Expected and unexpected evolution of plant RNA editing factors CLB19, CRR28 and RARE1: retention of CLB19 despite a phylogenetically deep loss of its two known editing targets in Poaceae

Anke Hein,Volker Knoop

doi:10.1186/s12862-018-1203-4

Abstract

BackgroundC-to-U RNA editing in mitochondria and chloroplasts and the nuclear-encoded, RNA-binding PPR proteins acting as editing factors present a wide field of co-evolution between the different genetic systems in a plant cell. Recent studies on chloroplast editing factors RARE1 and CRR28 addressing one or two chloroplast editing sites, respectively, found them strictly conserved among 65 flowering plants as long as one of their RNA editing targets remained present.ResultsExtending the earlier sampling to 117 angiosperms with high-quality genome or transcriptome data, we find more evidence confirming previous conclusions but now also identify cases for expected evolutionary transition states such as retention of RARE1 despite loss of its editing target or the degeneration of CRR28 truncating its carboxyterminal DYW domain. The extended angiosperm set was now used to explore CLB19, an “E+”-type PPR editing factor targeting two chloroplast editing sites, rpoAeU200SF and clpPeU559HY, in Arabidopsis thaliana. We found CLB19 consistently conserved if one of the two targets was retained and three independent losses of CLB19 after elimination of both targets. The Ericales show independent regains of the ancestrally lost clpPeU559HY editing, further explaining why multiple-target editing factors are lost much more rarely than single target factors like RARE1. The retention of CLB19 despite loss of both editing targets in some Ericaceae, Apocynaceae and in Camptotheca (Nyssaceae) likely represents evolutionary transitions. However, the retention of CLB19 after a phylogenetic deep loss in the Poaceae rather suggests a yet unrecognized further editing target, for which we suggest editing event ndhAeU473SL.ConclusionExtending the scope of studies on plant organelle RNA editing to further taxa and additional nuclear cofactors reveals expected evolutionary transitions, strikingly different evolutionary dynamics for multiple-target editing factors like CLB19 and CRR28 and suggests additional functions for editing factor CLB19 among the Poaceae.

Highlights

C-to-U RNA editing in mitochondria and chloroplasts and the nuclear-encoded, RNA-binding pentatricopeptide repeat (PPR) proteins acting as editing factors present a wide field of co-evolution between the different genetic systems in a plant cell
A wide field of investigation for nucleus-organelle co-ordination and co-evolution has emerged with the identification of specific RNA editing factors addressing the numerous sites of C-to-U RNA editing in plant chloroplasts and mitochondria
We recently found that in contrast to only moderate chloroplast RNA editing in typically investigated angiosperm models like Arabidopsis thaliana, Nicotiana tabacum or Oryza sativa with some 30–50 editing sites, editing is much more abundant in the chloroplast transcriptomes of early-branching angiosperms such as Amborella trichopoda with more than 130 chloroplast edits [17]

Summary

Introduction

C-to-U RNA editing in mitochondria and chloroplasts and the nuclear-encoded, RNA-binding PPR proteins acting as editing factors present a wide field of co-evolution between the different genetic systems in a plant cell. A wide field of investigation for nucleus-organelle co-ordination and co-evolution has emerged with the identification of specific RNA editing factors addressing the numerous sites of C-to-U RNA editing in plant chloroplasts and mitochondria. The individual sites of RNA editing in the two organelle transcriptomes are targeted by a special class of RNA-binding pentatricopeptide repeat (PPR) proteins [3, 4]. After the initial characterization of CRR4 as a first chloroplast [6] and MEF1 as a first mitochondrial editing factor [7] in the model angiosperm Arabidopsis thaliana, more than 70 PLS-type editing factors addressing individual or multiple sites in chloroplasts or mitochondria have been identified

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