Abstract
In transgenic (TG) tomato (Lycopersicon esculentum Mill.) overexpressed ω-3 fatty acid desaturase gene (LeFAD7) was identified, which was controlled by the cauliflower mosaic virus 35S promoter and induced increased contents of unsaturated fatty acids in thylakoid membrane. Under chilling stress at low irradiance (4 °C, 100 µmol m−2 s−1) TG plants with higher linolenic acids (18: 3) content maintained a higher O2 evolution rate, oxidizable P700 content, and maximal photochemical efficiency (Fv/Fm) than wild type (WT) plants. Low temperature treatment for 6 h resulted in extensive changes of chloroplast ultrastructure: in WT plants most chloroplasts became circular, the number of amyloids increased, appressed granum stacks were dissolved, grana disappeared, and the number of grana decreased, while only a few grana were found in leaves of TG plants. Hence the overexpression of LeFAD7 could increase the content of 18: 3 in thylakoid membrane, and this increase alleviated the photoinhibition of photosystem (PS) 1 and PS2 under chilling at low irradiance.
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Abbreviations
- DAs:
-
dienoic fatty acids
- DGDG:
-
digalactosyldiacylglycerol
- Fv/Fm :
-
maximal photochemical efficiency of photosystem 2
- JA:
-
jasmonic acid
- LeFAD7:
-
Lycopersicon esculentum ω-3 fatty acid desaturase gene
- MGDG:
-
monogalactosyldiacylglycerol
- P700:
-
photosystem 1 reaction centre
- PC:
-
phosphatidylcholine
- PFD:
-
photon flux density
- PG:
-
phosphatidylglycerol
- PI:
-
phosphatidylinositol
- SQDG:
-
sulfoquinovosyldiacylglycerol
- TAs:
-
trienoic fatty acids
- TG:
-
transgenic
- 16: 1(3t):
-
trans-hexadecenoic acids
- 16: 3:
-
hexadecatrienoic acids
- 18: 1:
-
oleic acid
- 18: 2:
-
linoleic acid
- 18: 3:
-
linolenic acids
References
Allen, D.J., Ort, D.R.: Impacts of chilling temperatures on photosynthesis in warm-climate plants.-Trends Plant Sci. 6: 36–42, 2001.
Allen, D.J., Ratner, K., Giller, Y.E., Gussakovsky, E.E., Shahak, Y., Ort, D.R.: An overnight chill induces a delayed inhibition of photosynthesis at midday in mango (Mangifera indica L.).-J. exp. Bot. 51: 1893–1902, 2000.
Berberich, T., Harada, M., Sugawara, K., Kodama, H., Iba, K., Kusano, T.: Two maize genes encoding omega-3 fatty acid desaturase and their differential expression to temperature.-Plant mol. Biol. 36: 297–306, 1998.
Browse, J., McCourt, P., Somerville, C.: A mutant of Arabidopsis deficient in C18:3 and C16:3 leaf lipids.-Plant Physiol. 81: 859–864, 1986.
Browse, J., Somerville, C.: Glycerolipid synthesis: biochemistry and regulation.-Annu. Rev. Plant Physiol. Plant mol. Biol. 42: 467–506, 1991.
Dai, Y.H., Liu, X.Y., Meng, Q.W., Zhao, S.J.: The change of photoinhibition and fatty acid component of thylakoid membrane of cucumber during chilling stress under low irradiance and recovery.-Plant Physiol. Commun. 40: 14–18, 2004.
Flexas, J., Badger, M., Chow, W.S., Medrano, H., Osmond, C.B.: Analysis of the relative increase in photosynthetic O2 uptake when photosynthesis in grapevine leaves is inhibited following low night temperatures and/or water stress.-Plant Physiol. 121: 675–684, 1999.
Graham, D., Patterson, B.D.: Responses of plants to low, nonfreezing temperatures: protein, metabolism, and acclimation.-Annu. Rev. Plant Physiol. Plant mol. Biol. 33: 347–372, 1982.
Gray, G.R., Savitch, L.V., Ivanov, A.G., Huner, N.: Photosystem II excitation pressure and development of resistance to photoinhibition. II. Adjustment of photosynthetic capacity in winter wheat and winter rye.-Plant Physiol. 110: 61–71, 1996.
Greer, D.H., Berry, J.A., Björkman, O.: Photoinhibition of photosynthesis in intact bean leaves: role of light and temperature, and requirement for chloroplast-protein synthesis during recovery.-Planta 168: 253–260, 1986.
Gu, H.Y., Qu, L.J., Ming, X.T.: Plant Gene and Molecular Manipulation.-Beijing University Press, Beijing 1995.
Güler, S., Seeliger, A., Härtel, H., Renger, G.., Benning, C.: A null mutant of Synechococcus sp. PCC7942 deficient in the sulfolipid sulfoquinovosyl diacylglycerol.-J. biol. Chem. 271: 7501–7507, 1996.
Havaux, M., Davaud, A.: Photoinhibition of photosynthesis in chilled potato leaves is not correlated with loss of Photosystem-II activity. Preferential inactivation of Photosystem I.-Photosynth. Res. 40: 75–92, 1994.
Horsch, R.B., Fry, J.E., Hoffmann, N.L., Eichholtz, D., Rogers, S.G., Fraley, R.T.: A simple and general method for transferring gene into plants.-Science 227: 1229–1231, 1985.
Huner, N.P., Williams, J.P., Maissan, E.E., Myscich, E.G., Krol, M., Laroche, A., Singh, J.: Low temperature-induced decrease in trans-delta-hexadecenoic acid content is correlated with freezing tolerance in cereals.-Plant Physiol. 89: 144–150, 1989.
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.
Kirsch, C., Takamiya-Wik, M., Reinold, S., Hahlbrock, K., Somssich, I.E.: Rapid, transient, and highly localized induction of plastidial ω-3 fatty acid desaturase mRNA at fungal infection sites in Petroselinum crispum.-Proc. nat. Acad. Sci. USA 94: 2079–2084, 1997.
Knight, H., Trewavas, A.J., Knight, M.R.: Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation.-Plant Cell 8: 489–503, 1996.
Kratsch, H.A., Wise, R.R.: The ultrastructure of chilling stress.-Plant Cell Environ. 23: 337–350, 2000.
Lemieux, B., Miquel, M., Somerville, C., Browse, J.: Mutants of Arabidopsis with alterations in seed lipid fatty acid composition.-Theor. appl. Genet. 80: 234–240, 1990.
Levitt, J.: Responses of Plants to Environmental Stress. Vol. 1.-Pp. 166–248. Academic Press, New York 1980.
Li, C.Y., Liu, G.H., Xu, C.C., Lee, G.I., Bauer, P., Ling, H.Q., Ganal, M.W., Howe, G.A.: The tomato suppressor of prosystemin-mediated responses 2 gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signal for defense gene expression.-Plant Cell 15: 1646–1661, 2003a.
Li, X.-G., Meng, Q.-W., Jiang, G.-Q., Zou, Q.: The susceptibility of cucumber and sweet pepper to chilling under low irradiance is related to energy dissipation and water-water cycle.-Photosynthetica 41: 259–265, 2003b.
Li, X.-G., Wang, X.-M., Meng, Q.-W., Zou, Q.: Factors limiting photosynthetic recovery in sweet pepper leaves after short-term chilling stress under low irradiance.-Photosynthetica 42: 257–262, 2004.
Liu, X.Y., Yang, J.H., Li, B., Yang, X.M., Meng, Q.W.: Antisense-mediated depletion of tomato chloroplast omega-3 fatty acid desaturase enhances thermal tolerance.-J. integr. Plant Biol. 48: 1096–1107, 2006.
Lyons, J.M., Raison, J.K.: A temperature-induced transition in mitochondrial oxidation: contrasts between cold and warm-blooded animals.-Comp. Biochem. Physiol. 37: 405–411, 1970.
Martin, B., Ort, D.R., Boyer, J.S.: Impairment of photosynthesis by chilling-temperatures in tomato.-Plant Physiol. 68: 329–334, 1981.
Martín, M., León, J., Dammann, C., Albar, J.P., Griffiths, G., Sánchez-Serrano, J.J.: Antisense-mediated depletion of potato leaf omega-3 fatty acid desaturase lowers linolenic acid content and reduces gene activation in response to wounding.-Eur. J. Biochem. 262: 283–290, 1999.
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.
Miquel, M., James, D., Dooner, H., Browse, J.: Arabidopsis requires polyunsaturated lipids for low-temperature survival.-Proc. nat. Acad. Sci. USA 90: 6208–6212, 1993.
Moon, B.Y., Higashi, S., Gombos, Z., Murata, N.: Unsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in TG tobacco plants.-Proc. nat. Acad. Sci. USA 92: 6219–6233, 1995.
Murakami, Y., Tsuyama, M., Kobayashi, Y., Kodama, H., Iba, K.: Trienoic fatty acids and plant tolerance of high temperature.-Science 287: 476–479, 2000.
Murata, N., Los, D.A.: Membrane fluidity and temperature perception.-Plant Physiol. 115: 875–879, 1997.
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.
Ohlrogge, J., Browse, J.: Lipid biosynthesis.-Plant Cell 7: 957–970, 1995.
Palta, J.P., Whitake, B.D., Weiss, L.S.: Plasma membrane lipids associated with genetic variability in freezing tolerance and cold acclimation of Solanum species.-Plant Physiol. 103: 793–803, 1993.
Pearcy, R.W.: Effect of growth temperature on the fatty acid composition of the leaf lipids in Atriplex lentiformis (Torr.) Wats.-Plant Physiol. 61: 484–486, 1978.
Raison, J.K., Roberts, J.K.M., Berry, J.A.: Correlations between the thermal stability of chloroplast (thylakoid) membranes and the composition and fluidity of their polar lipids upon acclimation of the higher plant, Nerium oleander, to growth temperature.-Biochim. biophys. Acta 688: 218–228, 1982.
Rawyler, A., Siegenthaler, P.A.: Transmembrane distribution of phospholipids and their involvement in electron transport as revealed by phospholipase A2 treatment of spinach thylakoids.-Biochim. biophys. Acta 635: 348–368, 1981.
Ristic, Z., Ashworth, E.N.: Changes in leaf ultrastructure and carbohydrates in Arabidopsis thalinana L. (Heynh) cv. Columbia during rapid cold acclimation.-Protoplasma 172: 111–123, 1993.
Routaboul, J.M., Fischer, S.F., Browse, J.: Trienoic fatry acids are required to maintain chloroplast function at low temperature.-Plant Physiol. 124: 1697–1705, 2000.
Sakurai, I., Hagio, M., Gombos, Z., Tyystjärvi, T., Paakkarinen, V., Aro, E.M., Wada, H.: Requirement of phosphatidylglycerol for maintenance of photosynthetic machinery.-Plant Physiol. 133: 1376–1384, 2003
Sato, N., Aoki, M., Maru, Y., Sonoike, K., Minoda, A., Tsuzuki, M.: Involvement of sulfoquinovosyl diacylglycerol in the structural integrity and heat-tolerance of photosystem 2.-Planta 217: 245–251, 2003.
Schansker, G., Srivastava, A., Govindjee, Strasser, R.J.: Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves.-Funct. Plant Biol. 30: 785–796, 2003.
Schreiber, U., Bilger, W., Neubauer, C.: Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis.-In: Schulze, E.-D., Caldwell, M.M. (ed.): Ecophysiology of Photosynthesis. Pp. 49–70. Springer-Verlag, Berlin 1994.
Siegenthaler, P.A., Eichenberger, W.: Structure, function and metabolism of plant lipids.-In: Plant Lipids-Metabolism-Congresses. Pp. 485–488, Elsevier Science Publ., Amsterdam 1984.
Somerville, C.: Direct tests of the role of membrane lipid composition in low-temperature-induced photoinhibition and chilling sensitivity in plants and cyanobacteria.-Proc. nat. Acad. Sci. USA 92: 6215–6218, 1995.
Somerville, C., Browse, J.: Plant lipids: metabolism, mutants and membranes.-Science 252: 80–87, 1991.
Somerville, C., Browse, J.: Dissecting desaturases: plants prove advantageous.-Trends Cell Biol. 6: 148–153, 1996.
Sonoike, K.: Photoinhibition of photosystem I: its physiological significance in the chilling sensitivity of plants.-Plant Cell Physiol. 37: 239–247, 1996.
Strand, A., Hurry, V., Gustafasson, P., Gardestrom, P.: Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates.-Plant J. 12: 605–614, 1997.
Su, W.A., Wang, W.Y., Li, J.S.: Analysis of plant lipid and fatty acid-TLC-GLC technology.-Plant Physiol. Commun. 3: 54–60, 1980.
Thomashow, M.F.: Arabidopsis thaliana as a model for studying mechanisms of plant cold tolerance.-In: Meyerowitz, E.M., Somerville, C.R. (ed.): Arabidopsis. Pp. 807–834. Cold Spring Harbor Laboratory Press, New York 1994.
Van Kooten, O., Snel, J.F.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology.-Photosynth. Res. 25: 147–150, 1990.
Vick, B.A., Zimmerman, D.C.: Biosynthesis of jasmonic acid by several plant species.-Plant Physiol. 75: 458–461, 1984.
Vijayan, P., Shockey, J., Adré Lévesque, C.A., Cook, R.J., Browse, J.: A role for jasmonate in pathogen defense of Arabidopsis.-Proc. nat. Acad. Sci. USA 95: 7209–7214, 1998.
Walker, D.: The Use of O2 Electrode and Fluorescence Probes in Simple Measurements of Photosynthesis.-Robert Hill Institute, University of Sheffield, Shefield 1990.
Xu, C.C., Jeon, Y.A., Lee, C.H.: Relative contributions of photochemical and non-photochemical routes to excitation energy dissipation in rice and barley illuminated at a chilling temperature.-Plant Physiol. 107: 447–453, 1999.
Xu, Y.N., Siegenthaler, P.A.: Low temperature treatments induce an increase in the relative content of both linolenic and trans-hexadecenoic acid in thylakoid membrane phosphatidylglycerol of squash cotyledons.-Plant Cell Physiol. 38: 611–618, 1997.
Yu, B., Benning, C.: Anionic lipids are required for chloroplast structure and function in Arabidopsis.-Plant J. 36: 762–770, 2003.
Yu, B., Xu, C., Benning, C.: Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth.-Proc. nat. Acad. Sci. USA 99: 5732–5737, 2002.
Zou, J., Abrams, G.D., Barton, D.L., Taylor, D.C., Pomeroy, M.K., Abrams, S.R.: Induction of lipid and oleoisin biosynthesis by (+)-abscisic acid and its metabolites in microsporederived embroyos of Brassica napus L. cv. Reston.-Plant Physiol. 108: 563–571, 1995.
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Liu, XY., Li, B., Yang, JH. 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). https://doi.org/10.1007/s11099-008-0030-z
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DOI: https://doi.org/10.1007/s11099-008-0030-z