Skip to main content
SpringerLink
Log in

Anaerobic induction of the maize GapC4 promoter in poplar leaves requires light and high CO2

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The maize (Zea mays L.) glyceraldehyde-3-phosphate dehydrogenase gene 4 (GapC4) promoter confers anaerobic gene expression in tobacco (Nicotiana tabacum L.), potato (Solanum tuberosum L.) and Arabidopsis thaliana (L.) Heynh. Here we have investigated its expression in hybrid poplar (Populus tremula × P. alba). Our results show that the promoter is not expressed in leaves and stems under normoxic conditions while anaerobiosis induces reporter gene expression in leaves up to a level observed for the STLS-1 promoter from potato that is shown to confer leaf-specific gene expression in transgenic poplar. Anaerobic induction is cell autonomous and requires a CO2 atmosphere and light. As in tobacco, the GapC4 promoter in poplar is wound inducible. The induction by CO2 and light may reflect a natural situation because flooding, a natural cause of anaerobiosis, is often accompanied by high CO2 concentrations in the floodwater. Our results show that the GapC4 promoter is suitable as an anaerobic reporter and as an inducible gene expression system in poplar.

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. 3a–d.

Similar content being viewed by others

Abbreviations

CaMV:

cauliflower mosaic virus

GapC4 :

glyceraldehyde-3-phosphate dehydrogenase gene 4

GUS:

β-glucuronidase

4-MU:

methylumbelliferone

STLS-1:

stem- and leaf-specific promoter 1

References

  • An G (1987) Binary Ti vectors for plant transformation and promoter analysis. Methods Enzymol 153:292–305

    CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 7:248–254

    Article  Google Scholar 

  • Bradshaw HD Jr, Stettler RF (1993) Molecular genetics of growth and development in Populus: I. Triploidy in hybrid poplars. Theor Appl Genet 86:301–307

    Google Scholar 

  • Bradshaw HD Jr, Ceulemans R, Davis J, Stettler R (2000) Emerging model systems in plant biology: poplar (Populus) as a model forest tree. J Plant Growth Regul 19:306–313

    CAS  Google Scholar 

  • Bülow L, Köhler U, Cerff R, Hehl R, Düring K (1999) Induction of the maize GapC4 promoter in transgenic potato under anaerobiosis and in Erwinia carotovora-inoculated tuber tissue. Mol Plant Microbe Interact 12:182–188

    Google Scholar 

  • Dennis ES, Dolferus R, Ellis M, Rahman M, Wu Y, Hoeren FU, Grover A, Ismond KP, Good AG, Peacock WJ (2000) Molecular strategies for improving waterlogging tolerance in plants. J Exp Bot 51:89–97

    Article  CAS  PubMed  Google Scholar 

  • Drew MC (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annu Rev Plant Physiol Plant Mol Biol 48:223–250

    Google Scholar 

  • Ellis MH, Dennis ES, James Peacock W (1999) Arabidopsis roots and shoots have different mechanisms for hypoxic stress tolerance. Plant Physiol 119:57–64

    Article  CAS  PubMed  Google Scholar 

  • Feuillet C, Lauvergeat V, Deswarte C, Pilate G, Boudet A, Grima-Pettenati J (1995) Tissue- and cell-specific expression of a cinnamyl alcohol dehydrogenase promoter in transgenic poplar plants. Plant Mol Biol 27:651–667

    CAS  PubMed  Google Scholar 

  • Geffers R, Cerff R, Hehl R (2000) Anaerobiosis specific interaction of tobacco nuclear factors with cis-regulatory sequences in the maize GapC4 promoter. Plant Mol Biol 43:11–21

    Article  CAS  PubMed  Google Scholar 

  • Gray-Mitsumune M, Molitor EK, Cukovic D, Carlson JE, Douglas CJ (1999) Developmentally regulated patterns of expression directed by poplar PAL promoters in transgenic tobacco and poplar. Plant Mol Biol 39:657–669

    Article  CAS  PubMed  Google Scholar 

  • Hänsch R, Fessel DG, Witt C, Hesberg C, Hoffmann G, Walch-Liu P, Engels C, Kruse J, Rennenberg H, Kaiser WM, Mendel RR (2001) Tobacco plants that lack expression of functional nitrate reductase in roots show changes in growth rates and metabolite accumulation. J Exp Bot 52:1251–1258

    Article  PubMed  Google Scholar 

  • Hänsch R, Mendel RR, Cerff R, Hehl R (2003) Light-dependent anaerobic induction of the maize glyceraldehyde-3-phosphate dehydrogenase 4 (GapC4) promoter in Arabidopsis thaliana and Nicotiana tabacum. Ann Bot London 91:149–154

    Google Scholar 

  • Hawkins S, Samaj J, Lauvergeat V, Boudet A, Grima Pettenati J (1997) Cinnamyl alcohol dehydrogenase: identification of new sites of promoter activity in transgenic poplar. Plant Physiol 113:321–325

    CAS  Google Scholar 

  • Jackson MB (2002) Long-distance signalling from roots to shoots assessed: the flooding story. J Exp Bot 53:175–181

    Article  CAS  PubMed  Google Scholar 

  • Jefferson RA, Burgess SM, Hirsh D (1986) Beta glucuronidase from Escherichia coli as a gene-fusion marker. Proc Natl Acad Sci USA 83:8447–8451

    CAS  PubMed  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    CAS  PubMed  Google Scholar 

  • Jouanin L, Brasileiro ACM, Leple JC, Pilate G, Cornu D (1993) Genetic transformation: a short review of methods and their applications, results and perspectives for forest trees. Ann Sci For 50:325–336

    Google Scholar 

  • Köhler U, Liaud M-F, Mendel RR, Cerff R, Hehl R (1995) The maize GapC4 promoter confers anaerobic reporter gene expression and shows homology to the maize anthocyanin regulatory locus C1. Plant Mol Biol 29:1293–1298

    PubMed  Google Scholar 

  • Köhler U, Donath M, Mendel RR, Cerff R, Hehl R (1996a) Intron-specific stimulation of anaerobic gene expression and splicing efficiency in maize cells. Mol Gen Genet 251:252–258

    Article  PubMed  Google Scholar 

  • Köhler U, Mendel RR, Cerff R, Hehl R (1996b) A promoter for strong and ubiquitous anaerobic gene expression in tobacco. Plant J 10:175–183

    CAS  Google Scholar 

  • Kumar S, Fladung M (2000) Transgene repeats in aspen: molecular characterisation suggests simultaneous integration of independent T-DNAs into receptive hotspots in the host genome. Mol Gen Genet 264:20–28

    Article  CAS  PubMed  Google Scholar 

  • Leplé JC, Brasileiro ACM, Michel MF, Delmotte F, Jouanin L (1992) Transgenic poplars expression of chimeric genes using four different constructs. Plant Cell Rep 11:137–141

    CAS  Google Scholar 

  • Manjunath S, Sachs MM (1997) Molecular characterization and promoter analysis of the maize cytosolic glyceraldehyde 3-phosphate dehydrogenase gene family and its expression during anoxia. Plant Mol Biol 33:97–112

    CAS  PubMed  Google Scholar 

  • Miglietta F, Raschi A, Bettarini I, Resti R, Selvi F (1993) Natural CO2 springs in Italy: a resource for examining long-term response of vegetation to rising atmospheric CO2 concentrations. Plant Cell Environ 16:873–878

    CAS  Google Scholar 

  • Ober E, Sharp R (1996) A microsensor for direct measurements of O2 partial pressure within plant tissues. J Exp Bot 47:447–454

    CAS  Google Scholar 

  • Sachs M, Subbaiah C, Saab I (1996) Anaerobic gene expression and flooding tolerance in maize. J Exp Bot 47:1–15

    CAS  Google Scholar 

  • Samaj J, Hawkins S, Lauvergeat V, Grima-Pettenati J, Boudet A (1998) Immunolocalization of cinnamyl alcohol dehydrogenase 2 (CAD 2) indicates a good correlation with cell-specific activity of CAD 2 promoter in transgenic poplar shoots. Planta 204:437–443

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. a laboratory manual. Cold Spring Harbor Laboratory Press, NY

  • Stockhaus J, Eckes P, Rocha-Sosa M, Schell J, Willmitzer L (1987) Analysis of cis-active sequences involved in the leaf-specific expression of a potato gene in transgenic plants. Proc Natl Acad Sci USA 84:7943–7947

    CAS  Google Scholar 

  • Tognetti R, Minnocci A, Penuelas J, Raschi A, Jones MB (2000) Comparative field water relations of three Mediterranean shrub species co-occurring at a natural CO2 vent. J Exp Bot 51:1135–1146

    Article  CAS  PubMed  Google Scholar 

  • Töpfer R, Schell J, Steinbiss HH (1988) Versatile cloning vectors for transient gene expression and direct gene transfer in plant cells. Nucleic Acids Res 16:8725

    Google Scholar 

  • Vander Mijnsbrugge K, Van Montagu M, Inze D, Boerjan W (1996) Tissue-specific expression conferred by the S-adenosyl-l-methionine synthetase promoter of Arabidopsis thaliana in transgenic poplar. Plant Cell Physiol 37:1108–1115

    PubMed  Google Scholar 

  • Villar CA, Bonetto C (2000) Chemistry and nutrient concentrations of the Lower Parana River and its floodplain marshes during extreme flooding. Arch Hydrobiol 148:461–479

    CAS  Google Scholar 

  • Weigel D, Nilsson O (1995) A developmental switch sufficient for flower initiation in diverse plants. Nature 377:495–500

    CAS  PubMed  Google Scholar 

  • Zhang J, VanToai T, Huynh L, Preiszner J (2000) Development of flooding-tolerant Arabidopsis thaliana by autoregulated cytokinin production. Mol Breed 6:135–144

    Article  Google Scholar 

  • Zhu B, Coleman GD (2001) The poplar bark storage protein gene (Bspa) promoter is responsive to photoperiod and nitrogen in transgenic poplar and active in floral tissues, immature seeds and germinating seeds of transgenic tobacco. Plant Mol Biol 46:383–394

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant through the "Forschungsschwerpunkt Agrarbiotechnologie des Landes Niedersachsen". We are grateful to Michael Wettern for critical comments on the manuscript and to Ramona Joachim for excellent technical assistance.

Author information

Authors and Affiliations

  1. Institut für Genetik, Technische Universität Braunschweig, Spielmannstrasse 7, 38106, Braunschweig, Germany

    Rüdiger Cerff & Reinhard Hehl

  2. Institut für Pflanzenbiologie, Technische Universität Braunschweig, Humboldtstrasse 1, 38106, Braunschweig, Germany

    Robert Hänsch, Tobias Kurz, Jutta Schulze & Ralf R. Mendel

Authors
  1. Robert Hänsch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tobias Kurz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jutta Schulze
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ralf R. Mendel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rüdiger Cerff
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Reinhard Hehl
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Reinhard Hehl.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hänsch, R., Kurz, T., Schulze, J. et al. Anaerobic induction of the maize GapC4 promoter in poplar leaves requires light and high CO2 . Planta 218, 79–86 (2003). https://doi.org/10.1007/s00425-003-1074-8

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-003-1074-8

Keywords

Search

Navigation