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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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Chloroplast genome maps of Klebsormidium flaccidum (A), Mesotaenium endlicherianum (B), and Roya anglica (C).
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evu061-F1: Chloroplast genome maps of Klebsormidium flaccidum (A), Mesotaenium endlicherianum (B), and Roya anglica (C).

Mentions: The chloroplast genome of Klebsormidium was assembled into a circular map of 176,832 bp (fig. 1A; NCBI GenBank accession number KJ461680); the third largest among currently sequenced streptophyte chloroplast genomes, smaller only than Pelargonium (Geraniaceae, Spermatophyta) and Chara (Charales, Charophyceae). The genome has a quadripartite organization, which differs from the typical embryophytic architecture by having exceptionally large IRs (51,118 bp each), a greatly reduced SSC region (1,817 bp), and a relatively shorter LSC region (72,779 bp). The expanded IR regions contain both small (rrn16) and large (rrn23) ribosomal RNA (rRNA) genes, seven tRNA genes typically found in streptophyte IRs, plus 23 additional protein-coding genes typically located in single-copy regions (fig. 2). Most remarkably, the rrn5 gene (5S rRNA) and the region homologous to the rrn4.5 gene in embryophytes (4.5S rRNA—in nonembryophyte streptophytes, the rrn4.5 gene-coding region forms an integral part of the 3′-end of the 23S ribosomal subunit) are absent from the genome (supplementary fig. S2, Supplementary Material online). The SSC region contains only a single gene (ccsA), whereas 59 protein-coding genes, and 21 tRNA genes, reside in the LSC region. Six ribosomal protein genes (rpl14, rpl16, rpl23, rps3, rps15, and rps16) usually present in streptophyte chloroplast genomes are missing, as are several other protein-coding genes (fig. 3). Two genes in the Klebsormidium genome, rps12 and psbA, require transsplicing for correct protein translation. In total, genes coding for two rRNA, 28 tRNA, and 82 proteins were identified in the Klebsormidium chloroplast genome. The GC content of the genome is relatively high (42%) compared among streptophytes (average 37%) but differs substantially between the IR and single-copy regions (46.0% and 36.5%, respectively). Mean intergenic spacer length was 358 bp (52,071 bp in total), with two conspicuous exceptions (6,340 and 4,231 bp). These two extended intergenic regions contain three unidentified ORFs (6,063, 1,785, and 1,425 bp), which had no strong matches (E value < 1e-4) among BLASTp searches of the refseq database or the custom ORF library. Group II introns were found in seven genes (table 2) and account for 3.7% of the total genome length. By comparison to the genome of Chara (Charophyceae) which has a larger overall size, the proportion of intergenic spacers and introns is several times lower, indicating that the large genome size of Klebsormidium can be attributed mainly to large IR regions.Fig. 1.—


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)

Chloroplast genome maps of Klebsormidium flaccidum (A), Mesotaenium endlicherianum (B), and Roya anglica (C).
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

evu061-F1: Chloroplast genome maps of Klebsormidium flaccidum (A), Mesotaenium endlicherianum (B), and Roya anglica (C).
Mentions: The chloroplast genome of Klebsormidium was assembled into a circular map of 176,832 bp (fig. 1A; NCBI GenBank accession number KJ461680); the third largest among currently sequenced streptophyte chloroplast genomes, smaller only than Pelargonium (Geraniaceae, Spermatophyta) and Chara (Charales, Charophyceae). The genome has a quadripartite organization, which differs from the typical embryophytic architecture by having exceptionally large IRs (51,118 bp each), a greatly reduced SSC region (1,817 bp), and a relatively shorter LSC region (72,779 bp). The expanded IR regions contain both small (rrn16) and large (rrn23) ribosomal RNA (rRNA) genes, seven tRNA genes typically found in streptophyte IRs, plus 23 additional protein-coding genes typically located in single-copy regions (fig. 2). Most remarkably, the rrn5 gene (5S rRNA) and the region homologous to the rrn4.5 gene in embryophytes (4.5S rRNA—in nonembryophyte streptophytes, the rrn4.5 gene-coding region forms an integral part of the 3′-end of the 23S ribosomal subunit) are absent from the genome (supplementary fig. S2, Supplementary Material online). The SSC region contains only a single gene (ccsA), whereas 59 protein-coding genes, and 21 tRNA genes, reside in the LSC region. Six ribosomal protein genes (rpl14, rpl16, rpl23, rps3, rps15, and rps16) usually present in streptophyte chloroplast genomes are missing, as are several other protein-coding genes (fig. 3). Two genes in the Klebsormidium genome, rps12 and psbA, require transsplicing for correct protein translation. In total, genes coding for two rRNA, 28 tRNA, and 82 proteins were identified in the Klebsormidium chloroplast genome. The GC content of the genome is relatively high (42%) compared among streptophytes (average 37%) but differs substantially between the IR and single-copy regions (46.0% and 36.5%, respectively). Mean intergenic spacer length was 358 bp (52,071 bp in total), with two conspicuous exceptions (6,340 and 4,231 bp). These two extended intergenic regions contain three unidentified ORFs (6,063, 1,785, and 1,425 bp), which had no strong matches (E value < 1e-4) among BLASTp searches of the refseq database or the custom ORF library. Group II introns were found in seven genes (table 2) and account for 3.7% of the total genome length. By comparison to the genome of Chara (Charophyceae) which has a larger overall size, the proportion of intergenic spacers and introns is several times lower, indicating that the large genome size of Klebsormidium can be attributed mainly to large IR regions.Fig. 1.—

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