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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- Baertschi S. W., Ingram C. D., Harris T. M., Brash A. R. 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 Jan 12;27(1):18–24. doi: 10.1021/bi00401a004. [DOI] [PubMed] [Google Scholar]
- Blée E., Schuber F. Occurrence of fatty acid epoxide hydrolases in soybean (Glycine max). Purification and characterization of the soluble form. Biochem J. 1992 Mar 15;282(Pt 3):711–714. doi: 10.1042/bj2820711. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Blée E., Wilcox A. L., Marnett L. J., Schuber F. Mechanism of reaction of fatty acid hydroperoxides with soybean peroxygenase. J Biol Chem. 1993 Jan 25;268(3):1708–1715. [PubMed] [Google Scholar]
- Bowsher C. G., Ferrie B. J., Ghosh S., Todd J., Thompson J. E., Rothstein S. J. Purification and partial characterization of a membrane-associated lipoxygenase in tomato fruit. Plant Physiol. 1992 Dec;100(4):1802–1807. doi: 10.1104/pp.100.4.1802. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Choi D., Bostock R. M., Avdiushko S., Hildebrand D. F. 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 isoprenoids in Solanum tuberosum L. Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2329–2333. doi: 10.1073/pnas.91.6.2329. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Croft KPC., Juttner F., Slusarenko A. J. Volatile Products of the Lipoxygenase Pathway Evolved from Phaseolus vulgaris (L.) Leaves Inoculated with Pseudomonas syringae pv phaseolicola. Plant Physiol. 1993 Jan;101(1):13–24. doi: 10.1104/pp.101.1.13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dorne A. J., Joyard J., Douce R. Do thylakoids really contain phosphatidylcholine? Proc Natl Acad Sci U S A. 1990 Jan;87(1):71–74. doi: 10.1073/pnas.87.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Douce R., Holtz R. B., Benson A. A. Isolation and properties of the envelope of spinach chloroplasts. J Biol Chem. 1973 Oct 25;248(20):7215–7222. [PubMed] [Google Scholar]
- 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. [DOI] [PubMed] [Google Scholar]
- Farmer E. E., Ryan C. A. Octadecanoid Precursors of Jasmonic Acid Activate the Synthesis of Wound-Inducible Proteinase Inhibitors. Plant Cell. 1992 Feb;4(2):129–134. doi: 10.1105/tpc.4.2.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Farmer E. E., Ryan C. A. Octadecanoid-derived signals in plants. Trends Cell Biol. 1992 Aug;2(8):236–241. doi: 10.1016/0962-8924(92)90311-a. [DOI] [PubMed] [Google Scholar]
- 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 Feb 19;958(3):424–433. doi: 10.1016/0005-2760(88)90228-7. [DOI] [PubMed] [Google Scholar]
- Funk C. D., Powell W. S. Metabolism of linoleic acid by prostaglandin endoperoxide synthase from adult and fetal blood vessels. Biochim Biophys Acta. 1983 Nov 1;754(1):57–71. doi: 10.1016/0005-2760(83)90082-6. [DOI] [PubMed] [Google Scholar]
- Gardner W. H. Sequential enzymes of linoleic acid oxidation in corn germ: lipoxygenase and linoleate hydroperoxide isomerase. J Lipid Res. 1970 Jul;11(4):311–321. [PubMed] [Google Scholar]
- Hamberg M., Hamberg G. Hydroperoxide-dependent epoxidation of unsaturated fatty acids in the broad bean (Vicia faba L.). Arch Biochem Biophys. 1990 Dec;283(2):409–416. doi: 10.1016/0003-9861(90)90662-i. [DOI] [PubMed] [Google Scholar]
- Joyard J., Block M. A., Douce R. Molecular aspects of plastid envelope biochemistry. Eur J Biochem. 1991 Aug 1;199(3):489–509. doi: 10.1111/j.1432-1033.1991.tb16148.x. [DOI] [PubMed] [Google Scholar]
- Kühn H., Wiesner R., Rathmann J., Schewe T. Formation of ketodienoic fatty acids by the pure pea lipoxygenase-1. Eicosanoids. 1991;4(1):9–14. [PubMed] [Google Scholar]
- Mason H. S., Mullet J. E. Expression of two soybean vegetative storage protein genes during development and in response to water deficit, wounding, and jasmonic acid. Plant Cell. 1990 Jun;2(6):569–579. doi: 10.1105/tpc.2.6.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ohta H., Shida K., Peng Y. L., Furusawa I., Shishiyama J., Aibara S., Morita Y. A Lipoxygenase Pathway Is Activated in Rice after Infection with the Rice Blast Fungus Magnaporthe grisea. Plant Physiol. 1991 Sep;97(1):94–98. doi: 10.1104/pp.97.1.94. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sigal E., Grunberger D., Highland E., Gross C., Dixon R. A., Craik C. S. Expression of cloned human reticulocyte 15-lipoxygenase and immunological evidence that 15-lipoxygenases of different cell types are related. J Biol Chem. 1990 Mar 25;265(9):5113–5120. [PubMed] [Google Scholar]
- Simpson T. D., Gardner H. W. Allene Oxide Synthase and Allene Oxide Cyclase, Enzymes of the Jasmonic Acid Pathway, Localized in Glycine max Tissues. Plant Physiol. 1995 May;108(1):199–202. doi: 10.1104/pp.108.1.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Song W. C., Brash A. R. Purification of an allene oxide synthase and identification of the enzyme as a cytochrome P-450. Science. 1991 Aug 16;253(5021):781–784. doi: 10.1126/science.1876834. [DOI] [PubMed] [Google Scholar]
- VIOQUE E., HOLMAN R. T. Characterization of the ketodienes formed in the oxidation of linoleate by lipoxidase. Arch Biochem Biophys. 1962 Dec;99:522–528. doi: 10.1016/0003-9861(62)90301-6. [DOI] [PubMed] [Google Scholar]
- Verhagen J., Bouman A. A., Vliegenthart J. F., Boldingh J. Conversion of 9-D- and 13-L-hydroperoxylinoleic acids by soybean lipoxygenase-1 under anaerobic conditions. Biochim Biophys Acta. 1976 Jan 18;486(1):114–120. doi: 10.1016/0005-2760(77)90075-3. [DOI] [PubMed] [Google Scholar]
- Vick B. A., Zimmerman D. C. The biosynthesis of jasmonic acid: a physiological role for plant lipoxygenase. Biochem Biophys Res Commun. 1983 Mar 16;111(2):470–477. doi: 10.1016/0006-291x(83)90330-3. [DOI] [PubMed] [Google Scholar]
- Wilen R. W., van Rooijen G. J., Pearce D. W., Pharis R. P., Holbrook L. A., Moloney M. M. Effects of jasmonic Acid on embryo-specific processes in brassica and linum oilseeds. Plant Physiol. 1991 Feb;95(2):399–405. doi: 10.1104/pp.95.2.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zimmerman D. C., Coudron C. A. Identification of Traumatin, a Wound Hormone, as 12-Oxo-trans-10-dodecenoic Acid. Plant Physiol. 1979 Mar;63(3):536–541. doi: 10.1104/pp.63.3.536. [DOI] [PMC free article] [PubMed] [Google Scholar]