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Low Temperature Tolerance of Tobacco Plants Transformed to Accumulate Proline, Fructans, or Glycine Betaine. Variable Chlorophyll Fluorescence Evidence

Photosynthetica volume 42, pages 179–185 (2004)Cite this article

Abstract

Tobacco (Nicotiana tabacum L.) has been transformed to accumulate different compatible solutes (proline, fructans, or glycine betaine) in order to improve its tolerance to abiotic stress. Photosynthetic activity of wild Type (wt) and transformed tobacco plants before and after freezing stress was studied by measuring chlorophyll (Chl) fluorescence. The JIP test of Chl fluorescence induction was used to analyze in details the functional activity of photosystem 2. No significant differences were found among wild Type and transgenic plants after 12 h of freezing. Both plant Types maintained the same values of the measured parameters [FV/FM, PI(CSM), ABS/RC, TR0/RC, ET/RC] after recovery of stress. The studied Chl fluorescence parameters decreased only for the wild Type plants, stressed for 24 h at −2 °C. The strong inhibition of photosynthetic reactions in the wt plant after 24 h of freezing could not be restored. The evaluated parameters of transgenic plants did not change significantly after 24 h at −2 °C and successfully survived freezing stress.

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References

  • Bajaj, S., Targolli, J., Liu, L.-F., Ho, T.-H.D., Wu, R.: Trans-genic approaches to increase dehydration-stress tolerance in plants.-Mol. Breed. 5: 493-503, 1999.

    Google Scholar 

  • Björkman, O., Demmig, B.: Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascu-lar plants of diverse origins.-Planta 170: 489-504, 1987.

    Google Scholar 

  • Bohnert, H.J., Jernsen, R.G.: Strategies for engineering water stress tolerance in plants.-Trends Biotechnol. 14: 89-97, 1996.

    Google Scholar 

  • Boyer, J.S.: Plant productivity and environment.-Science 218: 443-448, 1982.

    Google Scholar 

  • Deshnium, P., Los, D.A., Hayashi, H., Mustardy, L., Murata, N.: Transformation of Synechococcus with a gene for choline oxidase enhances tolerance to salt stress.-Plant mol. Biol. 29: 897-907, 1995.

    Google Scholar 

  • Enami, I., Kitamura, M., Tomo, T., Isokawa, Y., Ohta, H., Katoh, S.: Is the primary cause of thermal inactivation of oxy-gen evolution in spinach PS II membranes release of the ex-trinsic 33 kDa protein or of Mn?-Biochim. biophys. Acta 1186: 52-58, 1994.

    Google Scholar 

  • Goughlan, S.J., Heber, U.: The role of glycinebetaine in protec-tion of spinach thylakoids against freezing stress.-Planta 156: 62-69, 1982.

    Google Scholar 

  • Hincha, D.K., Hellwege, E.M., Heyer, A.G., Crowe, J.H.: Plant fructans stabilize phosphatidylcholine liposomes during freezing-drying.-Eur. J. Biochem. 267: 535-540, 2000.

    Google Scholar 

  • Hu, C.-A.A., Delauney, A.J., Verma, D.P.S.: A bifunctional enzyme (1-pyrroline-5-carboxylate-synthetase) catalyzes the first two steps in proline biosynthesis in plants.-Proc. nat. Acad. Sci. USA 89: 9354-9358, 1992.

    Google Scholar 

  • Huner, N.P.A., Öquist, G., Hurry, M.V., Krol, M., Falk, S., Griffith, M.: Photosynthesis, photoinhibition and low tem-perature acclimation in cold tolerant plants.-Photosynth. Res. 37: 19-39, 1993.

    Google Scholar 

  • Kishitany, S., Watanabe, K., Yasuda, S., Arakawa, K., Takabe, T.: Accumulation of glycinebetaine during cold acclimation and freezing tolerance in leaves of winter and spring barley plants.-Plant Cell Environ. 17: 89-97, 1994.

    Google Scholar 

  • Kitajama, M., Butler, W.L.: Quenching of chlorophyll fluores-cence and primary photochemistry in chloroplasts by dibro-mothymoquinone.-Biochim. biophys. Acta 376: 105-115, 1975.

    Google Scholar 

  • Klosson, R.J., Krause, G.H.: Freezing injury in cold-acclimated and unhardened spinach leaves. II. Effects of freezing on chlorophyll fluorescence and light scattering reactions.-Planta 151: 347-352, 1981.

    Google Scholar 

  • Konstantinova, T., Parvanova, D., Atanassov, A., Djilianoiv, D.: Freezing tolerant tobacco, transformed to accumulate os-moprotectants.-Plant Sci. 163: 157-164, 2002.

    Google Scholar 

  • Krause, G.H.: Photoinhibition induced by low temperatures.-In: Baker, N.R., Bowyer, J.R. (ed.): Photoinhibition of Photo-synthesis. From Molecular Mechanisms to the Field. Pp. 331-348. BIOS Scientfic Publ., Oxford 1994.

    Google Scholar 

  • Krause, G.H., Weis, E.: Chlorophyll fluorescence and photosynthesis: The basics.-Annu. Rev. Plant Physiol. Plant mol. Biol. 42: 313-349, 1991.

    Google Scholar 

  • Levitt, J.: Chilling, freezing and high temperature stress.-In: Kozlowski, T.T. (ed.): Responses of Plant to Environmental Stresses. Vol. 1.-Academic Press, New York 1980.

    Google Scholar 

  • Lichtenthaler, H.K.: Vegetation stress: an introduction to the stress concept in plants.-J. Plant.Physiol. 148: 4-14 1996.

    Google Scholar 

  • Maldonado-Rodriguez, R.: Biolyzer Software.-Bioenergetics Laboratory. University of Geneva. Switzerland. http://www.unige.ch/sciences/biologie/bioen/jipsoftware.html, 2002.

    Google Scholar 

  • Murashige, T., Skoog, F.: A revised medium for rapid growth and bioassays with tobacco tissue cultures.-Physiol. Plant. 15: 473-497, 1963.

    Google Scholar 

  • Ozaki, K., Hayashi, M.: Cryoprotective effects of cycloinulo-hexose on freezing and freeze-drying of liposomes.-Chem. Pharm. Bull. 44: 2116-2120, 1996.

    Google Scholar 

  • Papageorgiou, G.: Chlorophyll fluorescence: an intrinsic probe of photosynthesis.-In: Govindjee (ed.): Bioenergetics of Photosynthesis. Pp. 319-371. Academic Press, New York-San Francisco-London 1995.

    Google Scholar 

  • Popova, A.V.: Effect of serine on the photochemical activity of freeze-thawed thylakoid membranes.-Photosynthetica 29: 619-623, 1993.

    Google Scholar 

  • Popova, A.V., Busheva, M.R.: Cryoprotective effect of glycine betaine and glycerol is not based on a single mechanism.-Cryo Lett. 22: 293-298, 2001.

    Google Scholar 

  • Rajasheker, C.B.: Cold response and freezing tolerance in plants.-In: Wilkinson, R.E. (ed.): Plant-Environment Inter-actions. Pp. 321-341. Marcel Dekker, New York 2000.

    Google Scholar 

  • Rhodes, D., Hanson, A.D.: Quaternary ammonium and tertiary sulphonium compounds in higher plants.-Annu. Rev. Plant Physiol. Plant mol. Biol. 44: 357-384, 1993.

    Google Scholar 

  • Rudolph, A.S., Crowe, J.H., Crowe, L.M.: Effects of three sta-bilizing agents-proline, betaine, and trehalose on membrane phospholipids.-Arch. Biochem. Biophys. 245: 134-143, 1989.

    Google Scholar 

  • Sheveleva, E., Chmara, W., Bohnert, H.J., Jensen, R.G.: Increa-sed salt and drought tolerance by D-ononitol production in transgenic Nicotiana tabacum L.-Plant Physiol. 115: 1211-1219, 1997.

    Google Scholar 

  • Srivastava, A., Greppin, H., Strasser, R.J.: Acclimation of land plants to diurnal changes in temperature and light.-In: Mathis, P. (ed.): Photosynthesis: From Light to Biosphere. Vol. IV. Pp. 909-912. Kluwer Acad. Publ., Dordrecht-Boston-London 1995.

    Google Scholar 

  • Srivastava, A., Strasser, R.J.: Stress and stress management of land plants during regular day.-J. Plant Physiol. 148: 445-455, 1996.

    Google Scholar 

  • Steinmetz, M., Le Coq, D., Aymerich, S., Gonzy-Treboul, G., Gay, P.: The DNA sequence of the gene for the secreted Bacillus subtilis enzymes levansucrase and its genetic control sites.-Mol. gen. Genet. 200: 220-228, 1985.

    Google Scholar 

  • Strand, M., Öquist, G.: Effects of frost hardening, dehardening and freezing stress on in vivo chlorophyll fluorescence of seedlings of Scots pine (Pinus sylvestris L.).-Plant Cell Environ. 11: 231-238, 1988.

    Google Scholar 

  • Strasser, B.J., Strasser, R.J.: Measuring fast fluorescence transients to address environmental questions: The JIP test.-In: Mathis, P. (ed.): Photosynthesis: from Light to Biosphere. Vol. V. Pp. 977-980. Kluwer Academic Publ., Dordrecht-Boston-London 1995.

    Google Scholar 

  • Strasser, R.J., Srivastava, A., Govindjee: Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria.-Photochem. Photobiol. 61: 32-42, 1995.

    Google Scholar 

  • Strasser, R.J., Srivastava, A., Tsimilli-Michael, M.: The fluores-cence transient as a tool to characterize and screen photosyn-thetic samples.-In: Yunus, M., Pathre, U., Mohanty, P. (ed.): Probing Photosynthesis: Mechanisms, Regulation and Adap-tation. Pp. 443-483. Taylor & Francis, London-New York 2000.

    Google Scholar 

  • Yancey, P.H., Clark, M.E., Hand, S.C., Bowlus, R.D., Somero, G.N.: Living with water stress: Evolution of osmolyte sys-tems.-Science 217: 1214-1222, 1982.

    Google Scholar 

  • Yoshiba, Y., Kyosue, T., Katagiri, T., Ueda, H., Mizoguchi, T., Yamaguchi-Shinozaki, K., Wada, K., Harada, Y., Shinozaki, K.: Correlation between the induction of a gene for (1-pyrro-line-5-carboxylate-synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress.-Plant J. 7: 751-760, 1995.

    Google Scholar 

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Authors and Affiliations

  1. 8 Dragan Tzankov Blvd., 1164, Sofia, Bulgaria

    D. Parvanova, T. Konstantinova, A. Atanassov & D. Djilianov

  2. Institute of Biophysics, Bulgarian Academy of Sciences, Acad. G. Bonchev str. Bl. 21, 1113, Sofia, Bulgaria

    A. Popova, I. Zaharieva & S. Taneva

  3. Department of Biophysics and Radiobiology, Faculty of Biology, Sofia University, 8 Dragan Tzankov Blvd., 1164, Sofia, Bulgaria

    P. Lambrev & V. Goltsev

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  1. D. Parvanova
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  2. A. Popova
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  3. I. Zaharieva
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  4. P. Lambrev
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  5. T. Konstantinova
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  7. A. Atanassov
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  8. V. Goltsev
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  9. D. Djilianov
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Parvanova, D., Popova, A., Zaharieva, I. et al. Low Temperature Tolerance of Tobacco Plants Transformed to Accumulate Proline, Fructans, or Glycine Betaine. Variable Chlorophyll Fluorescence Evidence. Photosynthetica 42, 179–185 (2004). https://doi.org/10.1023/B:PHOT.0000040588.31318.0f

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  • DOI: https://doi.org/10.1023/B:PHOT.0000040588.31318.0f

  • freezing stress
  • JIP test
  • Nicotiana tabacum
  • transgenic plants