Skip to main content
Log in

Promiscuous mitochondrial group II intron sequences in plant nuclear genomes

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Gene translocations from the organelles to the nucleus are postulated by the endosymbiont hypothesis. We here report evidence for sequence insertions in the nuclear genomes of plants that are derived from noncoding regions of the mitochondrial genome. Fragments of mitochondrial group II introns are identified in the nuclear genomes of tobacco and a bean species. The duplicated intron sequences of 75–140 bp are derived from cis- and trans-splicing introns of genes encoding subunits 1 and 5 of the NADH dehydrogenase. The mitochondrial sequences are inserted in the vicinities of a lectin gene, different glucanase genes and a gene encoding a subunit of photosystem II. Sequence similarities between the nuclear and mitochondrial copies are in the range of 80 to 97%, suggesting recent transfer events that occurred in the basic glucanase genes before and in the lectin gene after the gene duplications in the evolution of the nuclear gene families. Overlapping regions of the same introns are in two instances also involved in intramitochondrial sequence duplications.

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.

Similar content being viewed by others

References

  • Ayliffe MA, Timmis JN (1992) Plastid DNA sequence homologies in the tobacco nuclear genome. Mol Gen Genet 236:105–112

    Google Scholar 

  • Brennicke A, Grohmann L, Hiesel R, Knoop V, Schuster W (1993) The mitochondrial genome on its way to the nucleus: different stages of gene transfer in higher plants. FEBS Letters 325:140–145

    Google Scholar 

  • Chapdelaine Y, Bonen L (1991) The wheat mitochondrial gene for subunit I of the NADH dehydrogenase complex: A trans-splicing model for this gene-in-pieces. Cell 65:465–472

    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 111:3815–3820

    Google Scholar 

  • Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395

    Google Scholar 

  • Ecke W, Schmitz U, Michaelis G (1990) The mitochondrial nad5 gene of sugar beet (Beta vulgaris) encoding a subunit of the respiratory NADH dehydrogenase. Curr Genet 18:133–139

    Google Scholar 

  • Fukuchi M, Shikanai T, Kossykh VG, Yamada Y (1991) Analysis of nuclear sequences homologous to the B4 plasmid-like DNA of rice mitochondria; evidence for sequence transfer from mitochondria to nuclei. Curr Genet 20:487–494

    Google Scholar 

  • Gray MW (1992) The endosymbiont hypothesis revisited. In: Wolstenholme DR, Jeon KW (eds) Mitochondrial genomes. Academic Press, San Diego, pp 233–357

    Google Scholar 

  • Grohmann L, Brennicke A, Schuster W (1992) The mitochondrial gene encoding ribosomal protein S 12 has been translocated to the nuclear genome in Oenothera. Nucleic Acids Res 20:5641–5646

    Google Scholar 

  • Harada JJ, Spadoro-Tank J, Maxwell JC, Schnell DJ, Etzler ME (1990) Two lectin genes differentially expressed in Dolichos biflorus differ primarily by a 116-base pair sequence in their 5′ flanking regions. J Biol Chem 265:4997–5001

    Google Scholar 

  • Hua S, Dube SK, Barnett NM, Kung S-d (1991) Nucleotide sequence of gene oee2-A and its cDNA encoding 23 kDa polypeptide of the oxygen-evolving complex of photosystem II in tobacco. Plant Mol Biol 17:551–553

    Google Scholar 

  • Hua S-B, Dube SK, Barnett NM, Kung S-d (1992) Photosystem II 23 kDa polypeptide of oxygen-evolving complex is encoded by a multigene family in tobacco. Plant Mol Biol 18:997–999

    Google Scholar 

  • Hunt MD, Newton KJ (1991) The NCS3 mutation: genetic evidence for the expression of ribosomal protein genes in Zea mays mitochondria. EMBO J 10:1045–1052

    Google Scholar 

  • Knoop V, Brennicke A (1991) A mitochondrial intron sequence in the 5′-flanking region of a plant nuclear lectin gene. Curr Genet 20:423–425

    Google Scholar 

  • Knoop V, Schuster W, Wissinger B, Brennicke A (1991) Trans splicing integrates an exon of 22 nucleotides into the nad5 mRNA in higher plant mitochondria. EMBO J 10:3483–3493

    Google Scholar 

  • Lamattina L, Grienenberger JM (1991) RNA editing of the transcript coding for subunit 4 of NADH dehydrogenase in wheat mitochondria: uneven distribution of the editing sites among the four exons. Nucleic Acids Res 19:3275–3282

    Google Scholar 

  • Linthorst HIM, Melchers LS, Mayer A, van Roekel JSC, Cornelissen BIC, Bol JF (1990) Analysis of gene families encoding acid and basic β-1,3-glucanases of tobacco. Proc Natl Acad Sci U S A 87:8756–8760

    Google Scholar 

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

    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

    Google Scholar 

  • Palmer JD, Herbon LA (1988) Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. J Mol Evol 28:87–97

    Google Scholar 

  • Pearson WR, Lipman DJ (1988) Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A 85:2444–2448

    Google Scholar 

  • Pereira de Souza A, Jubier M-F, Delcher E, Lancelin D, Lejeune B (1991) A trans-splicing model for the expression of the tripartite nad5 gene in wheat and maize mitochondria. Plant Cell 3:1363–1378

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 74:5463–5467

    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

    Google Scholar 

  • Sperisen C, Ryals J, Meins F (1991) Comparison of cloned genes provides evidence for intergenomic exchange of DNA in the evolution of a tobacco glucan endo-1,3-β-glucosidase gene family. Proc Natl Acad Sci U S A 88:1820–1824

    Google Scholar 

  • Stern DB, Bang AG, Thompson WF (1986) The watermelon mitochondrial URF-1 gene: Evidence for a complex structure. Curr Genet 10:857–869

    Google Scholar 

  • Sun C-W, Callis J (1993) Recent stable insertion of mitochondrial DNA into an Arabidopsis polyubiquitin gene by nonhomologous recombination. Plant Cell 5:97–107

    Google Scholar 

  • Wissinger B, Hiesel R, Schuster W, Brennicke A (1988) The NADH-dehydrogenase subunit 5 gene in Oenothera mitochondria contains two introns and is co-transcribed with the 5S rRNA gene. Mol Gen Genet 212:56–65

    Google Scholar 

  • Wissinger B, Hiesel R, Schobel W, Unseld M, Brennicke A, Schuster W (1991a) Duplicated sequence elements and their function in plant mitochondria. Z Naturforsch [C] 46c:709–716

    Google Scholar 

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

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Correspondence to: V. Knoop

Rights and permissions

Reprints and permissions

About this article

Cite this article

Knoop, V., Brennicke, A. Promiscuous mitochondrial group II intron sequences in plant nuclear genomes. J Mol Evol 39, 144–150 (1994). https://doi.org/10.1007/BF00163803

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00163803

Key words

Navigation