Skip to main content
Log in

Enhancement of low-temperature tolerance in transgenic tomato plants overexpressing Lefad7 through regulation of trienoic fatty acids

  • Published:
Photosynthetica

Abstract

We studied how tomato (Lycopersicon esculentum Mill.) chloroplast omega-3 fatty acid desaturase gene (Lefad7) overexpression enhanced low-temperature (LT) tolerance in transgenic tomato plants. In these plants, the content of linolenic acid (18:3) markedly increased and, correspondingly, the content of linoleic acid (18:2) decreased. Similar changes were found after 6 h under LT (4°C) treatment. Under LT stress, wild type (WT) tomato plants showed a much greater increase in relative electrolyte leakage and malondialdehyde (MDA) contents compared with transgenic plants. Transgenic plants exhibited higher activities of antioxidative enzymes and a lower content of reactive oxygen species (ROS). Transgenic plants maintained a relatively higher level of the net photosynthetic rate (P N) and chlorophyll (Chl) content than WT plants under LT stress. Taken together, we suggested that overexpression of Lefad7 enhanced LT tolerance by changing the composition of membrane lipids in tomato plants, with the increased content of trienoic fatty acids and reduced content of dienoic fatty acids that led to series of physiological alterations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

APX:

ascorbate peroxidase

AtFAD7 :

Arabidopsis thaliana omega-3 fatty acid desaturase

Chl:

chlorophyll

DAs:

dienoic fatty acids

DGDG:

digalactosyldiacylglycerol

FADs:

fatty acid desaturases

IUFA:

index of unsaturated fatty acid

Lefad7 :

Lycopersicon esculentum omega-3 fatty acid desaturase gene

LT:

low-temperature

MDA:

malondialdehyde

MGDG:

monogalactosyldiacylglycerol

PFD:

photon flux density

PG:

phosphatidylglycerol

P N :

net photosynthetic rate

PUFAs:

polyunsaturated fatty acids

ROS:

reactive oxygen species

SOD:

superoxide dismutase

SQDG:

ulfoquinovosyldiacylglycerol

TAs:

trienoic fatty acids

WT:

wild type

16:1(3t):

trans-hexadecenoic acids

16:3:

hexadecatrienoic acids

18:1:

oleic acid

18:2:

linoleic acid

18:3:

linolenic acids

References

  • Andreu, V., Collados, R., Testillano, P.S. et al.: In situ molecular identification of the plastid omega3 fatty acid desaturase FAD7 from soybean: evidence of thylakoid membrane localization. — Plant Physiol. 145: 1336–1344, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Andreu, V., Lagunas, B., Collados, R., et al.: The GmFAD7 gene family from soybean: identification of novel genes and tissue-specific conformations of the FAD7 enzyme involved in desaturase activity. — J. Exp. Bot. 61: 3371–3384, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Alonso, A., Queiroz, C.S., Magalhaes, A.C.: Chilling stress leads to increased cell membrane rigidity in roots of coffee (Coffea arabica L.) seedlings. — Biochim. Biophys. Acta 1323: 75–84, 1997.

    Article  PubMed  CAS  Google Scholar 

  • Barclay, K.D., McKersie, B.D.: Peroxidation reactions in plant membranes: effects of free fatty acids. — Lipids 29: 877–883, 1994.

    Article  PubMed  CAS  Google Scholar 

  • Browse, J., Kunst, L., Anderson, S. et al.: A mutant of Arabidopsis deficient in the chloroplast 16:1/18:1 desaturase. — Plant Physiol. 90: 522–529, 1989.

    Article  PubMed  CAS  Google Scholar 

  • Browse, J., McCourt, P., Somerville, C.: A mutant of Arabidopsis deficient in c(18:3) and c(16:3) leaf lipids. — Plant Physiol. 81: 859–864, 1986.

    Article  PubMed  CAS  Google Scholar 

  • Browse, J., Somerville, C.: Glycerolipid synthesis: biochemistry and regulation. — Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 467–506, 1991.

    Article  CAS  Google Scholar 

  • Bruinsma, J.: A Comment on spectrophotometric determination of chlorophyll. — Biochim. Biophys. Acta 52: 576–578, 1961.

    Article  PubMed  CAS  Google Scholar 

  • Burdon, R.H., Gill, V., Boyd, P.A., O’Kane, D.: Chilling, Oxidative Stress and Antioxidant Enzyme Responses in Arabidopsis thaliana. — Proc. Roy. Soc. Edinburgh B-Biol. Sci. 102: 177–185, 1994.

    Google Scholar 

  • Chapin, F.S., Zavaleta, E.S., Eviner, V.T. et al.: Consequences of changing biodiversity. — Nature 405: 234–242, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Cheesbrough, T.M.: Changes in the Enzymes for Fatty Acid Synthesis and Desaturation during Acclimation of Developing Soybean Seeds to Altered Growth Temperature. — Plant Physiol. 90: 760–764, 1989.

    Article  PubMed  CAS  Google Scholar 

  • Fryer, M.J., Andrews, J.R., Oxborough, K. et al.: Relationship between CO2 Assimilation, Photosynthetic Electron Transport, and Active O2 Metabolism in Leaves of Maize in the Field during Periods of Low Temperature. — Plant Physiol. 116: 571–580, 1998.

    Article  PubMed  CAS  Google Scholar 

  • Giannopolitis, C.N., Ries, S.K.: Superoxide Dismutases 1 Occurrence in Higher Plants. — Plant Physiol. 59: 309–314, 1977.

    Article  PubMed  CAS  Google Scholar 

  • Griffiths, G., Leverentz, M., Silkowski, H., Gill, N., Sanchez-Serrano, J.J.: Lipid hydroperoxide levels in plant tissues. — J. Exp. Bot. 51: 1363–1370, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Guo, B., Liang, Y.C., Zhu, Y.G., Zhao, F.J.: Role of salicylic acid in alleviating oxidative damage in rice roots (Oryza sativa) subjected to cadmium stress. — Environ. Pollution 147: 743–749, 2007.

    Article  CAS  Google Scholar 

  • Hara, M., Terashima, S., Fukaya, T., Kuboi, T.: Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. — Planta 217: 290–298, 2003.

    PubMed  CAS  Google Scholar 

  • Huang, G., Ma, S., Bai, L. et al.: Signal transduction during cold, salt, and drought stresses in plants. — Mol. Biol. Rep. 39: 969–987, 2012.

    Article  PubMed  Google Scholar 

  • Iba, K.: Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. — Annu. Rev. Plant Biol. 53: 225–245, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Jimenez, A., Hernandez, J.A., delRio, L.A., Sevilla, F.: Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. — Plant Physiol. 114: 275–284, 1997.

    PubMed  CAS  Google Scholar 

  • Kargiotidou, A., Deli, D., Galanopoulou, D., Tsaftaris, A., Farmaki, T.: Low temperature and light regulate delta 12 fatty acid desaturases (FAD2) at a transcriptional level in cotton (Gossypium hirsutum). — J. Exp. Bot. 59: 2043–2056, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Kodama, H., Hamada, T., Horiguchi, G. et al.: Genetic Enhancement of Cold Tolerance by Expression of a Gene for Chloroplast [omega]-3 Fatty Acid Desaturase in Transgenic Tobacco. — Plant Physiol. 105: 601–605, 1994.

    PubMed  CAS  Google Scholar 

  • Kratsch, H.A., Wise, R.R.: The ultrastructure of chilling stress. — Plant Cell Environ. 23: 337–350, 2000.

    Article  CAS  Google Scholar 

  • Lemieux, B., Miquel, M., Somerville, C., Browse, J.: Mutants of Arabidopsis with alterations in seed lipid fatty acid composition. — Theor. Appl. Genet. 80: 232–240, 1990.

    Article  Google Scholar 

  • Liu, X.Y., Li, B., Yang, J.H. et al.: Overexpression of tomato chloroplast omega-3 fatty acid desaturase gene alleviates the photoinhibition of photosystems 2 and 1 under chilling stress. — Photosynthetica 46: 185–192, 2008.

    Article  CAS  Google Scholar 

  • Liu, X.Y., Yang, J.H., Li, B. et al.: Antisense-mediated depletion of tomato chloroplast omega-3 fatty acid desaturase enhances thermal tolerance. — J. Integrative Plant Biol. 48: 1096–1107, 2006.

    Article  CAS  Google Scholar 

  • McConn, M., Hugly, S., Browse, J., Somerville, C.: A Mutation at the fad8 locus of Arabidopsis identifies a second chloroplast ω-3 desaturase. — Plant Physiol. 106: 1609–1614, 1994.

    PubMed  CAS  Google Scholar 

  • Miquel, M., Browse, J.: Arabidopsis mutants deficient in polyunsaturated fatty acid synthesis. Biochemical and genetic characterization of a plant oleoyl-phosphatidylcholine desaturase. — J. Biol. Chem. 267: 1502–1509, 1992.

    PubMed  CAS  Google Scholar 

  • Mittler, R.: Oxidative stress, antioxidants and stress tolerance. — Trends Plant Sci. 7: 405–410, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Murakami, Y., Tsuyama, M., Kobayashi, Y. et al.: Trienoic fatty acids and plant tolerance of high temperature. — Science 287: 476–479, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Murata, N., Los, D.A.: Membrane Fluidity and Temperature Perception. — Plant Physiol. 115: 875–879, 1997.

    PubMed  CAS  Google Scholar 

  • Nishida, I., Murata, N.: Chilling sensitivity in plants and cyanobacteria: The crucial contribution of membrane lipids. — Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 541–568, 1996.

    Article  PubMed  CAS  Google Scholar 

  • Nishiuchi, T., Iba, K.: Roles of plastid omega-3 fatty acid desaturases in defense response of higher plants. — J. Plant Res. 111: 481–486, 1998.

    Article  CAS  Google Scholar 

  • O’Kane, D., Gill, V., Boyd, P., Burdon, B.: Chilling, oxidative stress and antioxidant responses in Arabidopsis thaliana callus. — Planta 198: 371–377, 1996.

    Article  PubMed  Google Scholar 

  • Routaboul, J.M., Fischer, S.F., Browse, J.: Trienoic fatty acids are required to maintain chloroplast function at low temperatures. — Plant Physiol. 124: 1697–1705, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Sairam, R.K., Srivastava, G.C.: Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress. — Plant Sci. 162: 897–904, 2002.

    Article  CAS  Google Scholar 

  • Santos, C.L.V., Campos, A., Azevedo, H., Caldeira, G.: In situ and in vitro senescence induced by KCl stress: nutritional imbalance, lipid peroxidation and antioxidant metabolism. — J. Exp. Bot. 52: 351–360, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Shimada, T., Wakita, Y., Otani, M., Iba, K.: Modification of fatty acid composition in rice plants by transformation with a tobacco microsomal omega-3 fatty acid desaturase gene (NtFAD3). — Plant Biotech. 17: 43–48, 2000.

    Article  CAS  Google Scholar 

  • Somerville, C.: Direct tests of the role of membrane lipid composition in low-temperature-induced photoinhibition and chilling sensitivity in plants and cyanobacteria. — Proc. Natl. Acad. Sci. USA 92: 6215–6218, 1995.

    Article  PubMed  CAS  Google Scholar 

  • Somerville, C., Browse, J.: Dissecting desaturation: plants prove advantageous. — Trends Cell Biol. 6: 148–153, 1996.

    Article  PubMed  CAS  Google Scholar 

  • Su, W.A., Wang, W.Y., Li, J.S.: Analysis of plant lipid and fatty acid. — Plant Physiol. Commun. 3: 54–60, 1980.

    Google Scholar 

  • Teixeira, M.C., Carvalho, I.S., Brodelius, M.: Omega-3 fatty acid desaturase genes isolated from purslane (Portulaca oleracea L.): expression in different tissues and response to cold and wound stress. — J. Agric. Food Chem. 58: 1870–1877, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Upchurch, R.G.: Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. — Biotechnol. Lett. 30: 967–977, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Wang, A.G., Luo, G.H.: Quantitative relation between the reaction of hydroxylamine and superoxide anion radicals in plants. — Plant Physiol. Commun. 6: 55–57, 1990.

    CAS  Google Scholar 

  • Williams, J.P., Khan, M.U., Wong, D.: Low temperatureinduced fatty acid desaturation in Brassica napus: thermal deactivation and reactivation of the process. — Biochim. Biophys. Acta. 1128: 275–279, 1992.

    Article  PubMed  CAS  Google Scholar 

  • Xu, Y.N., Siegenthaler, P.A.: Low temperature treatments induce an increase in the relative content of both linolenic and delta(3)-trans-hexadecenoic acid in thylakoid membrane phosphatidylglycerol of squash cotyledons. — Plant Cell Physiol. 38: 611–618, 1997.

    Article  CAS  Google Scholar 

  • Yu, C., Wang, H.S., Yang, S. et al.: Overexpression of endoplasmic reticulum omega-3 fatty acid desaturase gene improves chilling tolerance in tomato. — Plant Physiol. Biochem. 47: 1102–1112, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, M., Barg, R., Yin, M. et al.: Modulated fatty acid desaturation via overexpression of two distinct omega-3 desaturases differentially alters tolerance to various abiotic stresses in transgenic tobacco cells and plants. — Plant J. 44: 361–371, 2005.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Q. W. Meng.

Additional information

Acknowledgements: This research was supported by a grant from the Major State Basic Research Development Program of China (973 program) (No. 2009CB118505) and the Natural Science Foundation of Zhejiang Province (Y3110327).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, X.Y., Teng, Y.B., Li, B. et al. Enhancement of low-temperature tolerance in transgenic tomato plants overexpressing Lefad7 through regulation of trienoic fatty acids. Photosynthetica 51, 238–244 (2013). https://doi.org/10.1007/s11099-013-0014-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-013-0014-5

Additional key words

Navigation