A unique transcriptome: 1782 positions of RNA editing alter 1406 codon identities in mitochondrial mRNAs of the lycophyte Isoetes engelmannii

Abstract

The analysis of the mitochondrial DNA of Isoetes engelmannii as a first representative of the lycophytes recently revealed very small introns and indications for extremely frequent RNA editing. To analyze functionality of intron splicing and the extent of RNA editing in I. engelmannii, we performed a comprehensive analysis of its mitochondrial transcriptome. All 30 groups I and II introns were found to be correctly removed, showing that intron size reduction does not impede splicing. We find that mRNA editing affects 1782 sites, which lead to a total of 1406 changes in codon meanings. This includes the removal of stop codons from 23 of the 25 mitochondrial protein encoding genes. Comprehensive sequence analysis of multiple cDNAs per locus allowed classification of partially edited sites as either inefficiently edited but relevant or as non-specifically edited at mostly low frequencies. Abundant RNA editing was also found to affect tRNAs in hitherto unseen frequency, taking place at 41 positions in tRNA-precursors, including the first identification of U-to-C exchanges in two tRNA species. We finally investigated the four group II introns of the nad7 gene and could identify 27 sites of editing, most of which improve base pairing for proper secondary structure formation.

Chloroplast RNA editing going extreme: more than 3400 events of C-to-U editing in the chloroplast transcriptome of the lycophyte Selaginella uncinata

“…1). We conclude that loss of clpPi363g2 was accompanied by a recombination event involving regions of a mature clpP transcript/cDNA leading to a concomitant loss of editing events in its vicinity, similar to previously reported cases of organelle intron loss (e.g., Geiss et al 1994;Itchoda et al 2002;Lopez et al 2007;Ran et al 2010;Grewe et al 2011). Alternative explanations such as horizontal gene transfer (Hepburn et al 2012) or a pressure on intron retention exerted by RNA editing (Kagami et al 2012) must be kept in mind, however.…”

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

“…Only some RNA editing events, mostly at ''silent'' sites that leave the encoded amino acid unchanged, are often found only partially edited to varying degrees in the steady state transcript pool of plant mitochondria (e.g., Mower and Palmer 2006;Grewe et al 2011).…”

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

“…While the high numbers of It has indeed been shown conclusively that losses of editing sites occur faster than gains in angiosperm mitochondria (Mower 2007;Shields and Wolfe 1997) and chloroplasts (Tillich et al 2006). However, a different picture may emerge on larger evolutionary timescales as reflected by the dramatic increase of RNA editing frequencies in ancient clades such as the hornworts and lycophytes (Duff 2006;Grewe et al 2011;Hecht et al 2011;Sper-Whitis et al 1996). In those lineages, and possibly in yet more ancient isolated lineages like Haplomitrium and Takakia, evolutionary forces reshaping nuclear genomes by massive waves of gene duplications may allow for neo-functionalizations of editing factors addressing new editing sites, which may appear faster than others are lost.…”