (fig. 1). Repeated sequences account for less than 7.5% of the total mitochondrial genome size in charophyceans, the observed variation being comparable to that found in bryophyte mtDNAs (table 1).Fig. 1.—

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