RNA editing: only eleven sites are present in the Physcomitrella patens mitochondrial transcriptome and a universal nomenclature proposal
- 424 Downloads
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.
KeywordsPhyscomitrella RNA editing Nomenclature Mitochondrial DNA
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.
- 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):1068–1074PubMedCrossRefGoogle 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):2089–2103PubMedCrossRefGoogle 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):434–445PubMedCrossRefGoogle 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):64–69PubMedCrossRefGoogle 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):1028–1035PubMedCrossRefGoogle 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):218–220Google 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):301–308Google 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 75:42–44Google Scholar