Plant-type mitochondrial RNA editing in the protist Naegleria gruberi: FIGURE 1.

Abstract

RNA editing converts hundreds of cytidines into uridines in plant mitochondrial and chloroplast transcripts. Recognition of the RNA editing sites in the organelle transcriptomes requires numerous specific, nuclear-encoded RNA-binding pentatricopeptide repeat (PPR) proteins with characteristic carboxy-terminal protein domain extensions (E/DYW) previously thought to be unique to plants. However, a small gene family of such plant-like PPR proteins of the DYW-type was recently discovered in the genome of the protist Naegleria gruberi. This raised the possibility that plant-like RNA editing may occur in this amoeboflagellate. Accordingly, we have investigated the mitochondrial transcriptome of Naegleria gruberi and here report on identification of two sites of C-to-U RNA editing in the cox1 gene and in the cox3 gene, both of which reconstitute amino acid codon identities highly conserved in evolution. An estimated 1.5 billion years of evolution separate the heterolobosean protist Naegleria from the plant lineage. The new findings either suggest horizontal gene transfer of RNA editing factors or that plant-type RNA editing is evolutionarily much more ancestral than previously thought and yet to be discovered in many other ancient eukaryotic lineages.

Two Interacting Proteins Are Necessary for the Editing of the NdhD-1 Site in Arabidopsis Plastids

“…The DYW consensus contains the cytidine deaminase signature HxE (x)nCxxC (Salone et al, 2007). In addition, the phylogenetic distribution of the DYW domain appears to exactly match the phylogenetic distribution of plant organellar RNA editing (Salone et al, 2007;Knoop, 2011;Rüdinger et al, 2011). These results supported the hypothesis that the DYW domain might contain the catalytic activity for editing in plant organelles (Salone et al, (A) Alignment of the DYW1 sequence with the DYW domain consensus .…”

Nuclear DYW-Type PPR Gene Families Diversify with Increasing RNA Editing Frequencies in Liverwort and Moss Mitochondria

“…Among several other features, the recently developed PREPACT allows automatic prediction of RNA editing sites in multiple sequence alignments or in full organelle genomes (Lenz et al 2010). The latter option has recently been used successfully to identify candidate RNA editing sites even in the mtDNA of a phylogenetic distant protist, which could subsequently be confirmed Rüdinger et al 2011a). However, RNA editing prediction with this strategy frequently proves to be too sensitive and identifies false positive candidate sites when based on individual reference sequences alone.…”

Identification of Two Pentatricopeptide Repeat Genes Required for RNA Editing and Zinc Binding by C-terminal Cytidine Deaminase-like Domains

“…The DYW domain is known to have zinc binding motifs (HXE and CXXC) (25), and analogous zinc-coordinating residues are conserved in nucleotide deaminases (26 -29). Phylogenetic analyses have shown that the distribution of PPR proteins with the DYW domain coincides with the distribution of C-to-U editing in land plants (25), in the protist, Naegleria gruberi (30,31), and possibly also in diverse lower eukaryotes such as Acanthamoeba, Physarum, Nitella, and rotifers (32). A bioinformatics analysis of the deaminase superfamily has shown that the C-terminal region exhibits structural characteristics of a deaminase domain and places the DYW deaminase domain in the deaminases superfamily (27).…”