Carbocyclic Fatty Acids in Plants: Biochemical and Molecular Genetic Characterization of Cyclopropane Fatty Acid Synthesis of Sterculia Foetida

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Carbocyclic Fatty Acids in Plants: Biochemical and Molecular Genetic Characterization of Cyclopropane Fatty Acid Synthesis of Sterculia Foetida Carbocyclic fatty acids in plants: Biochemical and molecular genetic characterization of cyclopropane fatty acid synthesis of Sterculia foetida Xiaoming Bao*, Sue Katz†, Mike Pollard*, and John Ohlrogge*‡ *Department of Plant Biology, Michigan State University, East Lansing, MI 48824; and †Montgomery Botanical Center, Miami, FL 33156 Contributed by Jan A. D. Zeevaart, Michigan State University, East Lansing, MI, March 14, 2002 (received for review January 23, 2002) Fatty acids containing three-member carbocyclic rings are found in a variety of desaturases (14, 15) in animals, which might be the bacteria and plants. Bacteria synthesize cyclopropane fatty acids underlying cause of some of the disorders. Because of the health (CPA-FAs) only by the addition of a methylene group from S- concerns, vegetable oils containing CPE-FAs need to be treated adenosylmethionine to the cis-double bond of monoenoic phos- with high temperature or hydrogenation before consumption pholipid-bound fatty acids. In plants CPA-FAs are usually minor (16). As a result, processing costs are increased whereas trans- components with cyclopropene fatty acids (CPE-FAs) more abun- fatty acids are also produced by the hydrogenation. Genetically dant. Sterculia foetida seed oil contains 65–78% CPE-FAs, princi- eliminating CPE-FAs from seed oils is therefore a nutritionally pally sterculic acid. To address carbocyclic fatty acid synthesis in desirable objective. plants, a cDNA library was constructed from developing seeds The biosynthetic pathway of CPA-FAs in bacteria is well during the period of maximum oil deposition. About 0.4% of 5,300 understood (17). The first CPA-FA synthase gene was cloned expressed sequence tags were derived from one gene, which from Escherichia coli on the basis of its ability to complement a shared similarities to the bacterial CPA-FA synthase. However, the CPA-FA-deficient mutant (18). It was demonstrated that bac- predicted protein is twice as large as the bacterial homolog and terial CPA-FAs were synthesized from monounsaturated fatty represents a fusion of an FAD-containing oxidase at the N terminus acids by addition of a methylene group, derived from S- and a methyltransferase at the C terminus. Functional analysis of adenosylmethionine, across the double bond. The monoenoic the isolated full-length cDNA was conducted in tobacco suspension fatty acyl substrates are esterified to phospholipids, most prom- cells where its expression resulted in the accumulation of up to inently phosphatidylethanolamine (17). After the identification 6.2% dihydrosterculate of total fatty acids. In addition, the dihy- of the E. coli CPA-FA synthase, three genes from Mycobacterium drosterculate was specifically labeled by [methyl-14C]methionine tuberculosis were found, which function as cyclopropane syn- and by [14C]oleic acid in the transgenic tobacco cells. In in vitro thases in mycolic acid biosynthesis (19, 20). By contrast, little assay of S. foetida seed extracts, S-adenosylmethionine served as attention has been paid to the biosynthesis of CPE-FAs in plants. a methylene donor for the synthesis of dihydrosterculate from Yano et al. (21) conducted in vivo labeling experiments with oleate. Dihydrosterculate accumulated largely in phosphatidylcho- several species of Malva and proposed that the pathway involved line in both systems. Together, a CPA-FA synthase was identified initial formation of dihydrosterculic acid from oleic acid with from S. foetida, and the pathway in higher plants that produce subsequent desaturation to sterculic acid (Fig. 1). carbocyclic fatty acids was defined as by transfer of C1 units, most In this study we examine the biochemical and molecular likely from S-adenosylmethionine to oleate. genetic basis for the biosynthesis of three-member ring carbo- cyclic fatty acids in plants. Sterculia foetida is a tropical tree wide array of unusual fatty acids is found in seed oils (1, 2). belonging to the Sterculiaceae family of order Malvales. The AAmong these are fatty acids containing three-member seeds of S. foetida are rich in oil (55% dry weight) and contain carbocyclic rings, namely cis-cyclopropane fatty acids (CPA- up to 78% CPE-FAs (2, 22), one of the highest levels of FAs) and cyclopropene fatty acids (CPE-FAs). Carbocyclic fatty carbocyclic fatty acids reported in nature. Here, we report the acids are distributed across several plant orders, most notably isolation, with an expressed sequence tag (EST) approach, and Malvales but including the Fabales and Sapindales (2–4). Ster- functional characterization of the eukaryotic CPA-FA synthase culic acid is often the prevalent CPE-FA, but malvalic acid, one gene. carbon shorter in chain length than sterculic acid, can be a significant component. In Litchi chinensis seed oil, dihydroster- Materials and Methods culic acid is the major carbocyclic fatty (5, 6). The CPA- and Plant Material and Chemicals. Developing seeds of S. foetida L. CPE-FAs are not confined to seeds. Long-chain CPA-FAs have were collected from July 20 to October 15, 1998 at Montgomery been described in various polar lipid classes of leaves of early Botanical Center (Miami, FL); the accession number of the tree spring plants (7), whereas both CPA- and CPE-FAs are found in sampled is MBC 78453A. On receiving the fresh seeds, the seed root, leaf, stem, and callus tissue in plants of the Malvaceae (8, coats were removed and the cotyledons and embryos were used 9). In addition to carbon and energy storage in seeds, the for labeling experiments or were frozen and stored at Ϫ80°C for function of CPA- and CPE-FAs in plants may involve resistance RNA extraction, enzymology, and lipid analysis. Tobacco sus- to fungal attack (10). Although CPA-FAs are widely distributed pension cells (Nicotiana tabacum L. cv. Bright yellow 2) were in bacterial lipids, no CPE-FAs have been reported in bacteria to date. The cyclopropene ring of sterculic acid is highly strained, and Abbreviations: FAME, fatty acid methyl ester; CPA-FA, cyclopropane fatty acid; CPE-FA, cyclopropene fatty acid; SfCPA-FAS, Sterculia foetida cyclopropane fatty acid synthase; therefore, the acid exhibits a unique and reactive chemistry (3) 18:1, oleic acid; 18:2, linolenic acid; EST, expressed sequence tag. suggesting commercial oleochemical applications were sterculic Data deposition: The sequence reported in this paper has been deposited in the GenBank acid available in sufficient quantity. Many seed lipids containing database (accession no. AF470622). CPE-FAs are extensively consumed by humans, especially in ‡To whom reprint requests should be addressed. E-mail: [email protected]. tropical areas (11). It is well documented that dietary CPE-FAs The publication costs of this article were defrayed in part by page charge payment. This lead to the accumulation of hard fats and other physiological article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. disorders in animals (12, 13). CPE-FAs are strong inhibitors of §1734 solely to indicate this fact. 7172–7177 ͉ PNAS ͉ May 14, 2002 ͉ vol. 99 ͉ no. 10 www.pnas.org͞cgi͞doi͞10.1073͞pnas.092152999 Downloaded by guest on September 27, 2021 activity was located and quantified by using an Instant-Imager. Finally, the labeled spots were recovered for GC͞MS analysis. Assay of CPA-FA Synthase. Frozen cotyledon tissue from S. foetida developing seeds was ground to a fine powder in liquid nitrogen. A cell-free extract was prepared by thawing the powder and briefly homogenizing in four volumes of chilled buffer contain- ing 0.1 M Na Tricine⅐NaOH (pH 7.0), 1% wt͞vol defatted BSA, 1% wt͞vol polyvinylpyrrolidone-40, 15% vol͞vol glycerol, and 1 mM 2-mercaptoethanol, then filtering the slurry through mira- cloth. CPA-FA synthase assays contained 0.1 ml of cell-free homogenate, 0.02–0.05 mM oleoyl-CoA, and 0.02 mM S-[methyl- 14C]adenosylmethionine substrate in a total volume of 0.2 ml and were incubated at 30°C for 1 h. The assay was terminated by the addition of 0.5 ml of 10% aqueous KOH and 1.0 ml of ethanol, and allowed to stand overnight to give complete saponification of the lipids. On acidification, the labeled free fatty acids were extracted into hexane, then the hexane phase washed with water and evaporated to dryness. An aliquot of the organic phase was Fig. 1. Proposed pathway for the biosynthesis of sterculic acid from oleic acid (21). assayed for radioactivity. The remainder of the product was analyzed by TLC directly or after treatment with an ether solution of diazomethane. maintained in liquid medium containing Murashige and Skoog basal salts (GIBCO), 3% sucrose, 2.5 mM Mes⅐KOH (pH 5.7), Library Construction and Sequencing. Equal amounts of developing 1 mg/ml thiamine, 1 mg/ml myo-inositol, and 1 ␮M 2,4- seeds from collections of August 5, August 25, September 10, dichlorophenoxyacetic acid. Cultures were subcultured weekly and September 30, 1998, were pooled. During this period, the with 5% (vol͞vol) inoculum from a 7-day-old culture and shaken deposition of carbocyclic fatty acids showed a linear increase. at 28°C in 200-ml flasks. L-[methyl-14C]methionine (55 mCi/ Ten grams of the developing seeds were ground into fine powder mmol) and [1-14C]oleic acid (50 mCi/mmol) were purchased in liquid nitrogen and RNA extracted as described by Schultz et from American Radiolabeled Chemicals (St. Louis). al. (26). A cDNA library of S. foetida developing seeds was constructed by Stratagene. The cDNAs were directionally cloned Lipid Analysis. into the Uni-ZAP vector at EcoRI and XhoI sites. The library To determine fatty acid accumulation during S. ϫ 7 foetida seed development an internal standard, tritridecanoin, consisted of 2.6 10 plaque-forming units of primary plaques was added to seed tissue before the lipid extraction. Lipids were with average insert size of 1.7 kb.
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