Frequent chloroplast RNA editing in early-branching flowering plants: pilot studies on angiosperm-wide coexistence of editing sites and their nuclear specificity factors.

Anke Hein,Monika Polsakiewicz,Volker Knoop

doi:10.1186/s12862-016-0589-0

Abstract

BackgroundRNA editing by cytidine-to-uridine conversions is an essential step of RNA maturation in plant organelles. Some 30–50 sites of C-to-U RNA editing exist in chloroplasts of flowering plant models like Arabidopsis, rice or tobacco. We now predicted significantly more RNA editing in chloroplasts of early-branching angiosperm genera like Amborella, Calycanthus, Ceratophyllum, Chloranthus, Illicium, Liriodendron, Magnolia, Nuphar and Zingiber. Nuclear-encoded RNA-binding pentatricopeptide repeat (PPR) proteins are key editing factors expected to coevolve with their cognate RNA editing sites in the organelles.ResultsWith an extensive chloroplast transcriptome study we identified 138 sites of RNA editing in Amborella trichopoda, approximately the 3- to 4-fold of cp editing in Arabidopsis thaliana or Oryza sativa. Selected cDNA studies in the other early-branching flowering plant taxa furthermore reveal a high diversity of early angiosperm RNA editomes. Many of the now identified editing sites in Amborella have orthologues in ferns, lycophytes or hornworts. We investigated the evolution of CRR28 and RARE1, two known Arabidopsis RNA editing factors responsible for cp editing events ndhBeU467PL, ndhDeU878SL and accDeU794SL, respectively, all of which we now found conserved in Amborella. In a phylogenetically wide sampling of 65 angiosperm genomes we find evidence for only one single loss of CRR28 in chickpea but several independent losses of RARE1, perfectly congruent with the presence of their cognate editing sites in the respective cpDNAs.ConclusionChloroplast RNA editing is much more abundant in early-branching than in widely investigated model flowering plants. RNA editing specificity factors can be traced back for more than 120 million years of angiosperm evolution and show highly divergent patterns of evolutionary losses, matching the presence of their target editing events.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0589-0) contains supplementary material, which is available to authorized users.

Highlights

RNA editing by cytidine-to-uridine conversions is an essential step of RNA maturation in plant organelles
The Amborella chloroplast editome Using PREPACT’s feature to predict RNA editing for entire organelle genomes we found predictions of up to more than one hundred RNA editing sites for the chloroplast genomes of several angiosperms representing early branches in the phylogeny of flowering plants such as Amborella trichopoda, Calycanthus floridus, Ceratophyllum demersum, Chloranthus spicatus, Illicium oligandrum, Liriodendron tulipifera, Magnolia kwangsiensis, Nuphar advena and Zingiber spectabile
In the case of Amborella trichopoda, the only living representative of the likely sister lineage to all other extant flowering plants, we found predictions of 90, 142 or 162 sites of C-to-U RNA editing to restore conserved codons at stringency thresholds of 90, 80 or 70 %, respectively, of the 17 references implemented in PREPACT 2.0 (Additional file 1)

Summary

Introduction

RNA editing by cytidine-to-uridine conversions is an essential step of RNA maturation in plant organelles. One striking discrepancy of RNA editing in the two organelles, concerns the observed abundance of editing events in widely studied model plants such as Arabidopsis thaliana, Nicotiana tabacum or Oryza sativa where some 400–500 mitochondrial sites coexist with only 30–40 such sites in chloroplasts [14] Such a strong bias of mitochondrial vs chloroplast RNA editing likewise exists in the moss Physcomitrella patens where only two events of chloroplast editing [15] are contrasted by eleven such sites in mitochondria [16]. The moss has recently become the first organism with a completed mutual assignment of organelle editing sites to their nuclear PPR protein cofactors [17,18,19]

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