Skip to main content
Log in

RNA editing: only eleven sites are present in the Physcomitrella patens mitochondrial transcriptome and a universal nomenclature proposal

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

RNA editing in mitochondria and chloroplasts of land plants alters the coding content of transcripts through site-specific exchanges of cytidines into uridines and vice versa. The abundance of RNA editing in model plant species such as rice or Arabidopsis with some 500 affected sites in their organelle transcripts hinders straightforward approaches to elucidate its mechanisms. The moss Physcomitrella patens is increasingly being appreciated as an alternative plant model system, enhanced by the recent availability of its complete chloroplast, mitochondrial, and nuclear genome sequences. We here report the transcriptomic analysis of Physcomitrella mitochondrial mRNAs as a prerequisite for future studies of mitochondrial RNA editing in this moss. We find a strikingly low frequency of RNA editing affecting only eleven, albeit highly important, sites of C-to-U nucleotide modification in only nine mitochondrial genes. Partial editing was seen for two of these sites but no evidence for any silent editing sites (leaving the identity of the encoded amino acid unchanged) as commonly observed in vascular plants was found in Physcomitrella, indicating a compact and efficient organization of the editing machinery. Furthermore, we here wish to propose a unifying nomenclature to clearly identify and designate RNA editing positions and to facilitate future communication and database annotation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Andrés C, Lurin C, Small ID (2007) The multifarious roles of PPR proteins in plant mitochondrial gene expression. Physiol Plantarum 129(1):14–22

    Article  Google Scholar 

  • Beckert S, Muhle H, Pruchner D, Knoop V (2001) The mitochondrial nad2 gene as a novel marker locus for phylogenetic analysis of early land plants: a comparative analysis in mosses. Mol Phylogenet Evol 18(1):117–126

    Article  PubMed  CAS  Google Scholar 

  • Binder S, Marchfelder A, Brennicke A (1994) RNA editing of tRNAPhe and tRNACys in mitochondria of Oenothera berteriana is initiated in precursor molecules. Mol Gen Genet 244(1):67–74

    Article  PubMed  CAS  Google Scholar 

  • Carrillo C, Bonen L (1997) RNA editing status of nad7 intron domains in wheat mitochondria. Nucleic Acids Res 25(2):403–409

    Article  PubMed  CAS  Google Scholar 

  • Cove D (2005) The moss Physcomitrella patens. Annu Rev Genet 39:339–358

    Article  PubMed  CAS  Google Scholar 

  • Covello PS, Gray MW (1989) RNA editing in plant mitochondria. Nature 341(6243):662–666

    Article  PubMed  CAS  Google Scholar 

  • Covello PS, Gray MW (1993) On the evolution of RNA editing. Trends Genet 9(8):265–268

    Article  PubMed  CAS  Google Scholar 

  • Delannoy E, Stanley WA, Bond CS, Small ID (2007) Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem Soc Trans 35(Pt 6):1643–1647

    Article  PubMed  CAS  Google Scholar 

  • Dombrovska E, Qiu YL (2004) Distribution of introns in the mitochondrial gene nad1 in land plants: phylogenetic and molecular evolutionary implications. Mol Phylogenet Evol 32(1):246–263

    Article  PubMed  CAS  Google Scholar 

  • Frank W, Decker EL, Reski R (2005) Molecular tools to study Physcomitrella patens. Plant Biol (Stuttg) 7(3):220–227

    Article  CAS  Google Scholar 

  • Freyer R, Kiefer-Meyer M-C, Kössel H (1997) Occurrence of plastid RNA editing in all major lineages of land plants. Proc Natl Acad Sci USA 94(12):6285–6290

    Article  PubMed  CAS  Google Scholar 

  • Geddy R, Brown GG (2007) Genes encoding pentatricopeptide repeat (PPR) proteins are not conserved in location in plant genomes and may be subject to diversifying selection. BMC Genomics 8:130

    Article  PubMed  Google Scholar 

  • Giegé P, Brennicke A (1999) RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc Natl Acad Sci USA 96(26):15324–15329

    Article  PubMed  Google Scholar 

  • Gott JM, Emeson RB (2000) Functions and mechanisms of RNA editing. Annu Rev Genet 34:499–531

    Article  PubMed  CAS  Google Scholar 

  • Groth-Malonek M, Pruchner D, Grewe F, Knoop V (2005) Ancestors of trans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosses with vascular plants. Mol Biol Evol 22(1):117–125

    Article  PubMed  CAS  Google Scholar 

  • Groth-Malonek M, Wahrmund U, Polsakiewicz M, Knoop V (2007) Evolution of a pseudogene: exclusive survival of a functional mitochondrial nad7 gene supports Haplomitrium as the earliest liverwort lineage and proposes a secondary loss of RNA editing in Marchantiidae. Mol Biol Evol 24(4):1068–1074

    Article  PubMed  CAS  Google Scholar 

  • Gualberto JM, Lamattina L, Bonnard G, Weil JH, Grienenberger JM (1989) RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature 341(6243):660–662

    Article  PubMed  CAS  Google Scholar 

  • Gualberto JM, Weil JH, Grienenberger JM (1990) Editing of the wheat coxIII transcript—evidence for 12 C to U and one U to C conversions and for sequence similarities around editing sites. Nucleic Acids Res 18(13):3771–3776

    Article  PubMed  CAS  Google Scholar 

  • Gualberto JM, Bonnard G, Lamattina L, Grienenberger JM (1991) Expression of the wheat mitochondrial nad3-rps12 transcription unit: correlation between editing and mRNA maturation. Plant Cell 3(10):1109–1120

    Article  PubMed  CAS  Google Scholar 

  • Handa H (2003) The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed (Brassica napus L.): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. Nucleic Acids Res 31(20):5907–5916

    Article  PubMed  CAS  Google Scholar 

  • Hiesel R, Wissinger B, Schuster W, Brennicke A (1989) RNA editing in plant mitochondria. Science 246(4937):1632–1634

    Article  PubMed  CAS  Google Scholar 

  • Hiesel R, Combettes B, Brennicke A (1994) Evidence for RNA editing in mitochondria of all major groups of land plants except the Bryophyta. Proc Natl Acad Sci USA 91(2):629–633

    Article  PubMed  CAS  Google Scholar 

  • Hirose T, Fan H, Suzuki JY, Wakasugi T, Tsudzuki T, Kössel H, Sugiura M (1996) Occurrence of silent RNA editing in chloroplasts: its species specificity and the influence of environmental and developmental conditions. Plant Mol Biol 30(3):667–672

    Article  PubMed  CAS  Google Scholar 

  • Hoch B, Maier RM, Appel K, Igloi GL, Kössel H (1991) Editing of a chloroplast mRNA by creation of an initiation codon. Nature 353(6340):178–180

    Article  PubMed  CAS  Google Scholar 

  • Inada M, Sasaki T, Yukawa M, Tsudzuki T, Sugiura M (2004) A systematic search for RNA editing sites in pea chloroplasts: an editing event causes diversification from the evolutionarily conserved amino acid sequence. Plant Cell Physiol 45(11):1615–1622

    Article  PubMed  CAS  Google Scholar 

  • Jobson RW, Qiu YL (2008) Did RNA editing in plant organellar genomes originate under natural selection or through genetic drift? Biol Direct 3(1):43

    Article  PubMed  Google Scholar 

  • Kempken F, Mullen JA, Pring DR, Tang HV (1991) RNA editing of sorghum mitochondrial atp6 transcripts changes 15 amino acids and generates a carboxy-terminus identical to yeast. Curr Genet 20(5):417–422

    Article  PubMed  CAS  Google Scholar 

  • Knoop V (2004) The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr Genet 46(3):123–139

    Article  PubMed  CAS  Google Scholar 

  • Kotera E, Tasaka M, Shikanai T (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433(7023):326–330

    Article  PubMed  CAS  Google Scholar 

  • Kugita M, Yamamoto Y, Fujikawa T, Matsumoto T, Yoshinaga K (2003) RNA editing in hornwort chloroplasts makes more than half the genes functional. Nucleic Acids Res 31(9):2417–2423

    Article  PubMed  CAS  Google Scholar 

  • Lamattina L, Weil JH, Grienenberger JM (1989) RNA editing at a splicing site of NADH dehydrogenase subunit IV gene transcript in wheat mitochondria. FEBS Lett 258(1):79–83

    Article  PubMed  CAS  Google Scholar 

  • Lu B, Hanson MR (1994) A single homogeneous form of ATP6 protein accumulates in petunia mitochondria despite the presence of differentially edited atp6 transcripts. Plant Cell 6(12):1955–1968

    Article  PubMed  CAS  Google Scholar 

  • Lu B, Wilson RK, Phreaner CG, Mulligan RM, Hanson MR (1996) Protein polymorphism generated by differential RNA editing of a plant mitochondrial rps12 gene. Mol Cell Biol 16(4):1543–1549

    PubMed  CAS  Google Scholar 

  • Lurin C, Andrés C, Aubourg S, Bellaoui M, Bitton F, Bruyère C, Caboche M, Debast C, Gualberto J, Hoffmann B, Lecharny A, Le Ret M, Martin-Magniette ML, Mireau H, Peeters N, Renou JP, Szurek B, Taconnat L, Small I (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16(8):2089–2103

    Article  PubMed  CAS  Google Scholar 

  • Maier RM, Hoch B, Zeltz P, Kössel H (1992) Internal editing of the maize chloroplast ndhA transcript restores codons for conserved amino acids. Plant Cell 4(5):609–616

    Article  PubMed  CAS  Google Scholar 

  • Maier RM, Zeltz P, Kössel H, Bonnard G, Gualberto JM, Grienenberger JM (1996) RNA editing in plant mitochondria and chloroplasts. Plant Mol Biol 32(1–2):343–365

    Article  PubMed  CAS  Google Scholar 

  • Maier UG, Bozarth A, Funk HT, Zauner S, Rensing SA, Schmitz-Linneweber C, Börner T, Tillich M (2008) Complex chloroplast RNA metabolism: just debugging the genetic programme? BMC Biol 6:36

    Article  PubMed  Google Scholar 

  • Malek O, Knoop V (1998) Trans-splicing group II introns in plant mitochondria: the complete set of cis-arranged homologs in ferns, fern allies, and a hornwort. RNA 4(12):1599–1609

    Article  PubMed  CAS  Google Scholar 

  • Malek O, Lättig K, Hiesel R, Brennicke A, Knoop V (1996) RNA editing in bryophytes and a molecular phylogeny of land plants. EMBO J 15(6):1403–1411

    PubMed  CAS  Google Scholar 

  • Marchfelder A, Brennicke A, Binder S (1996) RNA editing is required for efficient excision of tRNA(Phe) from precursors in plant mitochondria. J Biol Chem 271(4):1898–1903

    Article  PubMed  CAS  Google Scholar 

  • Miyata Y, Sugita M (2004) Tissue- and stage-specific RNA editing of rps14 transcripts in moss (Physcomitrella patens) chloroplasts. J Plant Physiol 161(1):113–115

    Article  PubMed  CAS  Google Scholar 

  • Miyata Y, Sugiura C, Kobayashi Y, Hagiwara M, Sugita M (2002) Chloroplast ribosomal S14 protein transcript is edited to create a translation initiation codon in the moss Physcomitrella patens. Biochim Biophys Acta 1576(3):346–349

    PubMed  CAS  Google Scholar 

  • Miyata Y, Sugita C, Maruyama K, Sugita M (2008) RNA editing in the anticodon of tRNA(Leu) (CAA) occurs before group I intron splicing in plastids of a moss Takakia lepidozioides S. Hatt. & Inoue. Plant Biol (Stuttg) 10(2):250–255

    Article  CAS  Google Scholar 

  • Mower JP, Palmer JD (2006) Patterns of partial RNA editing in mitochondrial genes of Beta vulgaris. Mol Genet Genomics 276(3):285–293

    Article  PubMed  CAS  Google Scholar 

  • Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M, Hirai A, Kadowaki K (2002) The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics 268(4):434–445

    Article  PubMed  CAS  Google Scholar 

  • O’Toole N, Hattori M, Andres C, Iida K, Lurin C, Schmitz-Linneweber C, Sugita M, Small I (2008) On the expansion of the pentatricopeptide repeat gene family in plants. Mol Biol Evol 25(6):1120–1128

    Article  PubMed  Google Scholar 

  • Okuda K, Nakamura T, Sugita M, Shimizu T, Shikanai T (2006) A pentatricopeptide repeat protein is a site-recognition factor in chloroplast RNA editing. J Biol Chem 281(49):37661–37667

    Article  PubMed  CAS  Google Scholar 

  • Okuda K, Myouga F, Motohashi R, Shinozaki K, Shikanai T (2007) Conserved domain structure of pentatricopeptide repeat proteins involved in chloroplast RNA editing. Proc Natl Acad Sci USA 104(19):8178–8183

    Article  PubMed  CAS  Google Scholar 

  • Phreaner CG, Williams MA, Mulligan RM (1996) Incomplete editing of rps12 transcripts results in the synthesis of polymorphic polypeptides in plant mitochondria. Plant Cell 8(1):107–117

    Article  PubMed  CAS  Google Scholar 

  • Pruchner D, Nassal B, Schindler M, Knoop V (2001) Mosses share mitochondrial group II introns with flowering plants, not with liverworts. Mol Genet Genomics 266(4):608–613

    Article  PubMed  CAS  Google Scholar 

  • Quatrano RS, McDaniel SF, Khandelwal A, Perroud PF, Cove DJ (2007) Physcomitrella patens: mosses enter the genomic age. Curr Opin Plant Biol 10(2):182–189

    Article  PubMed  CAS  Google Scholar 

  • Rensing SA, Rombauts S, Van de Peer Y, Reski R (2002) Moss transcriptome and beyond. Trends Plant Sci 7(12):535–538

    Article  PubMed  CAS  Google Scholar 

  • Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y, Tanahashi T, Sakakibara K, Fujita T, Oishi K, Shin I, Kuroki Y, Toyoda A, Suzuki Y, Hashimoto S, Yamaguchi K, Sugano S, Kohara Y, Fujiyama A, Anterola A, Aoki S, Ashton N, Barbazuk WB, Barker E, Bennetzen JL, Blankenship R, Cho SH, Dutcher SK, Estelle M, Fawcett JA, Gundlach H, Hanada K, Heyl A, Hicks KA, Hughes J, Lohr M, Mayer K, Melkozernov A, Murata T, Nelson DR, Pils B, Prigge M, Reiss B, Renner T, Rombauts S, Rushton PJ, Sanderfoot A, Schween G, Shiu SH, Stueber K, Theodoulou FL, Tu H, Van de Peer Y, Verrier PJ, Waters E, Wood A, Yang L, Cove D, Cuming AC, Hasebe M, Lucas S, Mishler BD, Reski R, Grigoriev IV, Quatrano RS, Boore JL (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319(5859):64–69

    Article  PubMed  CAS  Google Scholar 

  • Reski R (1998) Physcomitrella and Arabidopsis: the David and Goliath of reverse genetics. Trends Plant Sci 3(6):209–210

    Article  Google Scholar 

  • Reski R, Cove DJ (2004) Physcomitrella patens. Curr Biol 14(7):R261–R262

    Article  PubMed  CAS  Google Scholar 

  • Rivals E, Bruyere C, Toffano-Nioche C, Lecharny A (2006) Formation of the Arabidopsis pentatricopeptide repeat family. Plant Physiol 141(3):825–839

    Article  PubMed  CAS  Google Scholar 

  • Rüdinger M, Polsakiewicz M, Knoop V (2008) Organellar RNA editing and plant-specific extensions of pentatricopeptide repeat (PPR) proteins in jungermanniid but not in marchantiid liverworts. Mol Biol Evol 25(7):1405–1414

    Article  PubMed  Google Scholar 

  • Saha D, Prasad AM, Srinivasan R (2007) Pentatricopeptide repeat proteins and their emerging roles in plants. Plant Physiol Biochem 45(8):521–534

    Article  PubMed  CAS  Google Scholar 

  • Salone V, Rüdinger M, Polsakiewicz M, Hoffmann B, Groth-Malonek M, Szurek B, Small I, Knoop V, Lurin C (2007) A hypothesis on the identification of the editing enzyme in plant organelles. FEBS Lett 581(22):4132–4138

    Article  PubMed  CAS  Google Scholar 

  • Sasaki T, Yukawa Y, Miyamoto T, Obokata J, Sugiura M (2003) Identification of RNA editing sites in chloroplast transcripts from the maternal and paternal progenitors of tobacco (Nicotiana tabacum): comparative analysis shows the involvement of distinct trans-factors for ndhB editing. Mol Biol Evol 20(7):1028–1035

    Article  PubMed  CAS  Google Scholar 

  • Schaefer DG, Zryd JP (2001) The moss Physcomitrella patens, now and then. Plant Physiol 127(4):1430–1438

    Article  PubMed  CAS  Google Scholar 

  • Schuster W, Hiesel R, Wissinger B, Brennicke A (1990a) RNA editing in the cytochrome b locus of the higher plant Oenothera berteriana includes a U-to-C transition. Mol Cell Biol 10(5):2428–2431

    PubMed  CAS  Google Scholar 

  • Schuster W, Unseld M, Wissinger B, Brennicke A (1990b) Ribosomal protein S14 transcripts are edited in Oenothera mitochondria. Nucleic Acids Res 18(2):229–233

    Article  PubMed  CAS  Google Scholar 

  • Schuster W, Wissinger B, Unseld M, Brennicke A (1990c) Transcripts of the NADH-dehydrogenase subunit 3 gene are differentially edited in Oenothera mitochondria. EMBO J 9(1):263–269

    PubMed  CAS  Google Scholar 

  • Small ID, Peeters N (2000) The PPR motif—a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci 25(2):46–47

    Article  PubMed  CAS  Google Scholar 

  • Smith HC, Gott JM, Hanson MR (1997) A guide to RNA editing. RNA 3(10):1105–1123

    PubMed  CAS  Google Scholar 

  • Sper-Whitis GL, Russell AL, Vaughn JC (1994) Mitochondrial RNA editing of cytochrome c oxidase subunit II (coxII) in the primitive vascular plant Psilotum nudum. Biochem Biophys Acta Gene Struct Expr 1218(2):218–220

    CAS  Google Scholar 

  • Sper-Whitis GL, Moody JL, Vaughn JC (1996) Universality of mitochondrial RNA editing in cytochrome-c oxidase subunit I (coxI) among the land plants. Biochem Biophys Acta Gene Struct Expr 1307(3):301–308

    Google Scholar 

  • Steinhauser S, Beckert S, Capesius I, Malek O, Knoop V (1999) Plant mitochondrial RNA editing: extreme in hornworts and dividing the liverworts? J Mol Evol 48(3):303–312

    Article  PubMed  CAS  Google Scholar 

  • Sugita M, Miyata Y, Maruyama K, Sugiura C, Arikawa T, Higuchi M (2006) Extensive RNA editing in transcripts from the psbB operon and rpoA gene of plastids from the enigmatic moss Takakia lepidozioides. Biosci Biotechnol Biochem 70(9):2268–2274

    Article  PubMed  CAS  Google Scholar 

  • Sugiura C, Kobayashi Y, Aoki S, Sugita C, Sugita M (2003) Complete chloroplast DNA sequence of the moss Physcomitrella patens: evidence for the loss and relocation of rpoA from the chloroplast to the nucleus. Nucleic Acids Res 31(18):5324–5331

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24(8):1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Terasawa K, Odahara M, Kabeya Y, Kikugawa T, Sekine Y, Fujiwara M, Sato N (2006) The mitochondrial genome of the moss Physcomitrella patens sheds new light on mitochondrial evolution in land plants. Mol Biol Evol 24(3):699–709

    Article  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Tillich M, Schmitz-Linneweber C, Herrmann RG, Maier RM (2001) The plastid chromosome of maize (Zea mays): update of the complete sequence and transcript editing sites. Maize Genet Coop Newslett 75:42–44

    Google Scholar 

  • Tillich M, Funk HT, Schmitz-Linneweber C, Poltnigg P, Sabater B, Martin M, Maier RM (2005) Editing of plastid RNA in Arabidopsis thaliana ecotypes. Plant J 43(5):708–715

    Article  PubMed  CAS  Google Scholar 

  • Tillich M, Lehwark P, Morton BR, Maier UG (2006) The evolution of chloroplast RNA editing. Mol Biol Evol 23(10):1912–1921

    Article  PubMed  CAS  Google Scholar 

  • Tsudzuki T, Wakasugi T, Sugiura M (2001) Comparative analysis of RNA editing sites in higher plant chloroplasts. J Mol Evol 53(4–5):327–332

    Article  PubMed  CAS  Google Scholar 

  • Vangerow S, Teerkorn T, Knoop V (1999) Phylogenetic information in the mitochondrial nad5 gene of pteridophytes: RNA editing and intron sequences. Plant Biol 1(2):235–243

    Article  CAS  Google Scholar 

  • Verbitskiy D, Takenaka M, Neuwirt J, van der Merwe JA, Brennicke A (2006) Partially edited RNAs are intermediates of RNA editing in plant mitochondria. Plant J 47(3):408–416

    Article  PubMed  CAS  Google Scholar 

  • Williams MA, Tallakson WA, Phreaner CG, Mulligan RM (1998) Editing and translation of ribosomal protein S13 transcripts: unedited translation products are not detectable in maize mitochondria. Curr Genet 34(3):221–226

    Article  PubMed  CAS  Google Scholar 

  • Yang AJ, Mulligan RM (1991) RNA editing intermediates of cox2 transcripts in maize mitochondria. Mol Cell Biol 11(8):4278–4281

    PubMed  CAS  Google Scholar 

  • Yoshinaga K, Iinuma H, Masuzawa T, Uedal K (1996) Extensive RNA editing of U to C in addition to C to U substitution in the rbcL transcripts of hornwort chloroplasts and the origin of RNA editing in green plants. Nucleic Acids Res 24(6):1008–1014

    Article  PubMed  CAS  Google Scholar 

  • Yoshinaga K, Kakehi T, Shima Y, Iinuma H, Masuzawa T, Ueno M (1997) Extensive RNA editing and possible double-stranded structures determining editing sites in the atpB transcripts of hornwort chloroplasts. Nucleic Acids Res 25(23):4830–4834

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Research in the authors’ laboratories is supported by grants from the Deutsche Forschungsgemeinschaft DFG, in particular SFB-TR1 (Marburg), and BMBF FRISYS (Freiburg). We thank Andrew Bozarth for comments on the manuscript. H.T.F. thanks Christopher Grosche for skilful lab assistance. M.R. is grateful to Julia Dreistein for concentrated and helpful work during a laboratory practical training and to Judith Schleppenbäumer and Thomas Münster, MPI Cologne, who have kindly provided the P. patens Gransden strain. We wish to dedicate this publication to the memory of Rudolf Hiesel, colleague, friend and co-discoverer of RNA editing in plants, who passed away much too early.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Volker Knoop.

Additional information

Communicated by B. Franz Lang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rüdinger, M., Funk, H.T., Rensing, S.A. et al. RNA editing: only eleven sites are present in the Physcomitrella patens mitochondrial transcriptome and a universal nomenclature proposal. Mol Genet Genomics 281, 473–481 (2009). https://doi.org/10.1007/s00438-009-0424-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-009-0424-z

Keywords

Navigation