Envelope Membranes from Spinach Chloroplasts Are a Site of Metabolism of Fatty Acid Hydroperoxides

Overview

Journal Plant Physiol

Specialty Physiology

Date 1996 Feb 1

PMID 12226196

Citations 42

Authors

E Blee

J Joyard

Affiliations

Soon will be listed here.

Abstract

Enzymes in envelope membranes from spinach (Spinacia oleracea L.) chloroplasts were found to catalyze the rapid breakdown of fatty acid hydroperoxides. In contrast, no such activities were detected in the stroma or in thylakoids. In preparations of envelope membranes, 9S-hydroperoxy-10(E),12(Z)-octadecadienoic acid, 13S-hydroperoxy-9(Z),11(E)-octadecadienoic acid, or 13S-hydroperoxy-9(Z),11(E),15(Z)-octadecatrienoic acid were transformed at almost the same rates (1-2 [mu]mol min-1 mg-1 protein). The products formed were separated by reversed-phase high-pressure liquid chromatography and further characterized by gas chromatography-mass spectrometry. Fatty acid hydroperoxides were cleaved (a) into aldehydes and oxoacid fragments, corresponding to the functioning of a hydroperoxide lyase, (b) into ketols that were spontaneously formed from allene oxide synthesized by a hydroperoxide dehydratase, (c) into hydroxy compounds synthesized enzymatically by a system that has not yet been characterized, and (d) into oxoenes resulting from the hydroperoxidase activity of a lipoxygenase. Chloroplast envelope membranes therefore contain a whole set of enzymes that catalyze the synthesis of a variety of fatty acid derivatives, some of which may act as regulatory molecules. The results presented demonstrate a new role for the plastid envelope within the plant cell.

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References

Choi D, Bostock R, Avdiushko S, Hildebrand D . Lipid-derived signals that discriminate wound- and pathogen-responsive isoprenoid pathways in plants: methyl jasmonate and the fungal elicitor arachidonic acid induce different 3-hydroxy-3-methylglutaryl-coenzyme A reductase genes and antimicrobial.... Proc Natl Acad Sci U S A. 1994; 91(6):2329-33. PMC: 43364. DOI: 10.1073/pnas.91.6.2329. View

Farmer E, Ryan C . Octadecanoid Precursors of Jasmonic Acid Activate the Synthesis of Wound-Inducible Proteinase Inhibitors. Plant Cell. 1992; 4(2):129-134. PMC: 160114. DOI: 10.1105/tpc.4.2.129. View

Douce R, Holtz R, Benson A . Isolation and properties of the envelope of spinach chloroplasts. J Biol Chem. 1973; 248(20):7215-22. View

Dorne A, Joyard J, Douce R . Do thylakoids really contain phosphatidylcholine?. Proc Natl Acad Sci U S A. 1990; 87(1):71-4. PMC: 53201. DOI: 10.1073/pnas.87.1.71. View

Fruteau de Laclos B, Borgeat P . Conditions for the formation of the oxo derivatives of arachidonic acid from platelet 12-lipoxygenase and soybean 15-lipoxygenase. Biochim Biophys Acta. 1988; 958(3):424-33. DOI: 10.1016/0005-2760(88)90228-7. View

Mason H, Mullet J . Expression of two soybean vegetative storage protein genes during development and in response to water deficit, wounding, and jasmonic acid. Plant Cell. 1990; 2(6):569-79. PMC: 159912. DOI: 10.1105/tpc.2.6.569. View

Vick B, Zimmerman D . The biosynthesis of jasmonic acid: a physiological role for plant lipoxygenase. Biochem Biophys Res Commun. 1983; 111(2):470-7. DOI: 10.1016/0006-291x(83)90330-3. View

Gardner W . Sequential enzymes of linoleic acid oxidation in corn germ: lipoxygenase and linoleate hydroperoxide isomerase. J Lipid Res. 1970; 11(4):311-21. View

Douce R, Joyard J . Biochemistry and function of the plastid envelope. Annu Rev Cell Biol. 1990; 6:173-216. DOI: 10.1146/annurev.cb.06.110190.001133. View

10.

Wilen R, van Rooijen G, Pearce D, Pharis R, Holbrook L, Moloney M . Effects of jasmonic Acid on embryo-specific processes in brassica and linum oilseeds. Plant Physiol. 1991; 95(2):399-405. PMC: 1077544. DOI: 10.1104/pp.95.2.399. View

11.

Hamberg M, Hamberg G . Hydroperoxide-dependent epoxidation of unsaturated fatty acids in the broad bean (Vicia faba L.). Arch Biochem Biophys. 1990; 283(2):409-16. DOI: 10.1016/0003-9861(90)90662-i. View

12.

Baertschi S, Ingram C, Harris T, Brash A . Absolute configuration of cis-12-oxophytodienoic acid of flaxseed: implications for the mechanism of biosynthesis from the 13(S)-hydroperoxide of linolenic acid. Biochemistry. 1988; 27(1):18-24. DOI: 10.1021/bi00401a004. View

13.

Funk C, Powell W . Metabolism of linoleic acid by prostaglandin endoperoxide synthase from adult and fetal blood vessels. Biochim Biophys Acta. 1983; 754(1):57-71. DOI: 10.1016/0005-2760(83)90082-6. View

14.

Zimmerman D, Coudron C . Identification of Traumatin, a Wound Hormone, as 12-Oxo-trans-10-dodecenoic Acid. Plant Physiol. 1979; 63(3):536-41. PMC: 542865. DOI: 10.1104/pp.63.3.536. View

15.

Joyard J, BLOCK M, Douce R . Molecular aspects of plastid envelope biochemistry. Eur J Biochem. 1991; 199(3):489-509. DOI: 10.1111/j.1432-1033.1991.tb16148.x. View

16.

Song W, Brash A . Purification of an allene oxide synthase and identification of the enzyme as a cytochrome P-450. Science. 1991; 253(5021):781-4. DOI: 10.1126/science.1876834. View

17.

Blee E, Schuber F . Occurrence of fatty acid epoxide hydrolases in soybean (Glycine max). Purification and characterization of the soluble form. Biochem J. 1992; 282 ( Pt 3):711-4. PMC: 1130845. DOI: 10.1042/bj2820711. View

18.

Verhagen J, Bouman A, Vliegenthart J, BOLDINGH J . Conversion of 9-D- and 13-L-hydroperoxylinoleic acids by soybean lipoxygenase-1 under anaerobic conditions. Biochim Biophys Acta. 1976; 486(1):114-20. DOI: 10.1016/0005-2760(77)90075-3. View

19.

Bowsher C, Ferrie B, Ghosh S, Todd J, Thompson J, Rothstein S . Purification and partial characterization of a membrane-associated lipoxygenase in tomato fruit. Plant Physiol. 1992; 100(4):1802-7. PMC: 1075867. DOI: 10.1104/pp.100.4.1802. View

20.

Ohta H, Shida K, Peng Y, Furusawa I, Shishiyama J, Aibara S . A Lipoxygenase Pathway Is Activated in Rice after Infection with the Rice Blast Fungus Magnaporthe grisea. Plant Physiol. 1991; 97(1):94-8. PMC: 1080968. DOI: 10.1104/pp.97.1.94. View