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

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Abstract

RNA editing in mitochondria and chloroplasts of land plants alters transcript sequences by site-specific conversions of cytidines into uridines. RNA editing frequencies vary extremely between land plant clades, ranging from zero in some liverworts to more than 2,000 sites in lycophytes. Unique pentatricopeptide repeat (PPR) proteins with variable domain extension (E/E+/DYW) have recently been identified as specific editing site recognition factors in model plants. The distinctive functions of these PPR protein domain additions have remained unclear, although deaminase function has been proposed for the DYW domain. To shed light on diversity of RNA editing and DYW proteins at the origin of land plant evolution, we investigated editing patterns of the mitochondrial nad5, nad4, and nad2 genes in a wide sampling of more than 100 liverworts and mosses using the recently developed PREPACT program (www.prepact.de) and exemplarily confirmed predicted RNA editing sites in selected taxa. Extreme variability in RNA editing frequency is seen both in liverworts and mosses. Only few editings exist in the liverwort Lejeunea cavifolia or the moss Pogonatum urnigerum whereas up to 20% of cytidines are edited in the liverwort Haplomitrium mnioides or the moss Takakia lepidozioides. Interestingly, the latter are taxa that branch very early within their respective clades. Amplicons targeting the E/E+/DYW domains and subsequent random clone sequencing show DYW domains among bryophytes to be highly conserved in comparison with their angiosperm counterparts and to correlate well with RNA editing frequencies regarding their diversities. We propose that DYW proteins are the key players of RNA editing at the origin of land plants.

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Acknowledgments

We are grateful to Prof. Jan-Peter Frahm and Dr. Boon-Chuan Ho (University Bonn) for their help to collect bryophyte plant material and to Prof. Wolfgang Alt and Martin Bock (University Bonn) for doing initial MATLAB simulations and help with the Fisher’s exact test. Work in the authors’ laboratory on RNA editing and DYW proteins is supported by DFG Grant Kn411/7, work on liverwort and moss phylogeny was supported by the DFG Grant Kn411/6. Finally, we would like to thank two anonymous reviewers for their helpful suggestions for changes in the manuscript and Julia Hecht for comments on text and language.

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  1. Ute Volkmar

    Present address: Instituut voor Plantkunde en Microbiologie, Laboratorium voor Plantensystematiek, K.U. Leuven, Kasteelpark Arenberg 31, 3001, Leuven, Belgium

  2. Milena Groth-Malonek

    Present address: KWS SAAT AG, Grimsehlstr. 31, 37555, Einbeck, Germany

Authors and Affiliations

  1. IZMB – Institut für Zelluläre und Molekulare Botanik, Abteilung Molekulare Evolution, Universität Bonn, Kirschallee 1, 53115, Bonn, Germany

    Mareike Rüdinger, Ute Volkmar, Henning Lenz, Milena Groth-Malonek & Volker Knoop

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Correspondence to Mareike Rüdinger.

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Supplementary Figure 1

Gene family sampling simulation. The graphs show simulations of different genes of a family to be found in a given number of randomly sequenced clones (left: 30 clones, right: 51 clones) assuming an ideal unbiased PCR (uniformly distributed amount of products). Depending on the actual number of different genes and the number of clones sequenced (red line) the number of different genes sampled in the selection can be simulated. Blue dots show the mean of different PPRs drawn from 10,000 replicates. The gray area indicates the 2σ confidence interval (PDF 116 kb)

Supplementary Table S1

Comparison of RNA editing frequencies in selected model plants. RNA editing frequencies (number of sites/coding nucleotides) were calculated on the basis of completely investigated transcriptomes and extrapolated from nad4, nad5 and nad2 alone (XLS 35 kb)

Supplementary Table S2

RNA editing site matrices of the mitochondrial nad5 gene of liverworts. Excel sheets present the matrices of RNA editing sites predicted with Marchantia polymorpha, Chara vulgaris, Arabidopsis thaliana or Physcomitrella patens as reference taxon and the list of common predicted editing sites (Commons). Editing sites confirmed on cDNA level are highlighted in bold. Crosses indicate editing sites which could not be verified on cDNA level. Total numbers of putative editing sites per taxon are listed in a separate column (sum). Multiple RNA editing events simultaneously affecting a single codon are listed as one editing event, numbers of multisteps are indicated in the column “multistep” (XLS 204 kb)

Supplementary Table S3

RNA editing site matrices of the mitochondrial nad4 gene of liverworts. Excel sheets present the matrices of RNA editing sites predicted with Marchantia polymorpha, Chara vulgaris, Arabidopsis thaliana or Physcomitrella patens as reference taxon and the list of common predicted editing sites (Commons). Editing sites confirmed on cDNA level are highlighted in bold. Crosses indicate editing sites which could not be verified on cDNA level. Total numbers of putative editing sites per taxon are listed in a separate column (sum). Multiple RNA editing events simultaneously affecting a single codon are listed as one editing event, numbers of multisteps are indicated in the column “multistep” (XLS 221 kb)

Supplementary Table S4

RNA editing site matrices of the mitochondrial nad5 gene of mosses. Excel sheets present the matrices of RNA editing sites predicted with Marchantia polymorpha, Chara vulgaris, Arabidopsis thaliana or Physcomitrella patens as reference taxon and the list of common predicted editing sites (Commons). Editing sites confirmed on cDNA level are highlighted in bold. Crosses indicate editing sites which could not be verified on cDNA level. Total numbers of putative editing sites per taxon are listed in a separate column (sum). Multiple RNA editing events simultaneously affecting a single codon are listed as one editing event, numbers of multisteps are indicated in the column “multistep” (XLS 174 kb)

Supplementary Table S5

RNA editing site matrices of the mitochondrial nad2 gene of mosses. Excel sheets present the matrices of RNA editing sites predicted with Marchantia polymorpha, Chara vulgaris, Arabidopsis thaliana or Physcomitrella patens as reference taxon and the list of common predicted editing sites (Commons). Editing sites confirmed on cDNA level are highlighted in bold. Crosses indicate editing sites which could not be verified on cDNA level. Total numbers of putative editing sites per taxon are listed in a separate column (sum). Multiple RNA editing events simultaneously affecting a single codon are listed as one editing event, numbers of multisteps are indicated in the column “multistep” (XLS 128 kb)

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Rüdinger, M., Volkmar, U., Lenz, H. et al. Nuclear DYW-Type PPR Gene Families Diversify with Increasing RNA Editing Frequencies in Liverwort and Moss Mitochondria. J Mol Evol 74, 37–51 (2012). https://doi.org/10.1007/s00239-012-9486-3

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