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      Metabolic Engineering Plant Seeds with Fish Oil-Like Levels of DHA

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          Abstract

          Background

          Omega-3 long-chain (≥C 20) polyunsaturated fatty acids (ω3 LC-PUFA) have critical roles in human health and development with studies indicating that deficiencies in these fatty acids can increase the risk or severity of cardiovascular and inflammatory diseases in particular. These fatty acids are predominantly sourced from fish and algal oils, but it is widely recognised that there is an urgent need for an alternative and sustainable source of EPA and DHA. Since the earliest demonstrations of ω3 LC-PUFA engineering there has been good progress in engineering the C 20 EPA with seed fatty acid levels similar to that observed in bulk fish oil (∼18%), although undesirable ω6 PUFA levels have also remained high.

          Methodology/Principal Findings

          The transgenic seed production of the particularly important C 22 DHA has been problematic with many attempts resulting in the accumulation of EPA/DPA, but only a few percent of DHA. This study describes the production of up to 15% of the C 22 fatty acid DHA in Arabidopsis thaliana seed oil with a high ω3/ω6 ratio. This was achieved using a transgenic pathway to increase the C 18 ALA which was then converted to DHA by a microalgal Δ6-desaturase pathway.

          Conclusions/Significance

          The amount of DHA described in this study exceeds the 12% level at which DHA is generally found in bulk fish oil. This is a breakthrough in the development of sustainable alternative sources of DHA as this technology should be applicable in oilseed crops. One hectare of a Brassica napus crop containing 12% DHA in seed oil would produce as much DHA as approximately 10,000 fish.

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          Most cited references 17

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          An alternative to fish oils: Metabolic engineering of oil-seed crops to produce omega-3 long chain polyunsaturated fatty acids.

          It is now accepted that omega-3 polyunsaturated fatty acids, especially eicosapentaenoic acid (EPA; 20:5Delta5,8,11,14,17) and docosahexaenoic acid (DHA, 22:6Delta4,7,10,13,16,19) play important roles in a number of aspects of human health, with marine fish rich in these beneficial fatty acids our primary dietary source. However, over-fishing and concerns about pollution of the marine environment indicate a need to develop alternative, sustainable sources of very long chain polyunsaturated fatty acids (VLC-PUFAs) such as EPA and DHA. A number of different strategies have been considered, with one of the most promising being transgenic plants "reverse-engineered" to produce these so-called fish oils. Considerable progress has been made towards this goal and in this review we will outline the recent achievements in demonstrating the production of omega-3 VLC-PUFAs in transgenic plants. We will also consider how these enriched oils will allow the development of nutritionally-enhanced food products, suitable either for direct human ingestion or for use as an animal feedstuff. In particular, the requirements of aquaculture for omega-3 VLC-PUFAs will act as a strong driver for the development of such products. In addition, biotechnological research on the synthesis of VLC-PUFAs has provided new insights into the complexities of acyl-channelling and triacylglycerol biosynthesis in higher plants. Copyright 2009 Elsevier Ltd. All rights reserved.
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            Stepwise engineering to produce high yields of very long-chain polyunsaturated fatty acids in plants.

            Very long chain polyunsaturated fatty acids (VLCPUFAs) such as arachidonic acid (AA), eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) are valuable commodities that provide important human health benefits. We report the transgenic production of significant amounts of AA and EPA in Brassica juncea seeds via a stepwise metabolic engineering strategy. Using a series of transformations with increasing numbers of transgenes, we demonstrate the incremental production of VLCPUFAs, achieving AA levels of up to 25% and EPA levels of up to 15% of total seed fatty acids. Both fatty acids were almost exclusively found in triacylglycerols, with AA located preferentially at sn-2 and sn-3 positions and EPA distributed almost equally at all three positions. Moreover, we reconstituted the DHA biosynthetic pathway in plant seeds, demonstrating the practical feasibility of large-scale production of this important omega-3 fatty acid in oilseed crops.
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              Arabidopsis mutants deficient in polyunsaturated fatty acid synthesis. Biochemical and genetic characterization of a plant oleoyl-phosphatidylcholine desaturase.

              The overall fatty acid composition of leaf lipids in a mutant of Arabidopsis thaliana was characterized by reduced levels of polyunsaturated 18-carbon fatty acids and an increased proportion of oleate as a consequence of a single recessive nuclear mutation. Quantitative analysis of the fatty acid composition of individual lipids demonstrated that all the major phospholipids of the extrachloroplast membranes are affected by the mutation, whereas the chlorplast lipids show fatty acid compositions only slightly different from those of wild type plants. These results are consistent with the parallel operation of two pathways of lipid synthesis in plant leaf cells (the prokaryotic pathway in the chloroplast and the eukaryotic pathway in the endoplasmic reticulum) and with genetic evidence (Browse, J., Kunst, L., Anderson, S., Hugly, S., and Somerville, C.R. (1989) Plant Physiol 90, 522-529) that an independent 18:1/16:1 desaturase operates on chloroplast membrane lipids. Direct enzyme assays confirmed that the mutant plants are deficient in the activity of a microsomal oleoyl-phosphatidycholine desaturase and demonstrated that this desaturase is the major enzyme responsible for the synthesis of polyunsaturated phospholipids. Despite this deficiency in 18:1-desaturase activity, mutant plants contained relatively high levels of 18:3 in their leaf phospholipids. This finding is interpreted as additional evidence that considerable two-way exchange of lipid occurs between the chloroplast and endoplasmic reticulum and that this exchange allows the chloroplast desaturases to provide lipids containing 18:3 to the extrachloroplast compartment, thus partially alleviating the deficiency in 18:1 desaturase activity.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                7 November 2012
                : 7
                : 11
                Affiliations
                [1 ]CSIRO Food Futures National Research Flagship, Canberra, Australian Capital Territory, Australia
                [2 ]CSIRO Plant Industry, Canberra, Australian Capital Territory, Australia
                [3 ]CSIRO Marine and Atmospheric Research, Hobart, Tasmania, Australia
                Ghent University, Belgium
                Author notes

                Competing Interests: This study was partly funded by Nuseed Pty Ltd and the Australian Grains Research and Development Corporation (GRDC). Some of the data provided in this study may have been included in patent applications. CSIRO is in a commercial arrangement with GRDC and Nuseed to develop DHA land plants, although there is no product name as yet. There are no further patents, products in development or marketed products to declare. This does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials, as detailed online in the guide for authors.

                Conceived and designed the experiments: JP SS. Performed the experiments: JP PS MM QL. Analyzed the data: JP PS XZ SB PN SS. Contributed reagents/materials/analysis tools: PN. Wrote the paper: JP PN SS.

                Article
                PONE-D-12-17856
                10.1371/journal.pone.0049165
                3492320
                23145108

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Pages: 7
                Funding
                This research was funded by CSIRO Food Futures Flagship, Nuseed Pty Ltd and the Australian Grains Research and Development Corporation. The funders had no role in study design, data collection and analysis, or preparation of the manuscript. The authors were granted permission to publish the manuscript by the funders.
                Categories
                Research Article
                Agriculture
                Agricultural Biotechnology
                Biology
                Biochemistry
                Lipids
                Fatty Acids
                Biotechnology
                Genetic Engineering
                Genetically Modified Foods
                Plant Biotechnology
                Genetically Modified Organisms
                Transgenic Plants
                Plant Science
                Plant Biotechnology
                Transgenic Plants
                Plants
                Seeds

                Uncategorized

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