Mosses share mitochondrial group II introns with flowering plants, not with liverworts

Abstract

Extant bryophytes are regarded as the closest living relatives of the first land plants, but relationships among the bryophyte classes (mosses, liverworts and hornworts) and between them and other embryophytes have remained unclear. We have recently found that plant mitochondrial genes with positionally stable introns are well suited for addressing questions of plant phylogeny at a deep level. To explore further data sets we have chosen to investigate the mitochondrial genes nad4 and nad7, which are particularly rich in intron sequences. Surprisingly, we find that in these genes mosses share three group II introns with flowering plants, but none with the liverwort Marchantia polymorpha or other liverworts investigated here. In mitochondria of Marchantia, nad7 is a pseudogene containing stop codons, but nad7 appears as a functional mitochondrial gene in mosses, including the isolated genus Takakia. We observe the necessity for strikingly frequent C-to-U RNA editing to reconstitute conserved codons in Takakia when compared to other mosses. The findings underline the great evolutionary distances among the bryophytes as the presumptive oldest division of land plants. A scenario involving differential intron gains from fungal sources in what are perhaps the two earliest diverging land plant lineages, liverworts and other embryophytes, is discussed. With their positionally stable introns, nad4 and nad7 represent novel marker genes that may permit a detailed phylogenetic resolution of early clades of land plants.

The Mitochondrial Genome of Chara vulgaris: Insights into the Mitochondrial DNA Architecture of the Last Common Ancestor of Green Algae and Land Plants[W]

“…All of the 32 introns in Marchantia mtDNA, with the exception of the nad2 intron, reside at distinct positions relative to the 20 to 23 introns in angiosperm mtDNAs, suggesting that most, if not all, of the liverwort introns arose independently from their angiosperm counterparts. The distribution patterns of mitochondrial introns among basal land plants (both bryophytes and vascular plants) are consistent with this hypothesis (Malek et al, 1997;Malek and Knoop, 1998;Beckert et al, 1999;Pruchner et al, 2001). The alternative hypothesis that all of the introns in the four completely sequenced land plant mtDNAs were present in the common ancestor of all land plants and that subsequently many were lost independently in early-diverging lineages appears unlikely in light of the finding that mitochondrial introns are stable in bryophytes belonging to the same class (Beckert et al, , 2001Pruchner et al, 2001) and also in both flowering and nonflowering vascular plants Qiu et al, 1998;Vangerow et al, 1999).…”

“…The distribution patterns of mitochondrial introns among basal land plants (both bryophytes and vascular plants) are consistent with this hypothesis (Malek et al, 1997;Malek and Knoop, 1998;Beckert et al, 1999;Pruchner et al, 2001). The alternative hypothesis that all of the introns in the four completely sequenced land plant mtDNAs were present in the common ancestor of all land plants and that subsequently many were lost independently in early-diverging lineages appears unlikely in light of the finding that mitochondrial introns are stable in bryophytes belonging to the same class (Beckert et al, , 2001Pruchner et al, 2001) and also in both flowering and nonflowering vascular plants Qiu et al, 1998;Vangerow et al, 1999). A notable exception is the group-I intron in cox1 that has been identified in 48 of the 335 genera of angiosperms examined in the course of an extensive DNA gel blot survey Cho and Palmer, 1999).…”

The chloroplast and mitochondrial genome sequences of the charophyte Chaetosphaeridium globosum : Insights into the timing of the events that restructured organelle DNAs within the green algal lineage that led to land plants

“…Mesostigma and land-plant mtDNAs share no introns, and only 1 of the 32 introns in Marchantia mtDNA (18) is conserved in A. thaliana (19) and B. vulgaris mtDNAs (20), suggesting that most of the liverwort mitochondrial introns have arisen independently from those present in angiosperms. The distribution patterns of mitochondrial introns among basal land plants are consistent with this hypothesis and also indicate that all five trans-spliced introns conserved among angiosperm mtDNAs arose from cis-spliced intron homologs (21)(22)(23)(24)(25). RNA-editing events involving mainly the conversions of cytidine into uridine have been observed in the mitochondria of basal land plants and angiosperms (26)(27)(28)(29) as well as in their chloro-plasts (26,(30)(31)(32) but appear to be absent in both organelles of Marchantia and the few algae examined thus far.…”

RNA editing: only eleven sites are present in the Physcomitrella patens mitochondrial transcriptome and a universal nomenclature proposal

“…Extant taxa accordingly would reXect the secondary gains and losses of individual RNA editing sites in their editotypes during »450 MY of evolution. In the light of signiWcantly higher rates of RNA editing in other bryophytes, most notably in the basal moss genus Takakia; (Miyata et al 2008;Pruchner et al 2001;Sugita et al 2006), Physcomitrella would be an example of an impressive rate of back mutations, leaving behind only eleven mitochondrial and two chloroplastic editing sites.…”