Evolutionary Model of Plastidial RNA Editing in Angiosperms Presumed from Genome-Wide Analysis of Amborella trichopoda

Abstract

Amborella trichopoda is placed close to the base of the angiosperm lineage (basal angiosperm). By genome-wide RNA sequencing, we identified 184C-to-U RNA editing sites in the plastid genome of Amborella. This number is much higher than that observed in other angiosperms including maize (44 sites), rice (39 sites) and grape (115 sites). Despite the high frequency of RNA editing, the biased distribution of RNA editing sites in the genome, target codon preference and nucleotide preference adjacent to the edited cytidine are similar to that in other angiosperms, suggesting a common editing machinery. Consistent with this idea, the Amborella nuclear genome encodes 2–3 times more of the E- and DYW-subclass members of pentatricopeptide repeat proteins responsible for RNA editing site recognition in plant organelles. Among 165 editing sites in plastid protein coding sequences in Amborella, 100 sites were conserved at least in one out of 38 species selected to represent key branching points of the angiosperm phylogenetic tree. We assume these 100 sites represent at least a subset of the sites in the plastid editotype of ancestral angiosperms. We then mapped the loss and gain of editing sites on the phylogenetic tree of angiosperms. Our results support the idea that the evolution of angiosperms has led to the loss of RNA editing sites in plastids.

The Expansion and Diversification of Pentatricopeptide Repeat RNA-Editing Factors in Plants

“…The data on which this plot is based are tabulated in Supplemental Table 1. paralogs; most such clusters contain representatives from all the angiosperm groups. A rigorous analysis would require a full species tree for the OneKP samples and estimates of divergence times that are not available, but the observations listed above are consistent with the previously noted tendency toward a loss of editing (and editing factors) in angiosperms (Mower, 2008;Hein et al, 2016;Ishibashi et al, 2019).…”

“…Many moss genera have relatively few PLS proteins (<50) and presumably low numbers of editing sites (as demonstrated in Physcomitrella [Ichinose et al, 2013] and Funaria [R€ udinger et al, 2011a]). Angiosperms in general have been found to be losing editing sites over time (Freyer et al, 1997;Tillich et al, 2006;Jobson and Qiu, 2008;Mower, 2008;Hein et al, 2016), with the highest number of sites (and PLS-class sequences) being found in early-branching angiosperms such as Amborella (Hein et al, 2016;Ishibashi et al, 2019). All of these previous observations are confirmed (with much more data) by the trends in the OneKP dataset.…”

Plant organellar RNA editing: what 30 years of research has revealed

“…Welwitschia , however, has massively lost editing sites in both organelles, most likely to have been caused by retroprocessing (Fan et al , ). A gradual decrease in organellar RNA editing is apparent during the evolution of angiosperms (Freyer et al , ; Shields and Wolfe, ; Tillich et al , ; Mower, ; Cuenca et al , ; Sloan et al , ; Fujii and Small, ; Richardson et al , ; Hein et al , ; Ishibashi et al , ).…”

Tight association of genome rearrangements with gene expression in conifer plastomes

“…Most plastid genes are presumably transcribed as polycistronic mRNAs which then undergo various post-transcriptional modifications [3]. These processes generate tremendously elaborate transcriptomes with an unprecedented diversity of non-coding RNAs [4], multiple loci for transcriptional initiation and termination [5,6], a full or nearly full transcription of the genome [7,8], and varying frequencies of RNA-editing sites [9].…”