Abstract

BackgroundRNA editing by C-to-U conversions is nearly omnipresent in land plant chloroplasts and mitochondria, where it mainly serves to reconstitute conserved codon identities in the organelle mRNAs. Reverse U-to-C RNA editing in contrast appears to be restricted to hornworts, some lycophytes, and ferns (monilophytes). A well-resolved monilophyte phylogeny has recently emerged and now allows to trace the side-by-side evolution of both types of pyrimidine exchange editing in the two endosymbiotic organelles.ResultsOur study of RNA editing in four selected mitochondrial genes show a wide spectrum of divergent RNA editing frequencies including a dominance of U-to-C over the canonical C-to-U editing in some taxa like the order Schizaeales. We find that silent RNA editing leaving encoded amino acids unchanged is highly biased with more than ten-fold amounts of silent C-to-U over U-to-C edits. In full contrast to flowering plants, RNA editing frequencies are low in early-branching monilophyte lineages but increase in later emerging clades. Moreover, while editing rates in the two organelles are usually correlated, we observe uncoupled evolution of editing frequencies in fern mitochondria and chloroplasts. Most mitochondrial RNA editing sites are shared between the recently emerging fern orders whereas chloroplast editing sites are mostly clade-specific. Finally, we observe that chloroplast RNA editing appears to be completely absent in horsetails (Equisetales), the sister clade of all other monilophytes.ConclusionsC-to-U and U-to-C RNA editing in fern chloroplasts and mitochondria follow disinct evolutionary pathways that are surprisingly different from what has previously been found in flowering plants. The results call for careful differentiation of the two types of RNA editing in the two endosymbiotic organelles in comparative evolutionary studies.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0707-z) contains supplementary material, which is available to authorized users.

Highlights

  • RNA editing by C-to-U conversions is nearly omnipresent in land plant chloroplasts and mitochondria, where it mainly serves to reconstitute conserved codon identities in the organelle mRNAs

  • Mitochondrial RNA editing in monilophytes Our mitochondrial RNA editing analysis was based on four genes, which were previously included for phylogenetic studies in wide samplings of monilophyte taxa: atp1, nad5, rpl2, and rps1 [21, 27, 31, 32]

  • Comparison of mitochondrial and chloroplastid RNA editing For the comparison of mitochondrial and chloroplast RNA editing frequencies we investigated all available complete monilophyte chloroplast genomes

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Summary

Introduction

RNA editing by C-to-U conversions is nearly omnipresent in land plant chloroplasts and mitochondria, where it mainly serves to reconstitute conserved codon identities in the organelle mRNAs. Reverse U-to-C RNA editing in contrast appears to be restricted to hornworts, some lycophytes, and ferns (monilophytes). U-to-C editing occurs in at least some lycophytes, the quillworts (Isoetales) and the club mosses (Lycopodiales) [10, 22,23,24]. It is surprisingly absent in Selaginellales, the third lycophyte order, despite having record numbers of C-to-U editing in both mitochondria and chloroplasts [12, 16]

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