The Mitochondrial Genome of the Gymnosperm Cycas taitungensis Contains a Novel Family of Short Interspersed Elements, Bpu Sequences, and Abundant RNA Editing Sites

Research Center for Biodiversity, Academia Sinica, Taipei, Taiwan.
Molecular Biology and Evolution (Impact Factor: 9.11). 04/2008; 25(3):603-15. DOI: 10.1093/molbev/msn009
Source: PubMed


The mtDNA of Cycas taitungensis is a circular molecule of 414,903 bp, making it 2- to 6-fold larger than the known mtDNAs of charophytes and bryophytes, but similar to the average of 7 elucidated angiosperm mtDNAs. It is characterized by abundant RNA editing sites (1,084), more than twice the number found in the angiosperm mtDNAs. The A + T content of Cycas mtDNA is 53.1%, the lowest among known land plants. About 5% of the Cycas mtDNA is composed of a novel family of mobile elements, which we designated as "Bpu sequences." They share a consensus sequence of 36 bp with 2 terminal direct repeats (AAGG) and a recognition site for the Bpu 10I restriction endonuclease (CCTGAAGC). Comparison of the Cycas mtDNA with other plant mtDNAs revealed many new insights into the biology and evolution of land plant mtDNAs. For example, the noncoding sequences in mtDNAs have drastically expanded as land plants have evolved, with abrupt increases appearing in the bryophytes, and then in the seed plants. As a result, the genomic organizations of seed plant mtDNAs are much less compact than in other plants. Also, the Cycas mtDNA appears to have been exempted from the frequent gene loss observed in angiosperm mtDNAs. Similar to the angiosperms, the 3 Cycas genes nad1, nad2, and nad5 are disrupted by 5 group II intron squences, which have brought the genes into trans-splicing arrangements. The evolutionary origin and invasion/duplication mechanism of the Bpu sequences in Cycas mtDNA are hypothesized and discussed.

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    • ") but also in gymnosperms (Chaw et al., 2008), likely owing to a recombination event disrupting its group II intron nad2i542g2 into a trans-splicing status early in the spermatophyte stem lineage (Fig. 1). Cis-splicing orthologues of nad2i542g2 were identified in the ferns Asplenium nidus and Marsilea drummondii (Malek and Knoop, 1998; Malek et al., 1997) and subsequently also in the lycophytes Isoetes engelmannii (Grewe et al., 2009) and Selaginella moellendorffii (Hecht et al., 2011) clearly demonstrating the cis-arrangement of nad2i542g2 to be the evolutionary ancestral, plesiomorphic state as expected. "
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    ABSTRACT: The "Monilophyte" clade comprising ferns, horsetails, and whisk ferns receives unequivocal support from molecular data as the sister clade to seed plants. However, the branching order of its earliest emerging lineages, the Equisetales (horsetails), the Marattiales, the Ophioglossales/Psilotales and the large group of leptosporangiate ferns has remained dubious. We investigated the mitochondrial nad2 and rpl2 genes as two new, intron-containing loci for a wide sampling of taxa. We found that both group II introns - nad2i542g2 and rpl2i846g2 - are universally present among monilophytes. Both introns have orthologues in seed plants where nad2i542g2 has evolved into a trans-arrangement. In contrast, and despite substantial size extensions to more than 5 kb in Psilotum, nad2i542g2 remains cis-arranged in the monilophytes. For phylogenetic analyses, we filled taxonomic gaps in previously investigated mitochondrial (atp1, nad5) and chloroplast (atpA, atpB, matK, rbcL, rps4) loci and created a 9-gene matrix that also included the new mitochondrial nad2 and rpl2 loci. We extended the taxon sampling with two taxa each for all land plant outgroups (liverworts, mosses, hornworts, lycophytes and seed plants) to minimize the risk of phylogenetic artefacts. We ultimately obtained a well-supported molecular phylogeny placing Marattiales as sister to leptosporangiate ferns and horsetails as sister to all remaining monilophytes. In addition, an indel in an exon of the here introduced rpl2 locus independently supports the placement of horsetails. We conclude that under dense taxon sampling, phylogenetic information from a prudent choice of loci is currently superior to character-rich phylogenomic approaches at low taxon sampling. As here shown the selective choice of loci and taxa enabled us to resolve the long-enigmatic diversifications of the earliest monilophyte lineages. Copyright © 2015. Published by Elsevier Inc.
    Molecular Phylogenetics and Evolution 05/2015; 90. DOI:10.1016/j.ympev.2015.05.008 · 3.92 Impact Factor
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    • "Page: 875 862–878 2014 not clear whether shifts in GC composition determine synonymous codon usage or whether biases for specific codons shape the GC composition (Knight et al. 2001; Sharp et al. 2010; Behura and Severson 2013). Recent phylogenetic analyses using genomic-scale mtDNA or cpDNA data, focusing on land plants (Chaw et al. 2008; Chang and Graham 2011), ferns (Rai and Graham 2010), angiosperms (Jansen et al., 2007), or broad sampling of one group of angiosperms (Moore et al. 2010; Barrett et al. 2012) failed to test the potential bias introduced by the above parameters shaping the evolution of individual loci. We suggest that inferences from genomic data should always assess the effect of saturation, and composition and codonusage heterogeneity—processes whose effects are not independent but potentially correlated—particularly if the divergences of interest are ancient (e.g., origin of land plants) or the genomes evolving fast (e.g., nuclear exomes). "
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    ABSTRACT: Phylogenetic analyses using concatenation of genomic-scale data have been seen as the panacea for resolving the incongruences among inferences from few or single genes. However, phylogenomics may also suffer from systematic errors, due to the, perhaps cumulative, effects of saturation, among-taxa compositional (GC content) heterogeneity, or codon-usage bias plaguing the individual nucleotide loci that are concatenated. Here we provide an example of how these factors affect the inferences of the phylogeny of early land plants based on mitochondrial genomic data. Mitochondrial sequences evolve slowly in plants and hence are thought to be suitable for resolving deep relationships. We newly assembled mitochondrial genomes from 20 bryophytes, complemented these with 40 other streptophytes (land plants plus algal outgroups), compiling a data matrix of 60 taxa and 41 mitochondrial genes. Homogeneous analyses of the concatenated nucleotide data resolve mosses as sister-group to the remaining land plants. However, the corresponding translated amino acid data support the liverwort lineage in this position. Both results receive weak to moderate support in maximum likelihood analyses, but strong support in Bayesian inferences. Tests of alternative hypotheses using either nucleotide or amino-acid data provide implicit support for their respective optimal topologies, and clearly reject the hypotheses that bryophytes are monophyletic, liverworts and mosses share a unique common ancestor, or hornworts are sister to the remaining land plants. We determined that land plant lineages differ in their nucleotide composition, and in their usage of synonymous codon variants. Composition heterogeneous Bayesian analyses employing a non-stationary model that accounts for variation in among-lineage composition, and inferences from degenerated nucleotide data that avoids the effects of synonymous substitutions that underlie codon-usage bias, again recovered liverworts being sister to the remaining land plants but without support. These analyses indicate that the inference of an early-branching moss lineage based on the nucleotide data is caused by convergent compositional biases. Accommodating among-site amino acid compositional heterogeneity (CAT-model) yields no support for the optimal resolution of liverwort as sister to the rest of land plants, suggesting that the robust inference of the liverwort position in homogeneous analyses may be due in part to compositional biases among sites. All analyses support a paraphyletic bryophytes with hornworts composing the sister group to tracheophytes. We conclude that while genomic data may generate highly supported phylogenetic trees, these inferences may be artifacts. We suggest that phylogenomic analyses should assess the possible impact of potential biases through comparisons of protein-coding gene data and their amino-acid translations by evaluating the impact of substitutional saturation, synonymous substitutions, and compositional biases through data deletion strategies and by analyzing the data using heterogeneous composition models. We caution against relying on any one presentation of the data (nucleotide or amino acid) or any one type of analysis even when analyzing large-scale data sets, no matter how well-supported, without fully exploring the effects of substitution models.
    Systematic Biology 07/2014; DOI:10.1093/sysbio/syu049 · 14.39 Impact Factor
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    • "Maturase content is much more variable in land plant mitochondrial genomes (Mower et al. 2012b). The most well-known plant mitochondrial maturase (matR, encoded by intron nad1i728) is broadly distributed in most vascular plants, some hornworts, and some mosses (Dombrovska and Qiu 2004), and it is the only maturase found in the mitochondrial genomes of seed plants such as the crucifer Arabidopsis thaliana and the cycad Cycas taitungensis (Unseld et al. 1997; Chaw et al. 2008). The maturase in intron atp9i87, originally identified in the liverwort Marchantia polymorpha (Oda et al. 1992), was recently shown to also be present in the lycophyte Isoetes engelmannii (Grewe et al. 2011). "
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    ABSTRACT: Among land plants, mitochondrial and plastid group II introns occasionally encode proteins called maturases that are important for splicing. Angiosperm nuclear genomes also encode maturases that are targeted to the organelles, but it is not known whether nucleus-encoded maturases exist in other land plant lineages. To examine the evolutionary diversity and history of this essential gene family, we searched for maturase homologs in recently sequenced nuclear and mitochondrial genomes from diverse land plants. We found that maturase content in mitochondrial genomes is highly lineage specific, such that orthologous maturases are rarely shared among major land plant groups. The presence of numerous mitochondrial pseudogenes in the mitochondrial genomes of several species implies that the sporadic maturase distribution is due to frequent inactivation and eventual loss over time. We also identified multiple maturase paralogs in the nuclear genomes of the lycophyte Selaginella moellendorffii, the moss Physcomitrella patens, and the representative angiosperm Vitis vinifera. Phylogenetic analyses of organelle- and nucleus-encoded maturases revealed that the nuclear maturase genes in angiosperms, lycophytes, and mosses arose by multiple shared and independent transfers of mitochondrial paralogs to the nuclear genome during land plant evolution. These findings indicate that plant mitochondrial maturases have experienced a surprisingly dynamic history due to a complex interaction of multiple evolutionary forces that affect the rates of maturase gain, retention, and loss.
    Journal of Molecular Evolution 08/2013; 77(1-2). DOI:10.1007/s00239-013-9579-7 · 1.68 Impact Factor
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