A trans -splicing group I intron and tRNA-hyperediting in the mitochondrial genome of the lycophyte Isoetes engelmannii

Abstract

Plant mitochondrial genomes show much more evolutionary plasticity than those of animals. We analysed the first mitochondrial DNA (mtDNA) of a lycophyte, the quillwort Isoetes engelmannii, which is separated from seed plants by more than 350 million years of evolution. The Isoetes mtDNA is particularly rich in recombination events, and chloroplast as well as nuclear DNA inserts document the incorporation of foreign sequences already in this most ancestral vascular plant lineage. On the other hand, particularly small group II introns and short intergenic regions reveal a tendency of evolution towards a compact mitochondrial genome. RNA editing reaches extreme levels exceeding 100 pyrimidine exchanges in individual mRNAs and, hitherto unobserved in such frequency, also in tRNAs with 18 C-to-U conversions in the tRNA for proline. In total, some 1500 sites of RNA editing can be expected for the Isoetes mitochondrial transcriptome. As a unique molecular novelty, the Isoetes cox1 gene requires trans-splicing via a discontinuous group I intron demonstrating disrupted, but functional, RNAs for yet another class of natural ribozymes.

Monilophyte mitochondrial rps1 genes carry a unique group II intron that likely originated from an ancient paralog in rpl2

“…2). The rpl2 gene is absent altogether from the mtDNAs of the lycophytes Isoetes engelmannii and Selaginella moellendorffii (Grewe et al 2009;Hecht et al 2011). Alignment of the flanking exon sequences with a wider sequence sampling allowed us to label the tracheophyte rpl2 intron as rpl2i846g2 to indicate the insertion site behind the upstream coding nucleotide of Marchantia polymorpha as a reference, as proposed previously (Dombrovska and Qiu 2004).…”

“…The major hindrance for straightforward assemblies of many vascular plant mitochondrial DNAs is their high recombinational activity, often producing complex mtDNA structures with alternative coexisting gene arrangements, made all the more difficult by the large mitochondrial genome sizes in many cases. The particular complex heavily recombining mtDNAs of some lycophytes are an example for the former (Grewe et al 2009;Hecht et al 2011). The mtDNAs of angiosperms like Amborella trichopoda, the Cucurbitaceae or in the genus Silene, which may easily exceed one or even 10 Mbp, and accordingly the genome sizes of most free-living bacteria, are an example for the latter (Ward et al 1981;Alverson et al 2010Alverson et al , 2011Rodríguez-Moreno et al 2011).…”

“…The rpl2 gene is present in the mitochondrial genomes of liverworts, mosses, the lycophyte Phlegmariurus squarrosus (Liu et al 2012), in monilophytes (Knie et al 2015), and in most spermatophytes (Adams et al 2001(Adams et al , 2002Adams and Palmer 2003). In hornworts (Li et al 2009;Xue et al 2010), lycophytes Isoetes engelmannii (Grewe et al 2009 and Selaginella moellendorffii (Hecht et al 2011) rpl2 genes are absent from the mtDNA, indicating transfer to the nucleus. Intron rpl2i846g2 is present in all tracheophytes where rpl2 is retained in the mtDNA with the exception of independent losses in Mimulus guttatus (Mower et al 2012) and Equisetum bogotense (Knie et al 2015).…”

Extensive Loss of RNA Editing Sites in Rapidly Evolving Silene Mitochondrial Genomes: Selectionvs. Retroprocessing as the Driving Force

“…Outside seed plants, the moss Physcomitrella patens has only 11 edited sites in the mitochondrial genome, and the liverwort Marchantia polymorpha appears to have lost RNA editing altogether (Rü dinger et al 2008(Rü dinger et al , 2009). In contrast, other bryophytes, lycophytes, and ferns exhibit frequent mitochondrial editing (Malek et al 1996;Grewe et al 2009;Li et al 2009), while the only two nonseed plant chloroplast genomes examined (from one hornwort and one fern) also have high levels of editing (Kugita et al 2003;Wolf et al 2004).…”

“…Accordingly, neutral and nonadaptive models for the proliferation of RNA editing have also been proposed Fiebig et al 2004;Lynch et al 2006). C-to-U RNA editing appears to have evolved in a recent common ancestor of land plants, but the frequency of editing varies dramatically across lineages and between genomes (Turmel et al 2003;Salone et al 2007;Grewe et al 2009). Seed plants experience relatively frequent editing in mitochondrial genes with $400 sites per species (.1% of all coding sequence) in the few angiosperms examined so far (e.g., Giege and Brennicke 1999) and even higher rates inferred in gymnosperms (Lu et al 1998;Chaw et al 2008;Ran et al 2010).…”