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Analyses of charophyte chloroplast genomes help characterize the ancestral chloroplast genome of land plants.

Civaň P, Foster PG, Embley MT, Séneca A, Cox CJ - Genome Biol Evol (2014)

Bottom Line: The chloroplast genome of Roya differs from other zygnematophycean chloroplasts, including the newly sequenced Mesotaenium, by having a quadripartite structure that is typical of other streptophytes.Significantly, all zygnematophycean chloroplast genomes have undergone substantial genomic rearrangement, which may be the result of ancient retroelement activity evidenced by the presence of integrase-like and reverse transcriptase-like elements in the Roya chloroplast genome.Our results corroborate the close phylogenetic relationship between Zygnematophyceae and land plants and identify 89 protein-coding genes and 22 introns present in the chloroplast genome at the time of the evolutionary transition of plants to land, all of which can be found in the chloroplast genomes of extant charophytes.

View Article: PubMed Central - PubMed

Affiliation: Centro de Ciências do Mar, Universidade do Algarve, Faro, Portugal.

ABSTRACT
Despite the significance of the relationships between embryophytes and their charophyte algal ancestors in deciphering the origin and evolutionary success of land plants, few chloroplast genomes of the charophyte algae have been reconstructed to date. Here, we present new data for three chloroplast genomes of the freshwater charophytes Klebsormidium flaccidum (Klebsormidiophyceae), Mesotaenium endlicherianum (Zygnematophyceae), and Roya anglica (Zygnematophyceae). The chloroplast genome of Klebsormidium has a quadripartite organization with exceptionally large inverted repeat (IR) regions and, uniquely among streptophytes, has lost the rrn5 and rrn4.5 genes from the ribosomal RNA (rRNA) gene cluster operon. The chloroplast genome of Roya differs from other zygnematophycean chloroplasts, including the newly sequenced Mesotaenium, by having a quadripartite structure that is typical of other streptophytes. On the basis of the improbability of the novel gain of IR regions, we infer that the quadripartite structure has likely been lost independently in at least three zygnematophycean lineages, although the absence of the usual rRNA operonic synteny in the IR regions of Roya may indicate their de novo origin. Significantly, all zygnematophycean chloroplast genomes have undergone substantial genomic rearrangement, which may be the result of ancient retroelement activity evidenced by the presence of integrase-like and reverse transcriptase-like elements in the Roya chloroplast genome. Our results corroborate the close phylogenetic relationship between Zygnematophyceae and land plants and identify 89 protein-coding genes and 22 introns present in the chloroplast genome at the time of the evolutionary transition of plants to land, all of which can be found in the chloroplast genomes of extant charophytes.

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Phylogenetic analyses. (A) Bayesian MCMC phylogenetic analyses of 83 protein-coding chloroplast genes: PhyloBayes CAT + gcpREV + Γ, marginal likelihood: −Lh = 244,645.3855. (B) Strict consensus tree of six most parsimonious trees (length 239, consistency index = 0.243, retention index = 0.786) resulting from analysis of the structural data (gene and intron content, operon structure). Numbers at nodes are posterior probabilities and nonparametric bootstrap values for (A) and (B), respectively. The nodes representing the HLPA are highlighted.
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evu061-F4: Phylogenetic analyses. (A) Bayesian MCMC phylogenetic analyses of 83 protein-coding chloroplast genes: PhyloBayes CAT + gcpREV + Γ, marginal likelihood: −Lh = 244,645.3855. (B) Strict consensus tree of six most parsimonious trees (length 239, consistency index = 0.243, retention index = 0.786) resulting from analysis of the structural data (gene and intron content, operon structure). Numbers at nodes are posterior probabilities and nonparametric bootstrap values for (A) and (B), respectively. The nodes representing the HLPA are highlighted.

Mentions: In figure 4A, a Bayesian MCMC analysis of the best-fitting model (PhyloBayes CAT + gcpREV + Γ4; −Lh = 244,645.3855) of amino acid data of the 83 proteins is presented. The tree shows strong support (>0.95 posterior probability) for the paraphyly of charophytes, with Klebsormidium branching early in the phylogenetic grade before Chara and Chaetosphaeridium, and with Zygnematophyceae as the sister group to land plants. Within the Zygnematophyceae, all relationships are strongly supported, with Mesotaenium forming the earliest-branching lineage, and Zygnema sister to a clade formed by Roya and Staurastrum. This finding is in conflict with the traditional placing of Roya in the family Mesotaeniaceae but is in agreement with other phylogenetic reconstructions of conjugating algae (Gontcharov et al. 2003; Gontcharov and Melkonian 2010). Parsimony analysis of the structural data (gene and intron content, and operon structure) identified six optimal trees (tree length 239 steps, consistency index 0.243, retention index 0.786): The strict consensus tree is presented in figure 4B. Nonparametric parsimony bootstrap analysis of the structural data poorly supports a monophyletic Zygnematophyceae (54% bootstrap proportion [BP]) with strong support for the sister-group relationship between Roya and Staurastrum (97% BP). The streptophytes as a whole are well supported (98% BP), with Mesostigma and Chlorokybus forming the earliest-branching lineage. The remaining streptophytes form a well supported (100% BP) clade within which Klebsormidium is the first diverging lineage (83%). Relationships among Chara, Chaetosphaeridium, Zygnematophyceae, and the land plant clade (itself 87% BP) are unsupported (or negligibly supported <70%), but the topology is nevertheless congruent with that of the protein tree.Fig. 4.—


Analyses of charophyte chloroplast genomes help characterize the ancestral chloroplast genome of land plants.

Civaň P, Foster PG, Embley MT, Séneca A, Cox CJ - Genome Biol Evol (2014)

Phylogenetic analyses. (A) Bayesian MCMC phylogenetic analyses of 83 protein-coding chloroplast genes: PhyloBayes CAT + gcpREV + Γ, marginal likelihood: −Lh = 244,645.3855. (B) Strict consensus tree of six most parsimonious trees (length 239, consistency index = 0.243, retention index = 0.786) resulting from analysis of the structural data (gene and intron content, operon structure). Numbers at nodes are posterior probabilities and nonparametric bootstrap values for (A) and (B), respectively. The nodes representing the HLPA are highlighted.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4007539&req=5

evu061-F4: Phylogenetic analyses. (A) Bayesian MCMC phylogenetic analyses of 83 protein-coding chloroplast genes: PhyloBayes CAT + gcpREV + Γ, marginal likelihood: −Lh = 244,645.3855. (B) Strict consensus tree of six most parsimonious trees (length 239, consistency index = 0.243, retention index = 0.786) resulting from analysis of the structural data (gene and intron content, operon structure). Numbers at nodes are posterior probabilities and nonparametric bootstrap values for (A) and (B), respectively. The nodes representing the HLPA are highlighted.
Mentions: In figure 4A, a Bayesian MCMC analysis of the best-fitting model (PhyloBayes CAT + gcpREV + Γ4; −Lh = 244,645.3855) of amino acid data of the 83 proteins is presented. The tree shows strong support (>0.95 posterior probability) for the paraphyly of charophytes, with Klebsormidium branching early in the phylogenetic grade before Chara and Chaetosphaeridium, and with Zygnematophyceae as the sister group to land plants. Within the Zygnematophyceae, all relationships are strongly supported, with Mesotaenium forming the earliest-branching lineage, and Zygnema sister to a clade formed by Roya and Staurastrum. This finding is in conflict with the traditional placing of Roya in the family Mesotaeniaceae but is in agreement with other phylogenetic reconstructions of conjugating algae (Gontcharov et al. 2003; Gontcharov and Melkonian 2010). Parsimony analysis of the structural data (gene and intron content, and operon structure) identified six optimal trees (tree length 239 steps, consistency index 0.243, retention index 0.786): The strict consensus tree is presented in figure 4B. Nonparametric parsimony bootstrap analysis of the structural data poorly supports a monophyletic Zygnematophyceae (54% bootstrap proportion [BP]) with strong support for the sister-group relationship between Roya and Staurastrum (97% BP). The streptophytes as a whole are well supported (98% BP), with Mesostigma and Chlorokybus forming the earliest-branching lineage. The remaining streptophytes form a well supported (100% BP) clade within which Klebsormidium is the first diverging lineage (83%). Relationships among Chara, Chaetosphaeridium, Zygnematophyceae, and the land plant clade (itself 87% BP) are unsupported (or negligibly supported <70%), but the topology is nevertheless congruent with that of the protein tree.Fig. 4.—

Bottom Line: The chloroplast genome of Roya differs from other zygnematophycean chloroplasts, including the newly sequenced Mesotaenium, by having a quadripartite structure that is typical of other streptophytes.Significantly, all zygnematophycean chloroplast genomes have undergone substantial genomic rearrangement, which may be the result of ancient retroelement activity evidenced by the presence of integrase-like and reverse transcriptase-like elements in the Roya chloroplast genome.Our results corroborate the close phylogenetic relationship between Zygnematophyceae and land plants and identify 89 protein-coding genes and 22 introns present in the chloroplast genome at the time of the evolutionary transition of plants to land, all of which can be found in the chloroplast genomes of extant charophytes.

View Article: PubMed Central - PubMed

Affiliation: Centro de Ciências do Mar, Universidade do Algarve, Faro, Portugal.

ABSTRACT
Despite the significance of the relationships between embryophytes and their charophyte algal ancestors in deciphering the origin and evolutionary success of land plants, few chloroplast genomes of the charophyte algae have been reconstructed to date. Here, we present new data for three chloroplast genomes of the freshwater charophytes Klebsormidium flaccidum (Klebsormidiophyceae), Mesotaenium endlicherianum (Zygnematophyceae), and Roya anglica (Zygnematophyceae). The chloroplast genome of Klebsormidium has a quadripartite organization with exceptionally large inverted repeat (IR) regions and, uniquely among streptophytes, has lost the rrn5 and rrn4.5 genes from the ribosomal RNA (rRNA) gene cluster operon. The chloroplast genome of Roya differs from other zygnematophycean chloroplasts, including the newly sequenced Mesotaenium, by having a quadripartite structure that is typical of other streptophytes. On the basis of the improbability of the novel gain of IR regions, we infer that the quadripartite structure has likely been lost independently in at least three zygnematophycean lineages, although the absence of the usual rRNA operonic synteny in the IR regions of Roya may indicate their de novo origin. Significantly, all zygnematophycean chloroplast genomes have undergone substantial genomic rearrangement, which may be the result of ancient retroelement activity evidenced by the presence of integrase-like and reverse transcriptase-like elements in the Roya chloroplast genome. Our results corroborate the close phylogenetic relationship between Zygnematophyceae and land plants and identify 89 protein-coding genes and 22 introns present in the chloroplast genome at the time of the evolutionary transition of plants to land, all of which can be found in the chloroplast genomes of extant charophytes.

Show MeSH
Related in: MedlinePlus