Skip to main content
SpringerLink
Log in

RNA editing restores critical domains of a group I intron in fern mitochondria

  • Research Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

In the leptosporangiate fern Osmunda regalis, cox1 gene is disrupted by a 1071-nucleotide-long group I intron that is homologous to the Marchantia polymorpha cox1 intron 4 (cox1i395g1). This intron, which shares 89% sequence identity with its bryophyte counterpart, lost the capacity to encode for a maturase due to insertion/deletion mutations. The cox1 coding region is interrupted by a stop codon in both exons. The cox1 transcript undergoes 58 C-to-U and 13 U-to-C conversions, including the suppression of two stop codons that result in the recovery of a functional cox1 ORF. Interestingly, 4 C-to-U conversions found in mRNA precursors showed that the O. regalis cox1i395g1 intron is efficiently edited. These modifications improved the sequence identity with the Marchantia cox1i395 intron. In particular, the RNA editing events affect regions involved in secondary and tertiary structures of the intron, restoring three base pairing in the structural P5a and P9 helices, and correcting a highly conserved U in the P7 helix that contributes to the catalytic core. Moreover, cox1 intron orthologous from three different fern species were found to be edited by both C-to-U and U-to-C conversions in P7 and P9. Thus, RNA editing helps to correct the conserved domains of group I introns in “true ferns”, suggesting a possible link between editing and splicing. We present here the first experimental evidence of RNA editing concerning a group I intron in plant organelles.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adams PL, Stahley MR, Kosek AB, Wang J, Strobel SA (2004) Crystal structure of a self-splicing group I intron with both exons. Nature 430:45–50

    Article  PubMed  CAS  Google Scholar 

  • Bégu D, Araya A (2009) The horsetail Equisetum arvense mitochondria share two group I introns with the liverwort Marchantia, acquired a novel group II intron but lost intron-encoded ORFs. Curr Genet 55:69–79

    Article  PubMed  Google Scholar 

  • Bégu D, Graves PV, Domec C, Arselin G, Litvak S, Araya A (1990) RNA editing of wheat mitochondrial ATP synthase subunit 9: direct protein and cDNA sequencing. Plant Cell 2:1283–1290

    Article  PubMed  Google Scholar 

  • Blanc V, Litvak S, Araya A (1995) RNA editing in wheat mitochondria proceeds by a deamination mechanism. FEBS Lett 373:56–60

    Article  PubMed  CAS  Google Scholar 

  • Börner GV, Morl M, Wissinger B, Brennicke A, Schmelzer C (1995) RNA editing of a group II intron in Oenothera as a prerequisite for splicing. Mol Gen Genet 246:739–744

    Article  PubMed  Google Scholar 

  • Burke JM, Belfort M, Cech TR, Davies RW, Schweyen RJ, Shub DA, Szostak JW, Tabak HF (1987) Structural conventions for group I introns. Nucl Acids Res 15:7217–7221

    Article  PubMed  CAS  Google Scholar 

  • Castandet B, Choury D, Bégu D, Jordana X, Araya A (2010) Intron RNA editing is essential for splicing in plant mitochondria. Nucl Acids Res 38:7112–7121

    Article  PubMed  CAS  Google Scholar 

  • Cech TR (1988) Conserved sequences and structures of group I introns: building an active site for RNA catalysis—a review. Gene 73:259–271

    Article  PubMed  CAS  Google Scholar 

  • Chaw SM, Shih AC, Wang D, Wu YW, Liu SM, Chou TY (2008) The mitochondrial genome of the gymnosperm Cycas taitungensis contains a novel family of short interspersed elements, Bpu sequences, and abundant RNA editing sites. Mol Biol Evol 25:603–615

    Article  PubMed  CAS  Google Scholar 

  • Cho Y, Qiu YL, Kuhlman P, Palmer JD (1998) Explosive invasion of plant mitochondria by a group I intron. Proc Natl Acad Sci USA 95:14244–14249

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dujon B, Colleaux L, Jacquier A, Michel F, Monteilhet C (1986) Mitochondrial introns as mobile genetic elements: the role of intron-encoded proteins. Basic Life Sci 40:5–27

    PubMed  CAS  Google Scholar 

  • Farré JC, Araya A (2002) RNA splicing in higher plant mitochondria: determination of functional elements in group II intron from a chimeric cox II gene in electroporated wheat mitochondria. Plant J 29:203–213

    Article  PubMed  Google Scholar 

  • Férandon C, Moukha S, Callac P, Benedetto JP, Castroviejo M, Barroso G (2010) The Agaricus bisporus cox1 gene: the longest mitochondrial gene and the largest reservoir of mitochondrial group I introns. PLoS One 5:e14048

    Article  PubMed  Google Scholar 

  • Gampel A, Tzagoloff A (1987) In vitro splicing of the terminal intervening sequence of Saccharomyces cerevisiae cytochrome b pre-mRNA. Mol Cell Biol 7:2545–2551

    PubMed  CAS  Google Scholar 

  • Giegé P, Brennicke A (2001) From gene to protein in higher plant mitochondria. C R Acad Sci III 324:209–217

    PubMed  Google Scholar 

  • Golden BL, Gooding AR, Podell ER, Cech TR (1998) A preorganized active site in the crystal structure of the Tetrahymena ribozyme. Science 282:259–264

    Article  PubMed  CAS  Google Scholar 

  • Golden BL, Kim H, Chase E (2005) Crystal structure of a phage Twort group I ribozyme-product complex. Nat Struct Mol Biol 12:82–89

    Article  PubMed  CAS  Google Scholar 

  • Grewe F, Viehoever P, Weisshaar B, Knoop V (2009) A trans-splicing group I intron and tRNA-hyperediting in the mitochondrial genome of the lycophyte Isoetes engelmannii. Nucleic Acids Res 37:5093–5104

    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 341:660–662

    Article  PubMed  CAS  Google Scholar 

  • Guo F, Gooding AR, Cech TR (2004) Structure of the Tetrahymena ribozyme: base triple sandwich and metal ion at the active site. Mol Cell 16:351–362

    PubMed  CAS  Google Scholar 

  • Hecht J, Grewe F, Knoop V (2011) Extreme RNA editing in coding islands and abundant microsatellites in repeat sequences of Selaginella moellendorffii mitochondria: the root of frequent plant mtDNA recombination in early tracheophytes. Genome Biol. Evol 3:344–358

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Keren I, Bezawork-Geleta A, Kolton M, Maayan I, Belausov E, Levy M, Mett A, Gidoni D, Shaya F, Ostersetzer-Biran O (2009) AtnMat2, a nuclear-encoded maturase required for splicing of group-II introns in Arabidopsis mitochondria. RNA 15:2299–2311

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lang BF, Laforest MJ, Burger G (2007) Mitochondrial introns: a critical view. Trends Genet 23:119–125

    Article  PubMed  CAS  Google Scholar 

  • Lehnert V, Jaeger L, Michel F, Westhof E (1996) New loop–loop tertiary interactions in self-splicing introns of subgroup IC and ID: a complete 3D model of the Tetrahymena thermophila ribozyme. Chem Biol 3:993–1009

    Article  PubMed  CAS  Google Scholar 

  • Longo A, Leonard CW, Bassi GS, Berndt D, Krahn JM, Hall TM, Weeks KM (2005) Evolution from DNA to RNA recognition by the bI3 LAGLIDADG maturase. Nat Struct Mol Biol 12:779–787

    Article  PubMed  CAS  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 4:1599–1609

    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 15:1403–1411

    PubMed  CAS  Google Scholar 

  • Maréchal-Drouard L, Ramamonjisoa D, Cosset A, Weil JH, Dietrich A (1993) Editing corrects mispairing in the acceptor stem of bean and potato mitochondrial phenylalanine transfer RNAs. Nucleic Acids Res 21:4909–4914

    Article  PubMed  Google Scholar 

  • Michel F, Jacquier A, Dujon B (1982) Comparison of fungal mitochondrial introns reveals extensive homologies in RNA secondary structure. Biochimie 64:867–881

    Article  PubMed  CAS  Google Scholar 

  • Michel F, Ellington AD, Couture S, Szostak JW (1990) Phylogenetic and genetic evidence for base-triples in the catalytic domain of group I introns. Nature 347:578–580

    Article  PubMed  CAS  Google Scholar 

  • Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Kanegae T, Ogura Y, Kohchi T et al (1992) Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. A primitive form of plant mitochondrial genome. J Mol Biol 223:1–7

    Article  PubMed  CAS  Google Scholar 

  • Ohta E, Oda K, Yamato K, Nakamura Y, Takemura M, Nozato N, Akashi K, Ohyama K, Michel F (1993) Group I introns in the liverwort mitochondrial genome: the gene coding for subunit 1 of cytochrome oxidase shares five intron positions with its fungal counterparts. Nucl Acids Res 21:1297–1305

    Article  PubMed  CAS  Google Scholar 

  • Quiñones V, Zanlungo S, Holuigue L, Litvak S, Jordana X (1995) The cox1 initiation codon is created by RNA editing in potato mitochondria. Plant Physiol 108:1327–1328

    Article  PubMed  Google Scholar 

  • Sanchez-Puerta MV, Cho Y, Mower JP, Alverson AJ, Palmer JD (2008) Frequent, phylogenetically local horizontal transfer of the cox1 group I Intron in flowering plant mitochondria. Mol Biol Evol 25:1762–1777

    Article  PubMed  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. Biochim Biophys Acta 1307:301–308

    PubMed  Google Scholar 

  • Steinhauser S, Beckert S, Capesius I, Malek O, Knoop V (1999) Plant mitochondrial RNA editing. J Mol Evol 48:303–312

    Article  PubMed  CAS  Google Scholar 

  • Steitz TA, Steitz JA (1993) A general two-metal-ion mechanism for catalytic RNA. Proc Natl Acad Sci USA 90:6498–6502

    Article  PubMed  CAS  Google Scholar 

  • Terasawa K, Odahara M, Kabeya Y, Kikugawa T, Sekine Y, Fujiwara M, Sato N (2007) The mitochondrial genome of the moss Physcomitrella patens sheds new light on mitochondrial evolution in land plants. Mol Biol Evol 24:699–709

    Article  PubMed  CAS  Google Scholar 

  • Tocchini-Valentini GD, Fruscoloni P, Tocchini-Valentini GP (2011) Evolution of introns in the archaeal world. Proc Natl Acad Sci USA 108:4782–4787

    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 1:235–243

    Article  CAS  Google Scholar 

  • Vicens Q, Cech TR (2006) Atomic level architecture of group I introns revealed. Trends Biochem Sci 31:41–51

    Article  PubMed  CAS  Google Scholar 

  • Webb AE, Rose MA, Westhof E, Weeks KM (2001) Protein-dependent transition states for ribonucleoprotein assembly. J Mol Biol 309:1087–1100

    Article  PubMed  CAS  Google Scholar 

  • Wikström N, Pryer KM (2005) Incongruence between primary sequence data and the distribution of a mitochondrial atp1 group II intron among ferns and horsetails. Mol Phylogenet Evol 36:484–493

    Article  PubMed  Google Scholar 

  • Wissinger B, Schuster W, Brennicke A (1991) Trans-splicing in Oenothera mitochondria: nad1 mRNAs are edited in exon and trans-splicing group II intron sequences. Cell 65:473–482

    Article  PubMed  CAS  Google Scholar 

  • Woodson SA (2005) Structure and assembly of group I introns. Curr Opin Struct Biol 15:324–330

    Article  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. Nucl Acids Res 24:1008–1014

    Article  PubMed  CAS  Google Scholar 

  • Yu W, Schuster W (1995) Evidence for a site-specific cytidine deamination reaction involved in C to U RNA editing of plant mitochondria. J Biol Chem 270:18227–18233

    Article  PubMed  CAS  Google Scholar 

  • Zanlungo S, Quiñones V, Moenne A, Holuigue L, Jordana X (1995) Splicing and editing of rps10 transcripts in potato mitochondria. Curr Genet 27:565–571

    Article  PubMed  CAS  Google Scholar 

  • Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucl Acids Res 31:3406–3415

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Christophe Velours for providing yeast mitochondrial DNA. This research was supported by the Centre National de la Recherche Scientifique (CNRS), the Université Bordeaux-Segalen, and the Ministère de l’Enseignement Supérieur et de la Recherche, France. B.C. was supported by a doctoral fellowship of the Ministère de l’Enseignement Supérieur et de la Recherche. DNA sequencing was performed at the Genotyping and Sequencing Facility in Bordeaux (grants from the Conseil Régional d’Aquitaine n°. 20030304002FA and 20040305003FA, and from the European Union, FEDER n° 2003227.

Author information

Author notes

  1. Benoît Castandet

    Present address: Boyce Thompson Institute for Plant Research, Ithaca, NY, USA

Authors and Affiliations

  1. Laboratoire de Microbiologie Fondamentale et Pathogénicité UMR5234, Centre National de la Recherche Scientifique (C.N.R.S.) and Université Bordeaux Segalen, 146 rue Léo Saignat, 33076, Bordeaux Cedex, France

    Dominique Bégu, Benoît Castandet & Alejandro Araya

Authors
  1. Dominique Bégu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Benoît Castandet
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alejandro Araya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dominique Bégu.

Additional information

Communicated by R. Bock.

Electronic supplementary material

Below is the link to the electronic supplementary material.

294_2011_349_MOESM1_ESM.doc

Supplemental S1 DNA sequence comparison of cox1 group I introns from the fern O. regalis (GenBank JF681372) and the bryophyte M. polymorpha cox1i395 (Oda, et al. 1992). Intron sequences are in upper case and exonic sequences in lower case. Nucleotide identity is indicated by dots. Motifs P1 to P9, which are involved in base-pairing in the secondary structure of group I introns, were defined as reported by Ohta et al. (1993). Brackets indicate conserved core sequences P, Q, R and S. LAGLI-DADG endonuclease motifs are indicated by a thick line above the sequence. Stop codon in the putative encoded-ORF is underlined and indicated by an asterisk. The insertion of a dinucleotide (+2) that creates a premature stop codon in Osmunda putative-ORF is indicated. The predicted (C/T) editing sites in Osmunda group I intron are indicated by vertical arrows. (DOC 281 kb)

294_2011_349_MOESM2_ESM.doc

Supplemental S2 Consequence of RNA editing on the putative COX1 protein. The 66 edited codons in the mature transcripts are numbered according to the M. polymorpha ORF. Edited nucleotides are underlined in lower case. The data were obtained from sequence analysis of 31 isolated cDNA clones (GenBank JF681373). (DOC 95 kb)

294_2011_349_MOESM3_ESM.doc

Supplemental S3 Scheme of cox1 gene from different land plant species. The introns interrupting cox1 ORF are indicated by arrows. Black arrows with open circles indicate group I introns and arrows with filled circle indicate the presence of group II introns. E denotes the presence of an intron-encoded LAGLIDADG endonuclease and M indicates the presence of an RT-maturase ORF. Triangles indicate the intervening sequences orthologous to fungi mitochondrial introns. (DOC 1030 kb)

294_2011_349_MOESM4_ESM.doc

Supplemental S4 Scheme of cox1i395 group I introns from five fern species compared to the bryophyte Marchantia polymorpha (Mp) homologous intron. The variations between introns reside essentially in insertion (red triangles) or deletions (blue triangles) that affect the continuity of the putative LAGLIDADG type endonuclease encoded by the intron. Interrupted ORFs are indicated in grey. Blechnum gibbum (Bg), Dryopteris cycadina (Dc), Polypodium vulgare (Pv), Osmunda regalis (Or) and Equisetum arvense (Ea). (DOC 1010 kb)

Supplemental S5: Primers used in this work. (DOC 41 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bégu, D., Castandet, B. & Araya, A. RNA editing restores critical domains of a group I intron in fern mitochondria. Curr Genet 57, 317–325 (2011). https://doi.org/10.1007/s00294-011-0349-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-011-0349-z

Keywords

Search

Navigation