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Effects of drought on water content and photosynthetic parameters in potato plants expressing the trehalose-6-phosphate synthase gene of Saccharomyces cerevisiae

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Abstract

Two transgenic potato lines, T1 and T2, expressing the trehalose-6-phosphate synthase (TPS1) gene of yeast were isolated. In our experimental approach, we applied two novelties, namely the fusion of the drought-inducible promoter StDS2 to TPS1 and a marker-free transformation method. In contrast to the expected drought-induced expression, only a very low constitutive TPS1 expression was detected in the transgenic lines, probably due to chromosomal position effects. The observed expression pattern, however, was sufficient to alter the drought response of plants. Detached leaves of T1 and T2 showed an 8 h delay in wilting compared to the non-transformed control. Potted plants of T1 and T2 kept water 6 days longer than control plants and maintained high stomatal conductance and a satisfactory rate of net photosynthesis. During drought treatment, CO2 assimilation rate measured at saturating CO2 level was maintained at maximum level for 6–9 days in transgenic plants while it decreased rapidly after 3 days in the wild type plants. Under optimal growth conditions, lower CO2 fixation was detected in the transgenic than in the control plants. Stomatal densities of T1 and T2 leaves were reduced by 30–40%. This may have contributed to the lower CO2 fixation rate and altered drought response.

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Abbreviations

A :

Net photosynthetic CO2 assimilation rate

g s :

Stomatal conductance

RWC:

Relative water content

TPS1:

Trehalose-6-phosphate synthase 1

References

  • Araus JL, Slafer GA, Reynolds MP, Royo C (2002) Plant breeding and drought in C3 cereals: what should we breed for? Ann Bot 89:925–940

    Article  PubMed  Google Scholar 

  • Avonce N, Leyman B, Mascorro-Gallardo JO, Van Dijck P, Thevelein JM, Iturriaga G (2004) The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol 136:3649–3659

    Article  PubMed  CAS  Google Scholar 

  • Bajjii M, Lutts S, Kinet JM (2001) Water deficit effects on solute contribution to osmotic adjustment as a function of leaf aging in three durum wheat (Triticum durum Desf.) cultivars performing differently in arid conditions. Plant Sci 160:669–681

    Article  Google Scholar 

  • Bánfalvi Z, Molnár A, Lovas Á, Dóczi R, Lakatos L, Hutvágner G (2000) Potato transformations. In: Hrazdina G (ed) Use of agriculturally important genes in agricultural biotechnology. NATO Science Series, Vol 319. IOS Press, Amsterdam, pp 107–111

    Google Scholar 

  • Ben G-Y, Osmond C, Sharkey T (1987) Effects of water stress on in vivo photosynthetic biochemistry (maximum photosynthesis quantum yield and 77K fluorescence). In: Biggins J (ed) Progress in photosynthesis research, Vol V. Martinus-Nijhoff Publisher, Dordrecht, pp 157–160

    Google Scholar 

  • Blum A, Sullivan CY, Nguyen HT (1997) The effect of plant size on wheat response to agents of drought stress II. Water deficit heat and ABA. Aust J Plant Physiol 24:43–48

    Article  CAS  Google Scholar 

  • Busk PK, Pages M (1998) Regulation of abscisic acid-induced transcription. Plant Mol Biol 37:425–435

    Article  PubMed  CAS  Google Scholar 

  • Centritto M, Loreto F, Chartzoulakis K (2003) The use of low [CO2] to estimate diffusional and non-diffusional limitations of photosynthetic capacity of salt stressed olive samplings. Plant Cell Environ 26:585–594

    Article  Google Scholar 

  • Chaves MM (1991) Effects of water deficits on carbon assimilation. J Exp Bot 42:1–46

    Article  CAS  Google Scholar 

  • Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to whole plant. Func Plant Biol 30:239–264

    Article  CAS  Google Scholar 

  • Cherian S, Reddy MP, Ferreira RB (2006) Transgenic plants with improved dehydration-stress tolerance: progress and future prospects. Biol Plant 50:481–495

    Article  CAS  Google Scholar 

  • Cornic G (1994) Drought stress and high light effects on leaf photosynthesis. In: Baker NR, Boeyer JR (eds) Photoinhibition of photosynthesis. Bios Scientific Publishers, Oxford pp 279–313

    Google Scholar 

  • Cornic G (2000) Drought stress inhibits photosynthesis by decreased stomatal aperture—not by affecting ATP synthesis. Trends Plant Sci 5:187–188

    Article  Google Scholar 

  • Cornic G, Fresneau C (2002) Photosynthetic carbon reduction and carbon oxidation cycles are the main electron sinks for photosystem II activity during a mild drought. Ann Bot 89:887–894

    Article  PubMed  CAS  Google Scholar 

  • Deblaere R, Bytebier B, De Greve H, Deboeck F, Schell J, Van Montagu M, Leemans J (1985) Efficient octopine Ti plasmid-derived vectors for Agrobacterium-mediated gene transfer to plants. Nucl Acids Res 13:4777–4788

    Article  PubMed  CAS  Google Scholar 

  • Delfine S, Alvino A, Villani MC, Loreto F (1999) Restrictions to carbon dioxide conductance and photosynthesis in spinach leaves recovering from salt stress. Plant Physiol 119:1101–1106

    Article  PubMed  CAS  Google Scholar 

  • Delfine S, Loreto F, Alvino A (2001) Drought-stress effects on physiology, growth and biomass production of rainfed and irrigated bell pepper plants in the Mediterranean region. J Am Soc Hort Sci 126:297–304

    CAS  Google Scholar 

  • Dóczi R, Csanaki C, Bánfalvi Z (2002) Expression and promoter activity of the desiccation-specific Solanum tuberosum gene, StDS2. Plant Cell Environ 25:1197–1203

    Article  Google Scholar 

  • Dóczi R, Kondrák M, Kovács G, Beczner F, Bánfalvi Z (2005) Conservation of the drought-inducible DS2 genes and divergences from their ASR paralogues in solanaceous species. Plant Physiol Biochem 43:269–276

    Article  PubMed  CAS  Google Scholar 

  • Dulai S, Molnár I, Lehoczki E (1998) Effects of growth temperatures of 5 and 25°C on long-term responses of photosystem II to heat stress in atrazine-resistant and susceptible biotypes of Erigeron canadensis. Aust J Plant Physiol 25:145–153

    CAS  Google Scholar 

  • Flexas J, Bota J, Escalona JM, Sampol B, Medrano H (2002) Effects of drought on photosynthesis in grapevines under field conditions: an evaluation of stomatal and mesophyll limitations. Func Plant Biol 29:461–471

    Article  Google Scholar 

  • Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189

    Article  PubMed  CAS  Google Scholar 

  • French J (1997) Primary responses of root on leaf elongation to water deficits in the atmosphere and soil solution. J Exp Bot 48:985–999

    Google Scholar 

  • Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99:15898–15903

    Article  PubMed  CAS  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of non-photochemical quenching of chlorophyll fluorescence and rate of photosystem 2 photochemistry in leaves. Biochim Biophys Acta 990:87–92

    CAS  Google Scholar 

  • Giardi MT, Cona A, Gieken B, Kucera T, Masojídek T, Mattoo AK (1996) Long-term drought stress induces structural and functional reorganization of photosystem II. Planta 199:118–125

    Article  CAS  Google Scholar 

  • Goddijn OJ, Verwoerd TC, Voogd E, Krutwagen RW, de Graaf PT, van Dun K, Poels J, Ponstein AS, Damm B, Pen J (1997) Inhibition of trehalase activity enhances trehalose accumulation in transgenic plants. Plant Physiol 113:181–190

    Article  PubMed  CAS  Google Scholar 

  • Grieu P, Rubin C, Guckert A (1995) Effect of drought on photosynthesis in Trifolium repens: maintenance of photosystem II efficiency and of measured photosynthesis. Plant Physiol Biochem 33:19–24

    CAS  Google Scholar 

  • Holmström K-O, Mantyla E, Welin B, Mandal A, Palva ET, Tunnela OE, Londesborough J (1996) Drought tolerance in tobacco. Nature 379:683–684

    Article  Google Scholar 

  • Jang I-C, Oh SJ, Seo J-S, Choi W-B, Song SI, Kim CH, Kim YS, Seo H-S, Choi YD, Nahm BH, Kim JK (2003) Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiol 131:516–524

    Article  PubMed  CAS  Google Scholar 

  • Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291

    Article  PubMed  CAS  Google Scholar 

  • Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004) A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol 45:346–350

    Article  PubMed  CAS  Google Scholar 

  • Keck R, Boyer JS (1974) Chloroplast response to low leaf water potentials. III. Differing inhibition of electron transport and photophosphorylation. Plant Physiol 53:474–479

    Article  PubMed  CAS  Google Scholar 

  • Lawlor DW (2002) Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and the role of ATP. Ann Bot 89:871–885

    Article  PubMed  CAS  Google Scholar 

  • Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ 25:275–294

    Article  PubMed  CAS  Google Scholar 

  • Loreto F, Centritto M, Chartzoulakis K (2003) Photosynthetic limitations in olive cultivars with different sensitivity. Plant Cell Environ 26:595–601

    Article  CAS  Google Scholar 

  • Maroco JP, Rodrigues ML, Lopes C, Chaves MM (2002) Limitations to leaf photosynthesis in field-grown grapevine under drought - metabolic and modelling approaches. Func Plant Biol 29:451–459

    Article  Google Scholar 

  • Medrano H, Parry MAJ, Socias X, Lawlor DW (1997) Long term water stress inactivates Rubisco in subterranean clover. Ann Appl Biol 131:491–501

    Article  CAS  Google Scholar 

  • Molnár I, Gáspár L, Sárvári É, Dulai S, Hoffmann B, Molnár-Láng M, Galiba G (2004) Physiological and morphological responses to water stress in Aegilops biuncialis and Triticum aestivum genotypes with differing tolerance to drought. Func Plant Biol 31:1149–1159

    Article  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Romero C, Bellés JM, Vayá JL, Serrano R, Culiánez-Macia FA (1997) Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants: pleiotropic phenotypes include drought tolerance. Planta 201:293–297

    Article  CAS  PubMed  Google Scholar 

  • Schluepmann H, Pellny T, van Dijken A, Smeekens S, Paul M (2003) Trehalose-6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc Natl Acad Sci USA 100:6849–6854

    Article  PubMed  CAS  Google Scholar 

  • Schluepmann H, van Dijken A, Aghdasi M, Wobbes B, Paul M, Smeekens S (2004) Trehalose mediated growth inhibition of Arabidopsis seedlings is due to trehalose-6-phosphate accumulation. Plant Physiol 135:879–890

    Article  PubMed  CAS  Google Scholar 

  • Sharkey TD (1990) Water stress effects on photosynthesis. Photosynth 24:651

    Google Scholar 

  • Shure M, Wessler S, Fedoroff N (1983) Molecular identification and isolation of the Waxy locus of maize. Cell 35:225–233

    Article  PubMed  CAS  Google Scholar 

  • Silhavy D, Hutvágner G, Barta E, Bánfalvi Z (1995) Isolation and characterization of a water-stress-inducible cDNA clone from Solanum chacoense. Plant Mol Biol 27:587–595

    Article  PubMed  CAS  Google Scholar 

  • Stiekema WJ, Heidekamp F, Dirkse WG, van Beckum J, de Haan P, ten Bosh C, Louwerse JD (1988) Molecular cloning and analysis of four potato tuber mRNAs. Plant Mol Biol 11:255–269

    Article  CAS  Google Scholar 

  • Tezara W, Mitchell VJ, Driscoll SD, Lawlor DW (1999) Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401:914–917

    Article  CAS  Google Scholar 

  • Yeo E-T, Kwon H-B, Han S-E, Lee J-T, Ryu J-C, Byun M-O (2000) Genetic engineering of drought resistant potato plants by introduction of the trehalose-6-phosphate synthase (TPS1) gene from Saccharomyces cerevisiae. Mol Cells 10:263–268

    PubMed  CAS  Google Scholar 

  • van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150

    Article  Google Scholar 

  • van Loon (1981) The effect of water stress on potato growth, development and yield. Am Potato J 58:51–69

  • Vellai T, Molnár A, Lakatos L, Bánfalvi Z, Fodor A, Sáringer G (1999) Transgenic nematodes carrying a cloned stress resistance gene from yeast. In: Glazer I, Richardson P, Boemare N, Coudert F (eds) Survival of entomopathogenic nematodes. European Commission, Brussels, pp 105–121

    Google Scholar 

  • von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387

    Article  Google Scholar 

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Acknowledgments

We thank our colleagues A. Bimbó for constructing pAB10, G. Dallmann for providing pDV411, M. Kiss for technical assistance, F. Marincs and B. Jenes for discussion, and A. Keszei (The Australian National University, Acton, Australia) for editing the manuscript. This work was supported by the Hungarian national grants NKFP 4/0023/2002 and 4/038/2004. The contribution of S. Dulai has also been supported by the OTKA grant T 043120 and the Hungarian “Békésy György” postdoctoral fellowship.

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Correspondence to Zsófia Bánfalvi.

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Ibolya Stiller, and Sándor Dulai contributed equally to this work.

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Stiller, I., Dulai, S., Kondrák, M. et al. Effects of drought on water content and photosynthetic parameters in potato plants expressing the trehalose-6-phosphate synthase gene of Saccharomyces cerevisiae . Planta 227, 299–308 (2008). https://doi.org/10.1007/s00425-007-0617-9

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