Dataset Information

Organellar genomes of the four-toothed moss, Tetraphis pellucida.

ABSTRACT: BACKGROUND: Mosses are the largest of the three extant clades of gametophyte-dominant land plants and remain poorly studied using comparative genomic methods. Major monophyletic moss lineages are characterised by different types of a spore dehiscence apparatus called the peristome, and the most important unsolved problem in higher-level moss systematics is the branching order of these peristomate clades. Organellar genome sequencing offers the potential to resolve this issue through the provision of both genomic structural characters and a greatly increased quantity of nucleotide substitution characters, as well as to elucidate organellar evolution in mosses. We publish and describe the chloroplast and mitochondrial genomes of Tetraphis pellucida, representative of the most phylogenetically intractable and morphologically isolated peristomate lineage. RESULTS: Assembly of reads from Illumina SBS and Pacific Biosciences RS sequencing reveals that the Tetraphis chloroplast genome comprises 127,489 bp and the mitochondrial genome 107,730 bp. Although genomic structures are similar to those of the small number of other known moss organellar genomes, the chloroplast lacks the petN gene (in common with Tortula ruralis) and the mitochondrion has only a non-functional pseudogenised remnant of nad7 (uniquely amongst known moss chondromes). CONCLUSIONS: Structural genomic features exist with the potential to be informative for phylogenetic relationships amongst the peristomate moss lineages, and thus organellar genome sequences are urgently required for exemplars from other clades. The unique genomic and morphological features of Tetraphis confirm its importance for resolving one of the major questions in land plant phylogeny and for understanding the evolution of the peristome, a likely key innovation underlying the diversity of mosses. The functional loss of nad7 from the chondrome is now shown to have occurred independently in all three bryophyte clades as well as in the early-diverging tracheophyte Huperzia squarrosa.

SUBMITTER: Bell NE

PROVIDER: S-EPMC4035505 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Organellar genomes of the four-toothed moss, Tetraphis pellucida.

Bell Neil E NE Boore Jeffrey L JL Mishler Brent D BD Hyvönen Jaakko J

BMC genomics 20140519

<h4>Background</h4>Mosses are the largest of the three extant clades of gametophyte-dominant land plants and remain poorly studied using comparative genomic methods. Major monophyletic moss lineages are characterised by different types of a spore dehiscence apparatus called the peristome, and the most important unsolved problem in higher-level moss systematics is the branching order of these peristomate clades. Organellar genome sequencing offers the potential to resolve this issue through the p ...[more]

PMID: 24884426

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Project description:BackgroundThe plastid genomes of the green algal order Chlamydomonadales tend to expand their non-coding regions, but this phenomenon is poorly understood. Here we shed new light on organellar genome evolution in Chlamydomonadales by studying a previously unknown non-photosynthetic lineage. We established cultures of two new Polytoma-like flagellates, defined their basic characteristics and phylogenetic position, and obtained complete organellar genome sequences and a transcriptome assembly for one of them.ResultsWe discovered a novel deeply diverged chlamydomonadalean lineage that has no close photosynthetic relatives and represents an independent case of photosynthesis loss. To accommodate these organisms, we establish the new genus Leontynka, with two species (L. pallida and L. elongata) distinguishable through both their morphological and molecular characteristics. Notable features of the colourless plastid of L. pallida deduced from the plastid genome (plastome) sequence and transcriptome assembly include the retention of ATP synthase, thylakoid-associated proteins, the carotenoid biosynthesis pathway, and a plastoquinone-based electron transport chain, the latter two modules having an obvious functional link to the eyespot present in Leontynka. Most strikingly, the ~362 kbp plastome of L. pallida is by far the largest among the non-photosynthetic eukaryotes investigated to date due to an extreme proliferation of sequence repeats. These repeats are also present in coding sequences, with one repeat type found in the exons of 11 out of 34 protein-coding genes, with up to 36 copies per gene, thus affecting the encoded proteins. The mitochondrial genome of L. pallida is likewise exceptionally large, with its >104 kbp surpassed only by the mitogenome of Haematococcus lacustris among all members of Chlamydomonadales hitherto studied. It is also bloated with repeats, though entirely different from those in the L. pallida plastome, which contrasts with the situation in H. lacustris where both the organellar genomes have accumulated related repeats. Furthermore, the L. pallida mitogenome exhibits an extremely high GC content in both coding and non-coding regions and, strikingly, a high number of predicted G-quadruplexes.ConclusionsWith its unprecedented combination of plastid and mitochondrial genome characteristics, Leontynka pushes the frontiers of organellar genome diversity and is an interesting model for studying organellar genome evolution.

Project description:BackgroundThe C<-->U substitution types of RNA editing have been observed frequently in organellar genomes of land plants. Although various attempts have been made to explain why such a seemingly inefficient genetic mechanism would have evolved, no satisfactory explanation exists in our view. In this study, we examined editing patterns in chloroplast genomes of the hornwort Anthoceros formosae and the fern Adiantum capillus-veneris and in mitochondrial genomes of the angiosperms Arabidopsis thaliana, Beta vulgaris and Oryza sativa, to gain an understanding of the question of how RNA editing originated.ResultsWe found that 1) most editing sites were distributed at the 2nd and 1st codon positions, 2) editing affected codons that resulted in larger hydrophobicity and molecular size changes much more frequently than those with little change involved, 3) editing uniformly increased protein hydrophobicity, 4) editing occurred more frequently in ancestrally T-rich sequences, which were more abundant in genes encoding membrane-bound proteins with many hydrophobic amino acids than in genes encoding soluble proteins, and 5) editing occurred most often in genes found to be under strong selective constraint.ConclusionThese analyses show that editing mostly affects functionally important and evolutionarily conserved codon positions, codons and genes encoding membrane-bound proteins. In particular, abundance of RNA editing in plant organellar genomes may be associated with disproportionately large percentages of genes in these two genomes that encode membrane-bound proteins, which are rich in hydrophobic amino acids and selectively constrained. These data support a hypothesis that natural selection imposed by protein functional constraints has contributed to selective fixation of certain editing sites and maintenance of the editing activity in plant organelles over a period of more than four hundred millions years. The retention of genes encoding RNA editing activity may be driven by forces that shape nucleotide composition equilibrium in two organellar genomes of these plants. Nevertheless, the causes of lineage-specific occurrence of a large portion of RNA editing sites remain to be determined.

Dataset Information

Organellar genomes of the four-toothed moss, Tetraphis pellucida.

Publications

Organellar genomes of the four-toothed moss, Tetraphis pellucida.

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