Skip to main content
SpringerLink
Log in

Evolutionary origin of a plant mitochondrial group II intron from a reverse transcriptase/maturase-encoding ancestor

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Group II introns are widespread in plant cell organelles. In vivo, most if not all plant group II introns do not self-splice but require the assistance of proteinaceous splicing factors. In some cases, a splicing factor (also referred to as maturase) is encoded within the intronic sequence and produced by translation of the (excised) intron RNA. However, most present-day group II introns in plant organellar genomes do not contain open reading frames (ORFs) for splicing factors, and their excision may depend on proteins encoded by other organellar introns or splicing factors encoded in the nuclear genome. Whether or not the ancestors of all of these noncoding organellar introns originally contained ORFs for maturases is currently unknown. Here we show that a noncoding intron in the mitochondrial cox2 gene of seed plants is likely to be derived from an ancestral reverse transcriptase/maturase-encoding form. We detected remnants of maturase and reverse transcriptase sequences in the 2.7 kb cox2 intron of Ginkgo biloba, the only living species of an ancient gymnosperm lineage, suggesting that the intron originally harbored a splicing factor. This finding supports the earlier proposed hypothesis that the ancient group II introns that invaded organellar genomes were autonomous genetic entities in that they encoded the factor(s) required for their own excision and mobility.

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

  • Albertazzi FJ, Kudla J, Bock R (1998) The cox2 locus of the primitive angiosperm plant Acorus calamus: molecular structure, transcript processing and RNA editing. Mol Gen Genet 259:591–600

    Article  PubMed  Google Scholar 

  • Albrizio M, de Gara L, De Benedetto C, Arrigoni O, Gallerani R (1994) Investigations of the coxII intron structure in the mitochondrial genomes of angiosperms. Plant Sci 100:179–186

    Article  Google Scholar 

  • Anziano PQ, Butow RA (1991) Splicing-defective mutants of the yeast mitochondrial coxI gene can be corrected by transformation with a hybrid maturase gene. Proc Natl Acad Sci USA 88:5592–5596

    Article  PubMed  Google Scholar 

  • Belfort M (1991) Self-splicing introns in prokaryotes: migrant fossils? Cell 64:9–11

    Article  PubMed  Google Scholar 

  • Belfort M, Perlman PS (1995) Mechanisms of intron mobility. J Biol Chem 270:30237–30240

    Article  PubMed  Google Scholar 

  • Bergthorsson U, Adams KL, Thomason B, Palmer JD (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424:197–201

    Article  PubMed  Google Scholar 

  • Bock R (2001) RNA editing in plant mitochondria and chloroplasts. In: Bass B (ed) Frontiers in molecular biology: RNA editing, Oxford University Press, NewYork, pp 38–60

    Google Scholar 

  • Bonen L, Vogel J (2001) The ins and outs of group II introns. Trends Genet 17:322–323

    Article  PubMed  Google Scholar 

  • Bonen L, Boer PH, Gray MW (1984) The wheat cytochrome oxidase subunit II gene has an intron and three radical amino acid changes relative to maize. EMBO J 3:2531–2536

    PubMed  Google Scholar 

  • Cho Y, Qiu Y-L, 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  Google Scholar 

  • Chowira BM, Berzal-Herranz A, Burke JM (1994) Novel RNA polymerization reaction catalyzed by a group I ribozyme. EMBO J 12:3599–3605

    Google Scholar 

  • Copertino DW, Hallick RB (1993) Group II and group III introns of twintrons: potential relationship with nuclear pre-mRNA introns. Trends Biochem Sci 18:467–471

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Covello PS, Gray MW (1992) Silent mitochondrial and active nuclear genes for subunit 2 of cytochrome c oxidase (cox2) in soybean: evidence for RNA-mediated gene transfer. EMBO J 11:3815–3820

    PubMed  Google Scholar 

  • Curcio MJ, Belfort M (1996) Retrohoming: cDNA-mediated mobility of group II introns requires a catalytic RNA. Cell 84:9–12

    Article  PubMed  Google Scholar 

  • Davis CC, Wurdack KJ (2004) Host-to-parasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales. Science 305:676–678

    Article  PubMed  Google Scholar 

  • Deshpande NN, Hollingsworth M, Herrin DL (1995) The atpF group-II intron-containing gene from spinach chloroplasts is not spliced in transgenic Chlamydomonas chloroplasts. Curr Genet 28:122–127

    Article  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Dürrenberger F, Rochaix J-D (1991) Chloroplast ribosomal intron of Chlamydomonas reinhardtii: in vitro self-splicing, DNA endonuclease activity and in vivo mobility. EMBO J 10:3495–3501

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Gutierres S, Lelandais C, De Paepe R, Vedel F, Chetrit P (1997) A mitochondrial sub-stoichiometric orf87–nad3–nad1 exonA co-transcription unit present in Solanaceae was amplified in the genus Nicotiana. Curr Genet 31:55–62

    Article  PubMed  Google Scholar 

  • Hess WR, Hoch B, Zeltz P, Hübschmann T, Kössel H, Börner T (1994) Inefficient rpl2 splicing in barley mutants with ribosome-deficient plastids. Plant Cell 6:1455–1465

    Article  PubMed  Google Scholar 

  • Hetzer M, Wurzer G, Schweyen RJ, Mueller MW (1997) Trans-activation of group II intron splicing by nuclear U5 snRNA. Nature 386:417–420

    Article  PubMed  Google Scholar 

  • Hiesel R, Brennicke A (1983) Cytochrome oxidase subunit II gene in mitochondria of Oenothera has no intron. EMBO J 2:2173–2178

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Jenkins BD, Barkan A (2001) Recruitment of a peptidyl-tRNA hydrolase as a facilitator of group II intron splicing in chloroplasts. EMBO J 20:872–879

    Article  PubMed  Google Scholar 

  • Jenkins BD, Kulhanek DJ, Barkan A (1997) Nuclear mutations that block group II RNA splicing in maize chloroplasts reveal several intron classes with distinct requirements for splicing factors. Plant Cell 9:283–296

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Kudla J, Albertazzi FJ, Blazevic Hermann M, Bock R (2002) Loss of the mitochondrial cox2 intron 1 in a family of monocotyledonous plants and utilization of mitochondrial intron sequences for the construction of a nuclear intron. Mol Genet Genomics 267:223–240

    Article  PubMed  Google Scholar 

  • Kuhsel MG, Stickland R, Palmer JD (1990) An ancient group I intron shared by eubacteria and chloroplasts. Science 250:1570–1573

    PubMed  Google Scholar 

  • Laroche J, Li P, Maggia L, Bousquet J (1997) Molecular evolution of angiosperm mitochondrial introns and exons. Proc Natl Acad Sci USA 94:5722–5727

    Article  PubMed  Google Scholar 

  • Li F, Holloway SP, Lee J, Herrin DL (2002) Nuclear genes that promote splicing of group I introns in the chloroplast 23S rRNA and psbA genes in Chlamydomonas reinhardtii. Plant J 32:467–480

    Article  PubMed  Google Scholar 

  • Liere K, Link G (1995) RNA-binding activity of the matK protein encoded by the chloroplast trnK intron from mustard (Sinapis alba L.). Nucleic Acids Res 23:917–921

    PubMed  Google Scholar 

  • Mann V, Ekstein I, Nissen H, Hiser C, McIntosh L, Hirschberg J (1991) The cytochrome oxidase II gene in mitochondria of the sugar-beet Beta vulgaris L.. Plant Mol Biol 17:559–566

    Article  PubMed  Google Scholar 

  • Marienfeld JR, Unseld M, Brandt P, Brennicke A (1997) Viral nucleic acid sequence transfer between fungi and plants. Trends Genet 13:260–261

    Article  PubMed  Google Scholar 

  • Michel F, Ferat J-L (1995) Structure and activities of group II introns. Annu Rev Biochem 64:435–461

    Article  PubMed  Google Scholar 

  • Michel F, Umesono K, Ozeki H (1989) Comparative and functional anatomy of group II catalytic introns—a review. Gene 82:5–30

    Article  PubMed  Google Scholar 

  • Mohr G, Lambowitz AM (2003) Putative proteins related to group II intron reverse transcriptase/maturases are encoded by nuclear genes in higher plants. Nucleic Acids Res 31:647–652

    Article  PubMed  Google Scholar 

  • Mohr G, Perlman PS, Lambowitz AM (1993) Evolutionary relationships among group II intron-encoded proteins and identification of a conserved domain that may be related to maturase function. Nucleic Acids Res 21:4991–4997

    PubMed  Google Scholar 

  • Mower JP, Stefanovic S, Young GJ, Palmer JD (2004) Gene transfer from parasitic to host plants. Nature 432:165–166

    Article  Google Scholar 

  • Mulligan RM, Williams MA, Shanahan MT (1999) RNA editing site recognition in higher plant mitochondria. J Hered 90:338–344

    Article  PubMed  Google Scholar 

  • Neuhaus H, Link G (1987) The chloroplast tRNALys(UUU) gene from mustard (Sinapis alba) contains a class II intron potentially coding for a maturase-related polypeptide. Curr Genet 11:251–257

    Article  PubMed  Google Scholar 

  • Nugent JM, Palmer JD (1991) RNA mediated transfer of the gene coxII from the mitochondrion to the nucleus during flowering plant evolution. Cell 66:473–481

    Article  PubMed  Google Scholar 

  • Ostheimer GJ, Williams-Carrier R, Belcher S, Osborne E, Gierke J, Barkan A (2003) Group II intron splicing factors derived by diversification of an ancient RNA-binding domain. EMBO J 22:3919–3929

    Article  PubMed  Google Scholar 

  • Padgett RA, Podar M, Boulanger SC, Perlman PS (1994) The stereochemical course of group II intron self-splicing. Science 266:1685–1688

    PubMed  Google Scholar 

  • Perron K, Goldschmidt-Clermont M, Rochaix J-D (1999) A factor related to pseudouridine synthases is required for chloroplast group II intron trans-splicing in Chlamydomonas reinhardtii. EMBO J 18:6481–6490

    Article  PubMed  Google Scholar 

  • Perron K, Goldschmidt-Clermont M, Rochaix J-D (2004) A multiprotein complex involved in chloroplast group II intron splicing. RNA 10:704–711

    Article  PubMed  Google Scholar 

  • Pruitt KD, Hanson MR (1989) Cytochrome oxidase subunit II sequences in petunia mitochondria: two intron containing genes and an intron-less pseudo gene associated with cytoplasmic male sterility. Curr Genet 16:281–291

    Article  PubMed  Google Scholar 

  • Pruitt KD, Hanson MR (1991) Splicing of the Petunia cytochrome oxidase subunit II intron. Curr Genet 19:191–197

    Article  PubMed  Google Scholar 

  • Pyle AM, Cech TR (1991) Ribozyme recognition of RNA by tertiary interactions with specific ribose 2′-OH groups. Nature 350:628

    Article  PubMed  Google Scholar 

  • Qiu Y-L, Cho Y, Cox JC, Palmer JD (1998) The gain of three mitochondrial introns identifies liverworts as the earliest land plants. Nature 394:671–674

    Article  PubMed  Google Scholar 

  • Rabbi MF, Wilson KG (1993) The mitochondrial coxII intron has been lost in two different lineages of dicots and altered in others. Am J Bot 80:1216–1223

    Article  Google Scholar 

  • Rivier C, Goldschmidt-Clermont M, Rochaix J-D (2001) Identification of an RNA-protein complex involved in chloroplast group II intron trans-splicing in Chlamydomonas reinhardtii. EMBO J 20:1765–1773

    Article  PubMed  Google Scholar 

  • Rothenberg M, Hanson MR (1987) Different transcript abundance of two divergent ATP synthase subunit 9 genes in the mitochondrial genome of Petunia hybrida. Mol Gen Genet 209:21–27

    Article  Google Scholar 

  • Schuster W, Brennicke A (1987) Plastid, nuclear and reverse transcriptase sequences in the mitochondrial genome of Oenothera: is genetic information transferred between organelles via RNA? EMBO J 6:2857–2863

    PubMed  Google Scholar 

  • Scott WG, Klug A (1996) Ribozymes: structure and mechanism in RNA catalysis. Trends Biochem Sci 21:220–223

    Article  PubMed  Google Scholar 

  • Sheveleva EV, Hallick RB (2004) Recent horizontal intron transfer to a chloroplast genome. Nucleic Acids Res 32:803–810

    Article  PubMed  Google Scholar 

  • Sugita M, Sugiura M (1996) Regulation of gene expression in chloroplasts of higher plants. Plant Mol Biol 32:315–326

    Article  PubMed  Google Scholar 

  • Sugiura M (1992) The chloroplast genome. Plant Mol Biol 19:149–168

    Article  PubMed  Google Scholar 

  • Szczepanek T, Lazowska J (1996) Replacement of two non-adjacent amino acids in the S. cerevisiae bi2 intron-encoded RNA maturase is sufficient to gain a homing-endonuclease activity. EMBO J 15:3758–3767

    PubMed  Google Scholar 

  • Thomson MC, Macfarlane JL, Beagley CT, Wolstenholme DR (1994) RNA editing of mat-r transcripts in maize and soybean increases similarity of the encoded protein to fungal and bryophyte group II intron maturases: evidence that mat-r encodes a functional protein. Nucleic Acids Res 22:5745–5752

    PubMed  Google Scholar 

  • Till B, Schmitz-Linneweber C, Williams-Carrier R, Barkan A (2001) Crs1 is a novel group II intron splicing factor that was derived from a domain of ancient origin. RNA 7:1227–1238

    Article  PubMed  Google Scholar 

  • Toor N, Hausner G, Zimmerly S (2001) Coevolution of group II intron RNA structures with their intron-encoded reverse transcriptases. RNA 7:1142–1152

    Article  PubMed  Google Scholar 

  • Vaughn JC, Mason MT, Sper-Whitis GL, Kuhlman P, Palmer JD (1995) Fungal origin by horizontal gene transfer of a plant mitochondrial group I intron in the chimeric coxI gene of Peperomia. J Mol Evol 41:563–572

    Article  PubMed  Google Scholar 

  • Vogel J, Hübschmann T, Börner T, Hess WR (1997) Splicing and intron-internal RNA editing of trnK-matK transcripts in barley plastids: support for matK as an essential splicing factor. J Mol Biol 270:179–187

    Article  PubMed  Google Scholar 

  • Vogel J, Börner T, Hess WR (1999) Comparative analysis of splicing of the complete set of chloroplast group II introns in three higher plant mutants. Nucleic Acids Res 27:3866–3874

    Article  PubMed  Google Scholar 

  • Winkler M, Kück U (1991) The group IIB intron from the green alga Scenedesmus obliquus mitochondrion: molecular characterization of the in vitro splicing products. Curr Genet 20:495–502

    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 sequence. Cell 65:473–482

    Article  PubMed  Google Scholar 

  • Won H, Renner SS (2003) Horizontal gene transfer from flowering plants to Gnetum. Proc Natl Acad Sci USA 100:10824–10829

    Article  PubMed  Google Scholar 

  • Zhou Z, Zheng S (2003) The missing link in Ginkgo evolution. Nature 423:821–822

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dragica Blazević for excellent technical assistance during the early phase of this work. This research was supported by grants from the Deutsche Forschungsgemeinschaft (DFG) to RB and JK.

Author information

Authors and Affiliations

  1. Westfälische Wilhelms-Universität Münster, Institut für Biochemie und Biotechnologie der Pflanzen, Hindenburgplatz 55, 48143, Münster, Germany

    Daniela Ahlert & Ralph Bock

  2. Max-Planck-Institut für Molekulare Pflanzenphysiologie, Am Mühlenberg 1, 14476, Potsdam-Golm, Germany

    Katrin Piepenburg & Ralph Bock

  3. Westfälische Wilhelms-Universität Münster, Institut für Botanik und Botanischer Garten, Schlossplatz 4, 48149, Münster, Germany

    Jörg Kudla

Authors
  1. Daniela Ahlert
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katrin Piepenburg
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jörg Kudla
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ralph Bock
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ralph Bock.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ahlert, D., Piepenburg, K., Kudla, J. et al. Evolutionary origin of a plant mitochondrial group II intron from a reverse transcriptase/maturase-encoding ancestor. J Plant Res 119, 363–371 (2006). https://doi.org/10.1007/s10265-006-0284-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-006-0284-0

Keywords

Search

Navigation