Skip to main content
SpringerLink
Log in

Expression of a β-glucosidase gene results in increased accumulation of salicylic acid in transgenic Nicotiana tabacum cv. Xanthi-nc NN genotype

  • Genetic Transformation and Hybridization
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

A β-glucosidase gene (bglA) from Butyrivibrio fibrisolvens H17c was cloned into the binary vector pGA482 under the control of the 35S Cauliflower Mosaic Virus (CaMV) promoter. A second construct was generated for accumulation of the bglA gene product in the vacuole of transformed tobacco plants. Reverse transcription – polymerase chain reaction analysis demonstrated that the bglA gene was expressed in 71% of cytosol-targeted and 67% of vacuole-targeted transgenic tobacco T1 plants. T1 transgenic plants (pGLU100 and pGLU200) exhibited elevated levels of free salicylic acid (SA) with a concomitant significant decrease in the level of glucosylsalicylic acid (GSA) compared to the untransformed tobacco plants and tobacco plants transformed with the empty vector (pGA482). Following inoculation with Tobacco Mosaic Virus (TMV), lesion area was 51% smaller in pGLU100 plants and 60% smaller in pGLU200 plants compared to inoculated untransformed and negative control plants.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • An G (1985) High efficiency transformation of cultured tobacco cells. Plant Physiol 79:568–570

    PubMed  Google Scholar 

  • Bednarek SY, Raikhel NV (1991) The barley lectin carboxyl-terminal propeptide is a vacuolar protein sorting determinant in plants. Plant Cell 3:1195–1206

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Malamy J, Henning J, Conrath U, Sanchez-Casas P, Silva H, Ricigliano J, Klessig DK (1995) Induction, modification, and transduction of the salicylic acid signal in plant defense responses. Proc Natl Acad Sci USA 92:4134–4137

    Article  PubMed  CAS  Google Scholar 

  • Clarke SM, Mur LA, Wood JE, Scott IM (2004) Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. Plant J 38:432–447

    Article  PubMed  CAS  Google Scholar 

  • Dean JSR, Mohammed L (2003) Formation and vacuolar localization of salicylic acid glucose conjugates in soybean cell suspension cultures. Physiol Plant 118:328–336

    Article  CAS  Google Scholar 

  • Dean JV, Mills JD (2004) Uptake of salicylic acid 2-O-β-d-glucose into soybean tonoplast vesicles by an ATP-binding cassette transporter-type mechanism. Physiol Plant 120:603–612

    Article  PubMed  CAS  Google Scholar 

  • Dean JSR, Mohammed L, Fitzpatrick T (2005) The formation, vacuolar localization, and tonoplast transport of salicylic acid glucose conjugates in tobacco cell suspension cultures. Planta 221:287–296

    Article  PubMed  CAS  Google Scholar 

  • Delaney T, Uknes S, Vernooi B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gut-Rella M, Kessmann H, Ward E, Ryals J (1994) A central role of salicylic acid in plant disease resistance. Science 266:1247--1250

    Google Scholar 

  • Denecke J, Botterman J, Deblaere R (1990) Protein secretion in plant cells can occur via a default pathway. Cell 2:51–59

    CAS  Google Scholar 

  • Dixon RA (2001) Natural products and plant disease resistance. Nature 411:843–847

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Enyedi AJ, Raskin I (1993) Induction of UDP-glucose: Salicylic acid glucosyltransferase activity in tobacco mosaic virus-inoculated tobacco (Nicotiana tabacum) leaves. Plant Physiol 101:1375–1380

    PubMed  CAS  Google Scholar 

  • Enyedi AJ, Yalpani N, Silverman P, Raskin I (1992) Localization, conjugation, and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc Natl Acad Sci USA 89:2480–2484

    Article  PubMed  CAS  Google Scholar 

  • Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754–756

    Article  CAS  PubMed  Google Scholar 

  • Hennig J, Malamy J, Grynkiewicz G, Indulski J, Klessig DF (1993) Interconversion of the salicylic acid signal and its glucoside in tobacco. Plant J 4:593–600

    Article  PubMed  CAS  Google Scholar 

  • Horsch RB, Fry JE, Hoffman NL, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general method of transferring genes into plants. Science 227:1229–1231

    Article  CAS  Google Scholar 

  • Kawano T, Tanaka S, Kadono T, Muto S (2004a) Salicylic acid glucoside acts as a slow inducer of oxidativ burst in tobacco suspension culture. Zeitschrift fur Naturforschung 59c:684–692

    Google Scholar 

  • Kawano T, Furuichi T, Muto S (2004b) Controlled salicylic acid levels and corresponding signaling mechanisms in plants. Plant Biotech 21:319–335

    CAS  Google Scholar 

  • Lawton K, Weymann K, Friedrich L, Vernooij B, Uknes S, Ryals J (1995) Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol Plant Microbe Interact 8:863–870

    PubMed  CAS  Google Scholar 

  • Lee H, Raskin I (1998) Glucosylation of salicylic acid in Nicotiana tabacum cv. Xanthi-nc. Phytopathology 88:692–697

    CAS  PubMed  Google Scholar 

  • Lerner DR, Raikhel NV (1989) Cloning and characterization of root-specific barley lectin. Plant Physiol 91:124–129

    PubMed  CAS  Google Scholar 

  • Lin LL, Rumbak E, Zappe H, Thomson JA, Woods DR (1990) Cloning, sequencing and analysis of expression of a Butyrivibrio fibrisolvens gene encoding a β-glucosidase. J Gen Microbiol 136:1567–1576

    PubMed  CAS  Google Scholar 

  • Malamy J, Carr JP, Klessig DF, Raskin I (1990) Salicylic acid: A likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1001–1004

    Article  Google Scholar 

  • Mauch F, Mauch MB, Gaille C, Kull B, Hass D, Reimmann C (2001) Manipulation of salicylate content in Arabidopsis thaliana by the expression of an engineered salicylate synthase. Plant J 25:67–77

    Article  PubMed  CAS  Google Scholar 

  • Metraux J, Burkhart W, Moyer M, Dincher S, Middlesteasdt W, Williams S, Payne G, Carnes M, Ryals J (1989) Isolation of a complementary DNA encoding a chitinase with structural homology to a lysozyme/chitinase. Proc Natl Acad Sci USA 86:896--900

    Google Scholar 

  • Metraux J, Signer H, Ryals J, Ward E, Wyss-Benz M, Gaudin J, Raschdorf K, Schmid E, Blum W, Inverardi B (1990) Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250:1004--1006

    Google Scholar 

  • Mur LAJ, Bi YM, Darby RM, Firek S, Draper J (1997) Compromising early salicylic acid accumulation delays the hypersensitive response and increases viral dispersal during lesion establishment in TMV-infected tobacco. Plant J 12:1113–1126

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen JB, Hammerschmidt R, Zook MN (1991) Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv syringae. Plant Physiol 97:1342–1347

    Article  PubMed  CAS  Google Scholar 

  • Schneider M, Schweizer P, Meuwly P, Métraux JP (1996) Systemic acquired resistance in plants. In: Jeon KW (ed) International review of cytology, vol 168. Academic, San Diego, CA, pp 303–340

  • Schroeder MR, Borkhsenious ON, Matsuoka K, Nakamura K, Raikhel NV (1993) Colocalization of barley lectin and sporamin in vacuoles of transgenic tobacco plants. Plant Physiol 101:451–458

    Article  PubMed  CAS  Google Scholar 

  • Schulz M, Schnabl H, Manthe B, Schweihofen B, Casser I (1993) Uptake and detoxification salicylic acid by Vicia faba and Fagopyrum esculentum. Phytochemisry 33:291--294

  • Seo S, Ishizuka K, Ohashi Y (1995) Induction of salicylic acid β-glucosidase in tobacco leaves by exogenous salicylic acid. Plant Cell Physiol. 36:447--453

    Google Scholar 

  • Shulaev V, Leon J, Raskin I (1995) Is salicylic acid a translocated signal of systemic acquired resistance in tobacco? Plant Cell 7:1691–1701

    Article  PubMed  CAS  Google Scholar 

  • Van Wees S, Glazebrook J (2004) Loss of non-host resistance of Arabidopsis NahG to Pseudomonas syringae pv. phaseolicola is due to degradation products of salicylic acid. Plant J 33:733–742

    Article  Google Scholar 

  • Verberne MC, Verpoorte R, Bol JF, Mercado-Blanco J, Linthorst HJM (2000) Overproduction of salicylic acid in plants by bacterial transgenes results in enhanced resistance to pathogens. Nat Biotechnol 18:779–783

    Article  PubMed  CAS  Google Scholar 

  • Verberne MC, Brouwer N, Delbianco F, Linthorst HJM, Bol JF, Verpoorte R (2002) Method for the extraction of the volatile compound salicylic acid from tobacco leaf material. Phytochem Anal 13:45–50

    Article  PubMed  CAS  Google Scholar 

  • Vital A, Raikhel NV (1999) What do proteins need to reach different vacuoles? Trends Plant Sci 4:149–155

    Article  Google Scholar 

  • Wilkins TA, Bednarek SY, Raikhel NV (1990) Role of propeptide glycan in post-translational processing and transport of barley lectin to vacuoles in transgenic tobacco. Plant Cell 2:301–313

    Article  PubMed  CAS  Google Scholar 

  • Yalpani N, Altier DJ, Barbour E, Cigan AL, Scelonge CJ (2001) Production of 6-methylsalicylic acid by expression of a fungal polyketide synthase activates disease resistance in tobacco. Plant cell 13:1401–1409

    Article  PubMed  CAS  Google Scholar 

  • Yang YO, Shah J, Klessig DF (1997) Signal perception and transduction in plant defense responses. Genes Dev 11:1621–1639

    PubMed  CAS  Google Scholar 

  • Yin Z, Hennig J, Szwacka M, Malepszy S (2004) Tobacco PR-2d promoter is induced in transgenic cucumber in response to biotic and abiotic stimuli. Plant Physiol 161:621–629

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Ms. Talline Robadey and Dr. Wendy Tan for their assistance in the gene-sequencing project.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Western Michigan University, Kalamazoo, MI, 49008, USA

    Jiqiang Yao, Bethany Huot, Catherine Foune & Alexander Enyedi

  2. University of California Davis, Department of Viticulture and Enology, Davis, CA, 95616, USA

    Harshavardhan Doddapaneni

Authors
  1. Jiqiang Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bethany Huot
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Catherine Foune
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Harshavardhan Doddapaneni
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alexander Enyedi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexander Enyedi.

Additional information

Communicated by D. A. Somers

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yao, J., Huot, B., Foune, C. et al. Expression of a β-glucosidase gene results in increased accumulation of salicylic acid in transgenic Nicotiana tabacum cv. Xanthi-nc NN genotype. Plant Cell Rep 26, 291–301 (2007). https://doi.org/10.1007/s00299-006-0212-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-006-0212-8

Keywords

Search

Navigation