Evidence for RNA editing in mitochondria of all major groups of land plants except the Bryophyta.

Abstract

RNA editing has been documented in mitochondria of higher plants, notably dicots and monocots. To determine the distribution of mitochondrial RNA editing in the plant kingdom, we have now undertaken a survey of evolutionarily distant plants. RNA editing occurs in all major groups of land plants except the Bryophyta, suggesting that this process is an ancient trait that was established before the radiation of kormophyte plants. No editing is observed in representatives of the green algae, suggesting that editing arose in early land plants after the split of the Bryophyta or has been lost selectively in both algae and mosses. In ferns several U -* C changes are observed, one of which eliminates a genomically encoded UAA termination codon and creates a functional open reading frame.RNA editing has been observed in mitochondria and chloroplasts of angiosperm plants belonging to the Dicotyledonae and Monocotyledonae (1-3). In both organelles specific cytidines of the primary transcripts are altered to uridines in the mature mRNAs. Only a few instances of editing have been found in chloroplasts (4-6), whereas numerous editing events have been documented in mitochondria of higher plants for almost all mRNAs investigated (7-11). In the more thoroughly investigated higher plant species, all of the open reading frames encoding conserved functional polypeptides appear to be edited to some extent and the total number of editing sites documented amounts to 294 in wheat (11) and to >400 in Oenothera (10). The observed effect ofthis extensive editing on the encoded polypeptide sequences suggests that many of the higher plant mitochondrial genes would not encode functionally competent products without appropriate "correction" by RNA editing.Mitochondrial RNA editing has been reported in a number of angiosperm species, including the monocots wheat and maize and the dicots Oenothera, Sorghum, Petunia, Daucus, and Arabidopsis (7-11). The observation of analogous RNA editing in both monocots and dicots suggests that the origin of this process predates the divergence of the two lineages and is generally present in angiosperms. Recently, RNA editing has also been described in the gymnosperm Thuja (12). However, none of the plant species presumed to be closer to the evolutionary origin of flowering plants has been investigated. The only mitochondrial sequence data available allowing any inference about the need of RNA editing in nonflowering plants are from two bryophytes.Analysis of protein sequences deduced from the complete genomic nucleotide sequence of the liverwort Marchantia polymorpha (13) and comparison of several cDNA and genomic DNA sequences (14) did not show any evidence of RNA editing. Genomic sequence analysis of a mitochondrial gene in the moss Physcomitrella patens (15) allows a similar deduction, suggesting that RNA editing might not occur in mitochondria of the two bryophytes.The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "adve...

Diversity and Evolution of Mitochondrial RNA Editing Systems

“…Likewise, the type of mitochondrial mRNA editing recently described in dinoflagellate mitochondria (41) has not been found in the apicomplexans, the evolutionary sister group of dinoflagellates, nor in the ciliates, which together with apicomplexans and dinoflagellates constitute the Alveolata (40). The editing observed in plant organelles (C-to-U and U-to-C) does not seem to extend beyond the land plants, as no evidence of this type of editing has been found in any of the green algal mitochondrial systems so far examined, including the charophyte algae (26,52,53), the specific sister taxon that forms a monophyletic group (Streptophyta) with land plants.…”

Evolutionary dynamics of wheat mitochondrial gene structure with special remarks on the origin and effects of RNA editing in cereals

“…In evolutionary terms, this process is significant as it masks the deleterious effect of a T-to-C mutation by editing C for U after transcription, thus enabling a gene carrying this point mutation to retain its functionality. This type of editing was once considered to have developed with the emergence of tracheophyte (vascular plants) during land plant evolution (Oda et al, 1992;Hiesel et al, 1994). A later editing study of the mt cox3 gene indicated that the C-to-U editing occurs only rarely in bryophytes, greatly increasing its site in pteridophytes and gymnosperms (Malek et al, 1996).…”

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

“…RNA-editing events involving the conversions of cytidines to uridines and uridines to cytidines have been observed in the mitochondria of angiosperms and basal land plants (Hiesel et al, 1994;Maier et al, 1996;Malek et al, 1996;Sper-Whitis et al, 1996;Giegé and Brennicke, 1999;Steinhauser et al, 1999) but appear to be absent in the subclass of complex thalloid liverworts (Marchantiidae) ) and the few algae examined to date, including Mesostigma, Chaetosphaeridium (Turmel et al, 2002c), and members of the Charales (Malek et al, 1996;Steinhauser et al, 1999). This phylogenetic distribution supports the idea that RNA editing was acquired by streptophyte mitochondria coincidentally with the emergence of land plants but was lost secondarily or extremely reduced in incidence in the Marchantiidae .…”