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Changes in fatty acids of leaf polar lipids during chilling and post-chilling rewarming of Zea mays genotypes differing in response to chilling

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Abstract

Changes in fatty acids of leaf polar lipids: monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DGDG), sulfoquinosyldiacylglycerol (SQDG) and phosphatidylglycerol (PG) in maize seedlings of chiling-sensitive (CS) CM 7 and Co 151 lines and chilling-tolerant (CT) S 215 and EP 1 lines upon chilling for either 4 or 6 days in the dark and after rewarming for 4 days at original growth conditions were studied. The content of free fatty acids (FFA) in control leaves as well as alterations in the proportion of major fatty acids, unsaturation ratio (UR), double bond index (DBI) and changes in the proportion of heigh-temperature melting of both phosphatidylglycerol (htm-PG) and sulfoquinovosylglycerol (htm-SQDG) after chilling and rewarming of seedlings were estimated.

FFA content in intact leaves was 2–3-fold higher in the chilling susceptible CM 7 line than in the other three inbreeds studied. After chilling for 6 days the level of FFA increased only in CM 7 and S 215 lines by about 30 %. Upon rewarming seedlings chilled for 6 days the level of FFA increased about two-fold in CS Co 151 line and CT EP 1 line and decreased in CS CM 7 line. Limited accumulation of FFAs during chilling and post-chilling rewarming of maize seedlings, did not correspond to the extent of polar lipid breakdown (Kaniuga et al. 1999b) probably due to the contribution of active oxidative systems to the peroxidation of fatty acids under these conditions.

During rewarming seedlings chilled for 6 days major changes were observed in decrease of 18:3 and an increase of 16:0 in all four polar lipids studied with more pronounced changes in CS than CT lines. Similarly, in CS inbreeds a decrease in UR of fatty acids in MGDG, DGDG and SQDG after post-chilling rewarming was greater than in CT lines. Proportion of htm-fraction in both PG and SQDG increased after post-chilling rewarming in all four inbreeds, however to a lesser extent in CT than CS lines. A similar pattern of changes in DBI in CS and CT maize seedlings was observed in glycolipid and combine lipid classes.

More extensive degradation of polar lipids in CS than CT maize inbreeds following galactolipase action in chloroplasts (Kaniuga et al. 1998) provides FFAs for initiation of peroxidation by LOX which is manifested by decrease of UR and DBI. This sequence of reactions during chilling and post-chilling rewarming appears to be a main route of fatty acids peroxidation responsible for secondary events involved in chilling injury. In addition, the extent of these changes differentiates CS and CT inbreeds. Contribution of esterified fatty acids in thylakoid lipids to direct peroxidation, may be of minor importance.

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Abbreviations

Chl:

chlorophyll

CS, CR and CT:

chilling sensitive, — resistant and — tolerant

DGDG:

digalactosyldiacylglycerol

FFA:

free fatty acids

htm-PG:

high temperature melting fraction of PG

LAH:

lipid acyl hydrolase (galactolipase) EC 3.1.1.26

LOX:

lipoxygenase EC 1.13.11.12

MGDG:

monogalactosyldiacylglycerol

PG:

phosphatidylglycerol

SOD:

superoxide dismutase EC 1.15.1.1

SQDG:

sulfoquinovosyldiacylglycerol

16:0:

length of carbon chain: number of double bond

16:1t:

hexadeca-trans-3-enoic acid

O2 :

superoxide aniox radical

References

  • Barclay K.D., McKersie B.D. 1994. Peroxidation reactions in plant membranes: Effects of free fatty acids. Lipids, 29: 877–822.

    Article  PubMed  CAS  Google Scholar 

  • Bligh E.G., Dyer W.J. 1959. A rapid method of lipid extraction and purification. Can. J. Biochem. Physiol., 37: 911–917.

    PubMed  CAS  Google Scholar 

  • Bowler C., van Montaque M., Inzé D. 1992. Superoxide dismutase and stress tolerance. Annu. Rev. Plant. Physiol. Plant Mol. Biol., 43: 83–116.

    Article  CAS  Google Scholar 

  • Bowsher C.G., Ferrie B.J.M., Ghosh S., Todd J., Thompson J.E., Rothetein S.J. 1992. Purification and partial characterization of a membrane-associated lipoxygenase in tomato fruit. Plant Physiol., 100: 1802–1807.

    PubMed  CAS  Google Scholar 

  • Brown J.H., Lynch D.V., Thompson J.E. 1987. Molecular species specifity of phospholipid breakdown in microsomal membranes of senescing carnation flowers. Plant Physiol., 85: 679–683.

    PubMed  CAS  Google Scholar 

  • Christie W.W. 1989. Gas Chromatography and Lipids: a Practical Guide, The Oily Press, Ayr, Scotland, 64–128.

    Google Scholar 

  • Douce R., Joygard J., Black M.A., Dorne A-J. 1990. Glycolipid analysis and synthesis. In: Harwood, J.L. and J.R. Bowyer (eds), Methods in Plant Biochemistry, Vol. 4, Academic Press, London, 71–103.

    Google Scholar 

  • Douillard R., Bergeron E. 1981. Chloroplastic localization of soluble lipoxygenase activity in young leaves. Plant Sci. Lett., 22: 263–268.

    Article  CAS  Google Scholar 

  • Feussner J., Wasternack C. 1998. Lipoxygenase catalyzed oxygenation of lipids. Fett/Lipid, 100: 146–152.

    Article  CAS  Google Scholar 

  • Fobel M., Lynch D.V., Thompson J.E. 1987. Membrane deterioration in senescing carnation flowers. Coordinated effects of phospholipid degradation and the action of membranes lipoxygenase. Plant Physiol., 85:204–211.

    PubMed  CAS  Google Scholar 

  • Garstka M., Żarnowiecka A., Kaniuga Z. 1994. Peroxidation of free fatty acids in thylakoids of chilling-sensitive and chilling-tolerant plants. Acta Physiol. Plant., 16: 337–344.

    CAS  Google Scholar 

  • Gemel J., Sączyńska V., Kaniuga Z. 1988. Galactolipase activity and free fatty acid levels in chloroplasts of domestic and wild tomatoes with different chilling tolerance. Physiol. Plant., 74: 509–514.

    Article  CAS  Google Scholar 

  • Gemel J., Cieśla E., Kaniuga Z. 1989. Different response of two Zea mays inbreeds to chilling stress measured by chloroplast galactolipase activity and free fatty acid levels. Acta Physiol. Plant., 11: 3–11.

    CAS  Google Scholar 

  • Gemel J., Kaniuga Z. 1989. Galactolipase activity and free fatty acids in chloroplasts as indicators of chilling sensitivity of closely related plant species. In: Barber J. and Malkin R. (eds), Techniques and New Development in Photosynthesis Research, Plenum Press, New York, 597–600.

    Google Scholar 

  • Gut H., Matile Ph. 1989. Breakdown of galactolipids in senescent barley leaves. Bot. Acta, 102: 31–36.

    CAS  Google Scholar 

  • Hariyadi P., Parkin K.L. 1993. Chilling-induced oxidative stress in cucumber (Cucumis sativus L. cv. Calypso) seedlings. J. Plant. Physiol., 141: 733–738.

    CAS  Google Scholar 

  • Hildebrand D.F. 1989. Lipoxygenases. Physiol. Plant., 76: 249–253.

    Article  CAS  Google Scholar 

  • Hodges D.M., Andrews C.J., Johnson D.A., Hamilton R.I. 1996. Antioxidant compound responses to chilling stress in differentially sensitive inbred maize lines. Physiol. Plant., 98: 685–692.

    Article  CAS  Google Scholar 

  • Hodges D.M., Andrews C.J., Johnson D.A., Hamilton R.I. 1997. Antioxidant enzyme responses to chilling stress in differentially sensitive inbred maize lines. J. Exp. Bot., 48: 1105–1113.

    Article  CAS  Google Scholar 

  • Hodgson R.A.J., Orr G.R., Raison J.L. 1987. Inhibition of photosynthesis by chilling in the light. Plant Sci., 49: 75–79.

    Article  CAS  Google Scholar 

  • Hodgson R.A.J., Raison J.L. 1991a. Superoxide production by plants during chilling and its implication in the susceptibility of plants to chilling-induced photoinhibition. Planta, 183: 222–228.

    Article  CAS  Google Scholar 

  • Hodgson R.A.J., Raison J.L. 1991b. Lipid peroxidation and superoxide dismutase activity in relation to photoinhibition induced by chilling in moderate light. Planta, 185: 215–219.

    Article  CAS  Google Scholar 

  • Iio T., Yoden K. 1988. Hydrolysis of fluorescent substance from an oxidized phospholipid and an amino compound by phospholipase A2. Lipids, 23: 937–941.

    Article  PubMed  CAS  Google Scholar 

  • Kaniuga Z., Sochanowicz B., Ząbek J., Krzystyniak K. 1978. Photosynthetic apparatus in chilling sensitive plants. I. Reactivation of Hill reaction activity inhibited on the cold and dark storage of detached leaves and intact plants. Planta, 140: 121–128.

    Article  CAS  Google Scholar 

  • Kaniuga Z, Michalski W.P. 1978. Photosynthetic apparatus in chilling-sensitive plants. II. Changes in free fatty acid composition and photoperoxidation in chloroplasts following cold storage and illumination of leaves in relation to Hill reaction activity. Planta, 140: 129–136.

    Article  CAS  Google Scholar 

  • Kaniuga Z., Gemel J. 1984. Galactolipase activity and free fatty acid level in chloroplasts. Novel approach to characteristic of chilling sensitivity of plants. FEBS Lett., 171: 55–58.

    Article  CAS  Google Scholar 

  • Kaniuga Z. 1997. Galactolipase and chilling sensitivity of plants. Acta Biochim. Polon. 44: 21–36.

    PubMed  CAS  Google Scholar 

  • Kaniuga Z., Sączyńska V., Miśkiewicz E. 1998. Galactolipase but not the level of high-melting point phosphatidylglycerol is related to chilling tolerance in differentially sensitive Zea mays inbred lines. Plant Cell Reports, 17: 897–901.

    Article  CAS  Google Scholar 

  • Kaniuga Z., Sączyńska V., Miśkiewicz E., Garstka M. 1999a. The fatty acid composition of phosphatidylglycerol and sulfoquinovosyldiacylglycerol of Zea mays genotypes differing in chilling susceptibility. J. Plant Physiol., (in press).

  • Kaniuga Z., Sączyńska V., Miśkiewicz E., Garstka M. 1999b. Degradation of leaf polar lipids during chilling and post-chilling rewarming of Zea mays genotypes reflects differences in their chilling response. The role of galactolipase. Acta Physiol. Plant., 21: 45–56.

    Article  CAS  Google Scholar 

  • Lynch D.V., Thompson J.E. 1984. Lipoxygenase-mediated production of superoxide anion in senescing plant tissue. FEBS Lett., 173: 251–254.

    Article  CAS  Google Scholar 

  • McKersie B.D., Chen Y., de Beus M., Bowley S.R., Bowler C., Inzé D., D’Halluin K., Botterman J. 1993. Superoxide dismutase enhances tolerance of freezing stress in transgenic alfalfa (Medicago sativa L.) Plant Physiol., 103: 1155–1163.

    Article  PubMed  CAS  Google Scholar 

  • Murata N., Yamaya J. 1984. Temperature-dependent phase behaviour of phosphatidylglycerols from chilling-sensitive and chilling-resistant plants. Plant Physiol., 74: 1016–1024.

    PubMed  CAS  Google Scholar 

  • Orr G.R., Raison J.K. 1987. Compositional and thermal properties of thylakoid polar lipids of Nerium oleander L. in relation to chilling sensitivity. Plant Physiol., 84: 88–92.

    PubMed  CAS  Google Scholar 

  • Parkin K.L., Kuo S.-J. 1989. Chilling induced lipid degradation in cucumber (Cucumis sativus L., cv. Hybrid C) fruit. Plant Physiol., 90: 1049–1056.

    PubMed  CAS  Google Scholar 

  • Parkin K.L.,. Maragoni M.A, Jackman R.L., Yada R.Y., Stanley D.W. 1989. Chilling injury. A review of possible mechanism. J. Food Biochem., 13: 127–153.

    Article  CAS  Google Scholar 

  • Percival M.P., Williams W.P., Chapman D., Quinn P.J. 1980. Loss of Hill activity in isolated chloroplasts is not directly related to free fatty acid release during ageing. Plant Sci. Lett., 19: 47–54.

    Article  CAS  Google Scholar 

  • Porter N.A. 1984. Chemistry of lipids peroxidation. Methods Enzymol., 105: 273–282.

    Article  PubMed  CAS  Google Scholar 

  • Raison J.K., Wright L.C. 1983. Thermal phase transitions in the polar lipids of plant membranes. Their induction by disaturated phospholipids and their possible relation to chilling injury. Biochim. Biophys. Acta, 731: 69–78.

    Article  CAS  Google Scholar 

  • Raison J.K., Lyons J.M. 1986. Chilling injury: a plea for uniform terminology. Plant Cell Envirom., 9: 685–686.

    Article  Google Scholar 

  • Raison J.K., Brown M.A. 1989. Sensitivity of altitudinal ecotypes of wild tomato Lycopersicon hirsutum to chilling injury. Plant Physiol., 91: 1471–1475.

    PubMed  Google Scholar 

  • Raison J.K., Orr G.R. 1990. Proposals for a better understanding of the molecular basis of chilling injury. In: Wang, C.Y. (ed.) Chilling Injury of Horticultural Crops, CRC Press, Boca Raton, Florida (USA), 145–164.

    Google Scholar 

  • Sączyńska V., Gemel J., Kaniuga Z. 1990. Effect of chilling of Zea mays L. and Capsicum annuum L. leaves on inactivation of oxygen evolution and content of free fatty acids in chloroplasts. Acta Physiol. Plant., 12: 239–245.

    Google Scholar 

  • Sączyńska V., Gemel J., Kaniuga Z. 1993. Chilling susceptibility of Cucumis sativus species. Phytochemistry, 33: 61–67.

    Article  Google Scholar 

  • Sączyńska V., Miśkiewicz E., Z. Kaniuga 1994a. Adaptation of a colorimetric procedure with diphenylcarbazide for determination of free fatty acids in chloroplasts. Acta Physiol. Plant., 16: 129–136.

    Google Scholar 

  • Sączyńska V., Miśkiewicz E., Kaniuga Z. 1994b. Effect of pH and detergents on galactolipase activity in chloroplasts of chilling-sensitive and chilling-resistant plants. Acta Physiol. Plant., 16: 317–328.

    Google Scholar 

  • Senerata T., McKersie B.D., Stinson R.H. 1985. Stimulation of dehydratation injury to membranes from soybean axes by free radicals. Plant Physiol., 77: 472–474.

    Google Scholar 

  • Sen Gupta A., Heinen J.L., Holaday A.S., Burke J.J., Allen R.D. 1993a. Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn superoxide dismutase. Proc. Natl. Acad. Sci. USA, 90: 1629–1633.

    Article  CAS  Google Scholar 

  • Sen Gupta A., Webb R.P., Holaday A.S., Allen R.D. 1993b. Overexpression of superoxide dismutase protects plants from oxidative stress. Induction of ascorbate peroxidase in superoxide dismutase-overexpressing plants. Plant Physiol., 103: 1067–1073.

    CAS  Google Scholar 

  • Thompson J.E., Paliayth G., Brown J.H., Duxbury C.L. 1987. The involvement of activated oxygen in membrane deterioration during senescence. In: Thomson, W.W., Nothnagel, E.A. and Huflaker, R.C. (eds): Plant Senescence: Its Biochemistry and Physiology, The American Society of Plant Physiologists. Rockwille, 146–155.

    Google Scholar 

  • Van Hasselt Ph. R. 1974. Photooxidation of unsaturated lipids in Cucumis leaf disc during chilling. Acta Bot. Nederl. 23: 159–169.

    Google Scholar 

  • Walker M.A., McKersie B.D. 1993. Role of the ascorbate-glutathione antioxidant system in chilling resistance of tomato. J. Plant Physiol., 141: 234–239.

    CAS  Google Scholar 

  • Whitaker B.D. 1994. Lipid changes in mature-green tomatoes during ripening, during chilling and after rewarming subsequent to chilling. J. Amer. Soc. Hort. Sci., 119: 994–999.

    CAS  Google Scholar 

  • Whitaker B.D.L 1995. Lipid changes in mature-green bell pepper fruit during chilling at 2 °C and after transfer to 20 °C subsequent to chilling. Physiol. Plant., 93, 683–688.

    Article  CAS  Google Scholar 

  • Wise R.R., Naylor A.W. 1987. Chilling enhanced photoperoxidation. The peroxidative destruction of lipids during chilling injury to photosynthesis and ultrastructure. Plant Physiol., 83: 272–277.

    Article  PubMed  CAS  Google Scholar 

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Kaniuga, Z., Sączyńska, V., Miśkiewicz, E. et al. Changes in fatty acids of leaf polar lipids during chilling and post-chilling rewarming of Zea mays genotypes differing in response to chilling. Acta Physiol Plant 21, 231–241 (1999). https://doi.org/10.1007/s11738-999-0037-5

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  • DOI: https://doi.org/10.1007/s11738-999-0037-5

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