Skip to main content
SpringerLink
Log in

Horizontal gene transfer: regulated expression of a tobacco homologue of the Agrobacterium rhizogenes rolC gene

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

Abstract

A tobacco homologue (trolC) of the rolC gene of the Agrobacterium rhizogenes Ri-plasmid was cloned and sequenced from Nicotiana tabacum L. cv. Havana 425. The coding region of trolC is similar in sequence (69–87% for DNA and 5489% for the deduced amino acid sequence) to rolC genes of the agropine, mannopine, and mikimopine strains of Ri-plasmids and the N. glauca rolC homologue. Southern analyses showed that trolC is encoded by a small gene family derived from the tomentosiformis ancestor of tobacco. This suggests that trolC resulted from an ancient transfer of DNA between A. rhizogenes and a progenitor of modern tobacco. Transcripts of trolC were detected in three morphologically distinct cultivars of tobacco. trolC mRNA accumulated in young leaves and shoot tips, but not in lower leaves and roots of mature plants. Accumulation of trolC mRNA in cultured leaf tissues was strongly down-regulated by auxin and induced by cytokinin. These results are of particular interest because they suggest that a gene of bacterial origin introduced during evolution can have a function in a modern plant.

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

Similar content being viewed by others

References

  • Ackermann C (1977) Pflanzen aus Agrobacterium rhizogenes-Tumoren an Nicotiana tabacum. Plant Sci Lett 8:23–30

    Google Scholar 

  • Aoki S, Kawaoka A, Sekine M, Ichikawa T, Fujita T, Shinmyo A, Syono K (1994) Sequence of the cellular T-DNA in the untransformed genome of Nicotiana glauca that is homologous to ORFs 13 and 14 of the Ri plasmid and analysis of its expression in genetic tumors of N. glauca x N. langsdorffii. Mol Gen Genet 243:706–710

    Google Scholar 

  • Binns A, Meins F Jr (1973) Habituation of tobacco pith cells for factors promoting cell division is heritable and potentially reversible. Proc Natl Acad Sci USA 70:2660–2662

    Google Scholar 

  • Binns AN, Thomashow MF (1988) Cell biology of Agrobacterium infection and transformation of plants. Annu Rev Micorbiol 42:575–606

    Google Scholar 

  • Chilton M-D, Tepfer DA, Petit A, David C, Casse-Delbart F, Tempe J (1982) Agrobacterium rhizogenes inserts T-DNA into the genomes of host plant root cells. Nature 295:432–434

    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 

  • Durand-Tardif M, Broglie R, Slightom J, Tepfer D (1985) Structure and expression of Ri T-DNA from Agrobacterium rhizogenes in Nicotiana tabacum. Organ and phenotypic specificity. J Mol Biol 186:557–564

    Google Scholar 

  • Felix G, Meins F Jr (1987) Ethylene regulation of β-1,3-glucanase in tobacco. Planta 172:386–392

    Google Scholar 

  • Fujii N, Uchimiya H (1991) Conditions favorable for the somatic embryogenesis on carrot cell culture enhance expression of the rolC promoter-GUS fusion gene. Plant Physiol 95:238–241

    Google Scholar 

  • Furrier IL Huffman GA, Amasino RM, Garfinkel DJ, Gordon MP, Nester EW (1986) An Agrobacterium transformation i the evolution of the genus Nicotiana. Nature 319:422–427

    Google Scholar 

  • Gerstel DU (1976) Tobacco. In: Simmonds NW (ed) Evolution of crop plants. Longman, London, pp 273–277

    Google Scholar 

  • Goodall G, Wiebauer K, Filipowicz W (1990) Analysis of pre-mRNA processing in transfected plant protoplasts. Methods Enzymol 181:148–160

    Google Scholar 

  • Goodspeed TH (1954) The genus Nicotiana. Chronica Botanica, Waltham, Mass., USA

    Google Scholar 

  • Green PJ (1993) Control of mRNA stability in higher plants. Plant Physiol 102:1065–1070

    Google Scholar 

  • Hansen G, Larribe M, Vaubert D, Tempe J, Biermann BJ, Montoya AL, Chilton M-D, Brevet J (1991) Agrobacterium rhizogenes pRi8196 T-DNA: mapping and DNA sequence of functions involved in mannopine synthesis and hairy root. Proc Natl Acad Sci USA 88:7763–7767

    Google Scholar 

  • Heidecker G, Messing J (1986) Structural analysis of plant genes. Annu Rev Plant Physiol 37:439–466

    Google Scholar 

  • Heinemann JA (1991) Genetics of gene transfer between species. Trends Genet 7:181–185

    Google Scholar 

  • Ichikawa T, Ozeki, Syono K (1990) Evidence for the expression of the rol genes of Nicotiana glauca in genetic tumors of N. glauca x N. langsdorffii. Mol Gen Genet 220:177–180

    Google Scholar 

  • Ichikawa T, Syono K (1991) Tobacco genetic tumors. Plant Cell Physiol 32:1123–1128

    Google Scholar 

  • Jorgensen R, Snyder C, Jones JDG (1987) T-DNA is organized predominantly in inverted repeat structures in plants transformed with A. tumefaciens C58 derivatives. Mol Gen Genet 207:471–477

    Google Scholar 

  • Katagiri F, Chua N-H (1992) Plant transcription factors: present knowledge and future challenges. Trends Genet 8:22–27

    Google Scholar 

  • Kiyokawa S, Kobayashi K, Kikuchi Y, Kamada H, Harada H (1994) Root-inducing region of mikimopine type Ri plasmid pRi1724. Plant Physiol 104:801–802

    Google Scholar 

  • Leach F, Aoyagi K (1991) Promoter analysis of the highly expressed rolC and rolD root-inducing genes of Agrobacterium rhizogenes: enhancer and tissue-specific DNA determinants are dissociated. Plant Sci 79:69–76

    Google Scholar 

  • Magrelli A, Langenkemper K, Dehio C, Schell J, Spena A (1994) Splicing of the rolA transcript of Agrobacterium rhizogenes in Arabidopsis. Science 266:1986–1988

    Google Scholar 

  • Maurel C, Brevet J, Barbier-Brygoo H, Guern J, Tempe J (1990) Auxin regulates the promoter of the root-inducing rolB gene of Agrobacterium rhizogenes in transgenic tobacco. Mol Gen Genet 223:58–64

    Google Scholar 

  • Meins F Jr, Lutz J, Binns AN (1980) Variation in the competence of tobacco pith cells for cytokinin habituation in culture. Differentiation 16:71–75

    Google Scholar 

  • Memelink J, Hoge JHC, Schilperoort RA (1987) Cytokinin stress changes the developmental regulation of several defence-related genes in tobacco. EMBO J 6:3579–3583

    Google Scholar 

  • Mohnen DA (1985) Regulation of glucanohydrolases in Nicotiana tabacum on the messenger RNA level. Ph.D. Dissertation, University of Illinois, Urbana, Ill., USA

    Google Scholar 

  • Mohnen D, Shinshi H, Felix G, Meins F Jr (1985) Hormonal regulation of β-1,3-glucanase messenger RNA levels in cultured tobacco tissues. EMBO J 4:1631–1635

    Google Scholar 

  • Neuhaus J-M, Ahl-Goy P, Hinz U, Flores S, Meins F Jr (1991) High-level expression of a tobacco chitinase gene in Nicotiana sylvestris. Susceptibility of transgenic plants to Cercospora nicotianae infection. Plant Molec Biol 16:141–151

    Google Scholar 

  • Okamuro JK, Goldberg RB (1985) Tobacco single-copy DNA is highly homologous to sequences present in the genomes of its diploid progenitors. Mol Gen Genet 198:290–298

    Google Scholar 

  • Rogers SO, Bendich AJ (1988) Extraction of DNA from plant tissues. In: Galvin SB, Schilperoort RA (eds) Plant molecular biology manual, Kluwer Academic Publishers, Dordrecht, pp 1–10

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. a laboratory manual. 2nd edition. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

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

    Google Scholar 

  • Schmülling T, Schell J, Spena A (1988) Single genes from Agrobacterium rhizogenes influence plant development. EMBO J 7:2621–2629

    Google Scholar 

  • Schmülling T, Schell J, Spena A (1989) Promoters of the rolA, B, and C genes of Agrobacterium rhizogenes are differentially regulated in transgenic plants. Plant Cell 1:665–670

    Google Scholar 

  • Shinshi H, Mohnen D, Meins F Jr (1987) Regulation of a plant pathogenesis-related enzyme: inhibition of chitinase and chitinase mRNA accumulation in cultured tobacco tissues by auxin and cytokinin. Proc Natl Acad Sci USA 84:89–93

    Google Scholar 

  • Shinshi H, Neuhaus J-M, Ryals J, Meins F Jr (1990) Structure of a tobacco endochitinase gene: evidence that different chitinases genes can arise by transposition of sequences encoding a cysteine-rich domain. Plant Molec Biol 14:357–368

    Google Scholar 

  • Slightom JL, Durand-Tardif M, Jouanin L, Tepfer D (1986) Nucleotide sequence analysis of TL-DNA of Agrobacterium rhizogenes agropine type plasmid. J Biol Chem 261:108–121

    Google Scholar 

  • Spanò L, Pomponi M, Costantino P, van Slogteren GMS, Tempe J (1982) Identification of T-DNA in the root-inducing plasmid of the agropine type Agrobacterium rhizogenes 1855. Plant Mol Biol 1:291–300

    Google Scholar 

  • Spena A, Schmülling T, Koncz C, Schell JS (1987) Independent and synergistic activity of rolA, B and C loci in stimulating abnormal growth in plants. EMBO J 6:3891–3899

    Google Scholar 

  • Sperisen C, Ryals J, Meins F Jr (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 USA 88:1820–1824

    Google Scholar 

  • Tepfer D (1984) Transformation of several species of higher plants by Agrobacterium rhizogenes: sexual transmission of the transformed geneotype and phenotype. Cell 37:959–967

    Google Scholar 

  • Van Buuren M, Neuhaus J-M, Shinshi H, Ryals J, Meins F Jr (1992) The structure and regulation of homeologous tobacco endo chitinase genes of Nicotiana sylvestris and N. tomentosiformis origin. Mol Gen Genet 232:460–469

    Google Scholar 

  • White FF, Ghidossi G, Gordon MP, Nester EW (1982) Tumor induction by Agrobacterium rhizogenes involves transfer of plasmid DNA to the plant genome. Proc Natl Acad Sci USA 79:3193–3197

    Google Scholar 

  • White FF, Taylor BH, Huffman GA, Gordon MP, Nester EW (1985) Molecular and genetic analysis of the transferred DNA regions of the root-inducing plasmid of Agrobacterium rhizogenes. J Bacteriol 164:33–44

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Friedrich Miescher-Institute, Box 2543, CH-4002, Basel, Switzerland

    Alain D. Meyer, Takanari Ichikawa & Frederick Meins Jr

Authors
  1. Alain D. Meyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takanari Ichikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Frederick Meins Jr
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by J. Schell

These authors contributed equally to this study

Rights and permissions

Reprints and permissions

About this article

Cite this article

Meyer, A.D., Ichikawa, T. & Meins, F. Horizontal gene transfer: regulated expression of a tobacco homologue of the Agrobacterium rhizogenes rolC gene. Molec. Gen. Genet. 249, 265–273 (1995). https://doi.org/10.1007/BF00290526

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00290526

Key words

Search

Navigation