The modification of plant oil composition via metabolic engineering-better nutrition by design

Plant Biotechnology Journal

Volumn 11, Issue 2, 2013, Pages 157-168

  Haslam, Richard P ^a   Ruiz Lopez, Noemi ^a   Eastmond, Peter ^a   Moloney, Maurice ^a   Sayanova, Olga ^a   Napier, Johnathan A ^a  

^a ROTHAMSTED RESEARCH   (United Kingdom)

Author keywords

Lipids; Omega 3 fatty acids; Polyunsaturated fatty acids; Seed oils; Transgenic plants

Indexed keywords

OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; VEGETABLE OIL;

BIOSYNTHESIS; CHEMISTRY; CROP; METABOLIC ENGINEERING; PLANT SEED; REVIEW; SYNTHETIC BIOLOGY; TRANSGENIC PLANT;

BIOSYNTHETIC PATHWAYS; CROPS, AGRICULTURAL; FATTY ACIDS, OMEGA-3; FATTY ACIDS, OMEGA-6; METABOLIC ENGINEERING; PLANT OILS; PLANTS, GENETICALLY MODIFIED; SEEDS; SYNTHETIC BIOLOGY;

ANIMALIA;

EID: 84873153986     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12012     Document Type: Review

References (139)

1. Abbadi, A., Domergue, F., Bauer, J., Napier, J.A., Welti, R., Zähringer, U., Cirpus, P. and Heinz, E. (2004) Biosynthesis of very-long-chain polyunsaturated fatty acids in transgenic oilseeds: constraints on their accumulation. Plant Cell, 16, 2734-2748.
2. Bates, P.D. and Browse, J. (2011) The pathway of triacylglycerol synthesis through phosphatidylcholine in Arabidopsis produces a bottleneck for the accumulation of unusual fatty acids in transgenic seeds. Plant J. 68, 387-399.
3. Bates, P.D., Durrett, T.P., Ohlrogge, J.B. and Pollard, M. (2009) Analysis of acyl fluxes through multiple pathways of triacylglycerol synthesis in developing soybean embryos. Plant Physiol. 150, 55-72.
4. Beaudoin, F., Michaelson, L.V., Hey, S.J., Lewis, M.J., Shewry, P.R., Sayanova, O. and Napier, J.A. (2000) Heterologous reconstitution in yeast of the polyunsaturated fatty acid biosynthetic pathway. Proc. Natl Acad. Sci. U.S.A. 97, 6421-6426.
5. Beydoun, M.A., Kaufman, J.S., Satia, J.A. and Rosamond, W. (2007) Plasma n-3 fatty acids and the risk of cognitive decline in older adults: the Atherosclerosis risk in communities study. Am. J. Clin. Nutr. 85, 1103-1111.
6. Bostock, J., McAndrew, B., Richards, R., Jauncey, K., Telfer, T., Lorenzen, K., Little, D., Ross, L., Handisyde, N., Gatward, I. and Corner, R. (2010) Aquaculture: global status and trends. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 2897-2912.
7. Brown, A.P., Kroon, J.T.M., Swarbreck, D., Febrer, M., Larson, T.R., Graham, I.A., Caccamo, M. and Slabas, A.R. (2012) Tissue-specific whole transcriptome sequencing in Castor, directed at understanding triacyglycerol lipid biosynthetic pathways. PLoS ONE, 7, 1-13.
8. Burdge, G.C. (2006) Metabolism of alpha-linolenic acid in humans. Prostag. Leukotr. Ess. Fatty Acids, 75, 161-168.
9. Cahoon, E.B. and Kinney, A.J. (2005) The production of vegetable oils with novel properties: using genomic tools to probe and manipulate fatty acid metabolism. Eur. J. Lipid Sci. Technol. 107, 239-243.
10. Calder, P.C. (2004) Fatty acids and cardiovascular disease: evidence explained and mechanisms explored. Clin. Sci. 107, 1-11.
11. Carlsson, A.S., Yilmaz, J.L., Green, A.G., Stymne, S. and Hofvander, P. (2011) Replacing fossil oil with fresh oil - with what and for what? Eur. J. Lipid Sci. Technol. 113, 812-831.
12. Chan, A.P., Crabtree, J., Zhao, Q., Lorenzi, H., Orvis, J., Puiu, D., Melake-Berhan, A., Jones, K.M., Redman, J., Chen, G., Cahoon, E.B., Gedil, M., Stanke, M., Haas, B.J., Wortman, J.R., Fraser-Liggett, C.M., Ravel, J. and Rabinowicz, P.D. (2010) Draft genome sequence of the oilseed species Ricinus communis. Nat. Biotechnol. 28, 951-956.
13. Chen, R., Matsui, K., Ogawa, M., Oe, M., Ochiai, M. and Kawashima, H. (2006) Expression of Δ6, Δ5-desaturase and GLELO elongase genes from Mortierella alpina for production of arachidonic acid in Soybean [Glycine max (L.) Merrill] seeds. Plant Sci. 170, 399-406.
14. Cheng, D., Iqbal, J., Devenny, J., Chu, C.H., Chen, L., Dong, J., Seethala, R., Keim, W.J., Azzara, A.V., Lawrence, R.M., Pelleymounter, M.A. and Hussain, M.M. (2008) Acylation of acylglycerols by acyl coenzyme A:diacylglycerol acyltransferase 1 (DGAT1). Functional importance of DGAT1 in the intestinal fat absorption. J. Biol. Chem. 283, 29802-29811.
15. Cheng, B.F., Wu, G.H., Vrinten, P., Falk, K., Bauer, J. and Qiu, X. (2010) Towards the production of high levels of eicosapentaenoic acid in transgenic plants: the effects of different host species, genes and promoters. Transgenic Res. 19, 221-229.
16. Chiu, C.C., Su, K.P., Cheng, T.C., Liu, H.C., Chang, C.J., Dewey, M.E., Stewart, R. and Huang, S.Y. (2008) The effects of omega-3 fatty acids monotherapy in Alzheimer's disease and mild cognitive impairment: a preliminary randomized double-blind placebo-controlled study. Prog. Neuropsychopharmacol. 32, 1538-1544.
17. Chung, W.L., Chen, J.J. and Su, H.M. (2008) Fish oil supplementation of control and (n-3) fatty acid-deficient male rats enhances reference and working memory performance and increases brain regional docosahexaenoic acid levels. J. Nutr. 138, 1165-1171.
18. Clauß, K., Roepenack-Lahaye, E., Böttcher, C., Roth, M.R., Welti, R., Erban, A., Kopka, J., Scheel, D., Milkowski, C. and Strack, D. (2011) Over-expression of sinapine esterase BnSCE3 in oilseed rape seeds triggers global changes in seed metabolism. Plant Physiol. 155, 1127-1145.
19. Clemente, T.E. and Cahoon, E. (2009) Soybean oil: genetic approaches for modification of functionality and total content. Plant Physiol. 151, 1030-1040.
20. Cole, G.M. and Frautschy, S.A. (2006) DHA protects from amyloid and dendritic pathology in an Alzheimer's disease mouse model. Nutr. Health, 18, 249-259.
21. Collins, N., Tighe, A.P., Brunton, S.A. and Kris-Etherton, P.M. (2008) Differences between dietary supplement and prescription drug omega-3 fatty acid formulations: a legislative and regulatory perspective. J. Am. Coll. Nutr. 27, 659-666.
22. Costa, G.G., Cardoso, K.C., Del Bem, L.E., Lima, A.C., Cunha, M.A., de Campos-Leite, L., Vicentini, R., Papes, F., Moreira, R.C., Yunes, J.A., Campos, F.A. and Da Silva, M.J. (2010) Transcriptome analysis of the oil-rich seed of the bioenergy crop Jatropha curcas L. BMC Genomics, 11, 462.
23. Damude, H.G. and Kinney, A.J. (2008) Enhancing plant seed oils for human nutrition. Plant Physiol. 147, 962-968.
24. Das, T., Thurmond, J.M., Bobik, E., Leonard, A.E., Parker-Barnes, J.M., Huang, Y.S. and Mukerji, P. (2000) Polyunsaturated fatty acid-specific elongation enzymes. Biochem. Soc. Trans. 28, 658-660.
25. Devaiah, S.P., Roth, M.R., Baughman, E., Li, M., Tamura, P., Jeannotte, R., Welti, R. and Wang, X. (2006) Quantitative profiling of polar glycerolipid species from organs of wild-type Arabidopsis and a PHOSPHOLIPASE Da1 knockout mutant. Phytochemistry, 67, 1907-1924.
26. Domergue, F., Lerchl, J., Zähringer, U. and Heinz, E. (2002) Cloning and functional characterization of Phaeodactylum tricornutum front-end desaturases involved in eicosapentaenoic acid biosynthesis. Eur. J. Biochem. 269, 4105-4113.
27. Domergue, F., Abbadi, A., Ott, C., Zank, T.K., Zähringer, U. and Heinz, E. (2003) Acyl carriers used as substrates by the desaturases and elongases involved in very long-chain polyunsaturated fatty acids biosynthesis reconstituted in yeast. J. Biol. Chem. 278, 35115-35126.
28. Domergue, F., Abbadi, A., Zähringer, U., Moreau, H. and Heinz, E. (2005) In vivo characterization of the first acyl-CoA Δ6-desaturase from a member of the plant kingdom, the microalga Ostreococcus tauri. Biochem. J. 389, 483-490.
29. Dyer, J.M., Stymne, S., Green, A.G. and Carlsson, A.S. (2008) High-value oils from plants. Plant J. 54, 640-655.
30. Eckert, H., La Vallee, B., Schweiger, B.J., Kinney, A.J., Cahoon, E.B. and Clemente, T. (2006) Co-expression of the Borage Δ6-desaturase and the Arabidopsis Δ15-desaturase results in high accumulation of stearidonic acid in the seeds of transgenic Soybean. Planta, 224, 1050-1057.
31. Fehling, E., Lessire, R., Cassagne, C. and Mukherjee, K.D. (1992) Solubilization and partial purification of constituents of acyl-CoA elongase from Lunaria annua. Biochim. Biophys. Acta, 1126, 88-94.
32. Flider, J.F. (2005) GLA: uses and new sources. Inform, 16, 279-283.
33. Food and Agriculture Organisation of the United Nations (2010). The State of World Fisheries and Aquaculture. Rome: Food and Agriculture Organisation.
34. 18-Δ9 polyunsaturated fatty acid specific elongase component alters Arabidopsis glycerolipid profiles. Plant Physiol. 135, 859-866.
35. Garcia, S.M. and Rosenberg, A.A. (2010) Food security and marine capture fisheries: characteristics, trends, drivers and future perspectives. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 2869-2880.
36. van Gelder, B.M., Tijhuis, M., Kalmijn, S. and Kromhout, D. (2007) Fish consumption, n-3 fatty acids, and subsequent 5-y cognitive decline in elderly men: the Zutphen Elderly Study. Am. J. Clin. Nutr. 85, 1142-1147.
37. Givens, D.I. and Gibbs, R.A. (2008) Current intakes of EPA and DHA in European populations and the potential of animal-derived foods to increase them. Proc. Nutr. Soc. 67, 273-280.
38. Graham, I.A., Cirpus, P., Rein, D. and Napier, J.A. (2004) The use of very long chain polyunsaturated fatty acids to ameliorate metabolic syndrome: transgenic plants as an alternative sustainable source to fish oils. Nutr. Bull. 29, 228-233.
39. Hammond, B.G., Lemen, J.K., Ahmed, G., Miller, K.D., Kirkpatrick, J. and Fleeman, T. (2008) Safety assessment of SDA soybean oil: results of a 28-day gavage study and a 90-day/one generation reproduction feeding study in rats. Regul. Toxicol. Pharmacol. 52, 311-323.
40. Haraldsson, G.G. and Hjaltason, B. (2001) In Structured and Modified Lipids (Gunstone, F.D. ed.), pp. 313-350. New York, NY: Marcel Dekker.
41. Harris, W.S., Lemke, S.L., Hansen, S.N., Goldstein, D.A., DiRienzo, M.A., Su, H., Nemeth, M.A., Taylor, M.L., Ahmed, G. and George, C. (2008) Stearidonic acid-enriched soybean oil increased the omega-3 index, an emerging cardiovascular risk marker. Lipids, 43, 805-811.
42. Harwood, J.L. (1988) Fatty acid metabolism. Annu. Rev. Plant Physiol. 39, 101-188.
43. Haynes, C.A., Allegood, J.C., Sims, K., Wang, E.W., Sullards, C.M. and Merrill, A.H. (2008) Quantitation of fatty acyl-coenzyme A in mammalian cells by liquid chromatography-electrospray ionization tandem mass spectrometry. J. Lipid Res. 49, 1113-1125.
44. Hoffmann, M., Wagner, M., Abbadi, A., Fulda, M. and Feussner, I. (2008) Metabolic engineering of ω-3 very long chain polyunsaturated fatty acid production by an exclusively acyl-CoA-dependent pathway. J. Biol. Chem. 283, 22352-22362.
45. Hong, H., Datla, N., Reed, D.W., Covello, P.S., MacKenzie, S.L. and Qiu, X. (2002) High-level production of γ-linolenic acid in Brassica juncea using a Δ6 desaturase from Pythium irregulare. Plant Physiol. 129, 354-362.
46. Horn, P.J. and Chapman, K.D. (2012) Lipidomics in tissues, cells and subcellular compartments. Plant J. 70, 69-80.
47. Jakobsson, A., Westerberg, R. and Jacobsson, A. (2006) Fatty acid elongases in mammals: their regulation and roles in metabolism. Prog. Lipid Res. 45, 237-249.
48. James, M.A. and Slaski, R.J. (2009) A strategic review of the potential for aquaculture to contribute to the future security of food and non-food products and services in the UK and specifically England. Report commissioned by the Department for the Environment and Rural Affairs, 121pp.
49. James, D.W., Lim Jr, E., Keller, J., Plooy, I., Ralston, E. and Dooner, H.K. (1995) Directed tagging of the Arabidopsis FATTY ACID ELONGATION1 (FAE1) gene with the maize transposon activator. Plant Cell, 7, 309-319.
50. Kalmijn, S. (2000) Fatty acid intake and the risk of dementia and cognitive decline: a review of clinical and epidemiological studies. J. Nutr. Health Aging, 4, 202-207.
51. Khozin-Goldberg, I., Iskandarov, U. and Cohen, Z. (2011) LC-PUFA from photosynthetic microalgae: occurrence, biosynthesis, and prospects in biotechnology. Appl. Microbiol. Biotechnol. 94, 90-915.
52. Kinney, A.J., Cahoon, E.B., Damude, H.G., Hitz, W.D., Kolar, C.W. and Liu, Z.B. (2004) Production of very long chain polyunsaturated fatty acids in oilseed plants. WO 2004/071467 A2.
53. Kinney, A.J., Cahoon, E.B., Damude, H.G. and Liu, Z.B. (2011) Production of very long chain polyunsaturated fatty acids in oilseed plants. United States Patent Application 20110269983.
54. Krank, J., Murphy, R.C., Barkley, R.M., Duchoslav, E. and McAnoy, A. (2007) Qualitative analysis and quantitative assessment of changes in neutral glycerol lipid molecular species within cells. Methods Enyzmol. 432, 1-20.
55. Kris-Etherton, P.M., Grieger, J.A. and Etherton, T.D. (2009) Dietary reference intakes for DHA and EPA. Prostag. Leukotr. Ess. Fatty Acids, 81, 99-104.
56. Larson, T.R. and Graham, I.A. (2001) A novel technique for the sensitive quantification of acyl CoA esters from plant tissues. Plant J. 25, 115-125.
57. Lee, J., Welti, R., Schapaugh, W.T. and Trick, H.N. (2011) Phospholipid and triacylglycerol profiles modified by PLD suppression in soybean seed. Plant Biotechnol. J. 9, 359-372.
58. Lees, A.M. and Korn, E.D. (1966) Metabolism of unsaturated fatty acids in protozoa. Biochemistry, 5, 1475-1481.
59. Lemke, S.L., Vicini, J.L., Su, H. and Goldstein, D.A. (2010) Dietary intake of stearidonic acid-enriched soybean oil increases the omega-3 index: randomized, double-blind clinical study of efficacy and safety. Am. J. Clin. Nutr. 92, 766-775.
60. Li-Beisson, Y., Shorrosh, B., Beisson, F., Andersson, M.X., Arondel, V., Bates, P.D., Baud, S., Bird, D., DeBono, A., Durrett, T.P., Franke, R.B., Graham, I.A., Katayama, K., Kelly, A.A., Larson, T.R., Markham, J.E., Miquel, M., Molina, I., Nishida, I., Rowland, O., Samuels, L., Schmid, K.M., Wada, H., Welti, R., Xu, C., Zallot, R. and Ohlrogge, J. (2010) Acyl-lipid metabolism. The Arabidopsis Book, 8, e0133.
61. Liu, J.W., Huang, S., DeMichele, M., Bergana, E., Bobik, C., Hastilow, L.T., Chuang, P., Mukerji, S. and Knutzon, D. (2001) Evaluation of the seed oils from a canola plant genetically transformed to produce high levels of γ-linolenic acid. In γ-Linolenic Acid: Recent Advances in Biotechnology and Clinical Applications (Huang, Y.S., Ziboh, V.A., eds), pp. 61-71. Champaign, IL: AOCS Press.
62. Logue, J. and Sattar, N. (2011) Childhood obesity: a ticking time bomb for cardiovascular disease? Clin. Pharmacol. Ther. 90, 174-178.
63. Lu, C.F., Xin, Z.G., Ren, Z.H., Miquel, M. and Browse, J. (2009) An enzyme regulating triacylglycerol composition is encoded by the ROD1 gene of Arabidopsis. Proc. Natl Acad. Sci. U.S.A. 106, 18837-18842.
64. Metz, J.G., Roessler, P., Facciotti, D., Levering, C., Dittrich, F., Lassner, M., Valentine, R., Lardizabal, K., Domergue, F., Yamada, A., Yazawa, K., Knauf, V. and Browse, J. (2001) Production of polyunsaturated fatty acids by polyketide synthases in both prokaryotes and eukaryotes. Science, 293, 290-293.
65. Metz, J.G., Kuner, J., Rosenzweig, B., Lippmeier, J.C., Roessler, P. and Zirkle, R. (2009) Biochemical characterization of polyunsaturated fatty acid synthesis in Schizochytrium: release of the products as free fatty acids. Plant Physiol. Biochem. 47, 472-478.
66. Meyer, A., Cirpus, P., Ott, C., Shlecker, R., Zähringer, U. and Heinz, E. (2004a) Biosynthesis of docosahexaenoic acid in Euglena gracilis: biochemical and molecular evidence for the involvement of a Δ4-fatty acyl group desaturase. Biochemistry, 42, 9779-9788.
67. Meyer, A., Kirsch, H., Domergue, F., Abbadi, A., Sperling, P., Bauer, J., Cirpus, P., Zank, T.K., Moreau, H., Roscoe, T.J., Zähringer, U. and Heinz, E. (2004b) Novel fatty acid elongases and their use for the reconstitution of docosahexaenoic acid biosynthesis. J. Lipid Res. 45, 1899-1909.
68. Monsanto Company, Stearidonic (SDA) Omega-3 Soybean Oil GRAS Notice (2009) (http://www.accessdata.fda.gov/scripts/fcn/gras_notices/grn000283.pdf)
69. Mori, T.A., Watts, G.F., Burke, V., Hilme, E., Puddey, I.B. and Beilin, L.J. (2000) Differential effects of eicosapentaenoic acid and docosahexaenoic acid on vascular reactivity of the forearm microcirculation in hyperlipidemic, overweight men. Circulation, 102, 1264-1269.
70. Moriguchi, T. and Salem Jr, N. (2003) Recovery of brain docosahexaenoate leads to recovery of spatial task performance. J. Neurochem. 87, 297-309.
71. Morris, M.C., Evans, D.A., Bienias, J.L., Tangney, C.C., Bennett, D.A., Wilson, R.S., Aggarwal, N. and Schneider, J. (2003) Consumption of fish and n-3 fatty acids and risk of incident Alzheimer disease. Arch. Neurol. 60, 940-946.
72. Nakanishi, H., Shindou, H., Hishikawa, D., Harayama, T., Ogasawara, R., Suwabe, A., Taguchi, R. and Shimizu, T. (2006) Cloning and characterization of mouse lung-type acyl-CoA:lysophosphatidylcholine acyltransferase 1 (LPCAT1). Expression in alveolar type II cells and possible involvement in surfactant production. J. Biol. Chem. 281, 20140-20147.
73. Napier, J.A. (2007) The production of unusual fatty acids in transgenic plants. Annu. Rev. Plant Biol. 58, 295-319.
74. Napier, J.A. and Graham, I.A. (2010) Tailoring plant lipid composition: designer oilseeds come of age. Curr. Opin. Plant Biol. 13, 330-337.
75. Nestel, P., Shige, H., Pomeroy, S., Cehun, M., Abbey, M. and Raederstorff, D. (2002) The n-3 fatty acids eicosapentaenoic acid and docosahexaenoic acid increase systemic arterial compliance in humans. Am. J. Clin. Nutr. 76, 326-330.
76. Neuringer, M., Anderson, G.J. and Connor, W.E. (1988) The essentiality of n-3 fatty acids for the development and function of the retina and brain. Annu. Rev. Nutr. 8, 517-554.
77. Nykiforuk, C.L., Shewmaker, C., Harry, I., Yurchenko, O.P., Zhang, M., Reed, C., Oinam, G.S., Zaplachinski, S., Fidantsef, A., Boothe, J.G. and Moloney, M.M. (2012) High level accumulation of gamma linolenic acid (C18:3Δ6.9, 12 cis) in transgenic safflower (Carthamus tinctorius) seeds. Transgenic Res. 21, 367-381.
78. Ohlrogge, J. and Browse, J. (1995) Lipid biosynthesis. Plant Cell, 7, 957-970.
79. Ohlrogge, J.B. and Jaworski, J.G. (1997) Regulation of fatty acid synthesis. Annu. Rev. Plant Physiol. 48, 109-136.
80. Parker-Barnes, J.M., Das, T., Bobik, E., Leonard, A.E., Thurmond, J.M., Chaung, L.T., Huang, Y.S. and Mukerji, P. (2000) Identification and characterization of an enzyme involved in the elongation of n-6 and n-3 polyunsaturated fatty acid. Proc. Natl Acad. Sci. U.S.A. 97, 8284-8289.
81. Pauly, D., Christensen, V.V., Dalsgaard, J., Froese, R. and Torres Jr, F. (1998) Fishing down marine food webs. Science, 279, 860-863.
82. Pereira, S.L., Leonard, A.E., Huang, Y.S., Chuang, L.T. and Mukerji, P. (2004) Identification of two novel microalgal enzymes involved in the conversion of the omega-3-fatty acid, eicosapentaenoic acid, into docosahexaenoic acid. Biochem. J. 384, 357-366.
83. Petrie, J.R., Shrestha, P., Mansour, M.P., Nichols, P.D., Liu, Q. and Singh, S.P. (2010) Metabolic engineering of omega-3 long-chain polyunsaturated fatty acids in plants using an acyl-CoA Δ6-desaturase with omega-3 preference from the marine microalga Micromonas pusilla. Metab. Eng. 12, 233-240.
84. Petrie, J.R., Shrestha, P., Belide, S., Mansour, M.P., Liu, Q., Horne, J., Nichols, P.D. and Singh, S.P. (2012a) Transgenic production of arachidonic acid in oilseeds. Transgenic Res. 21, 139-147.
85. Petrie, J.R., Vanhercke, T., Shrestha, P., El Tahchy, A., White, A., Zhou, X.R., Liu, Q., Mansour, M.P., Nichols, P.D. and Singh, S.P. (2012b) Recruiting a new substrate for triacylglycerol synthesis in plants: the monoacylglycerol acyltransferase pathway. PLoS ONE, 7, e35214.
86. 18 Δ-9 polyunsaturated fatty acid-specific elongating activity from the docosahexaenoic acid (DHA)-producing microalga, Isocarysis galbana. FEBS Lett. 510, 159-165.
87. Qi, B., Fraser, T., Mugford, S., Dobson, G., Sayanova, O., Butler, J., Napier, J.A., Stobart, A.K. and Lazarus, C.M. (2004) Production of very long chain polyunsaturated ω-3 and ω-6 fatty acids in plants. Nat. Biotechnol. 22, 739-745.
88. Reddy, A.S. and Thomas, T.L. (1996) Expression of a cyanobacterial 6-desaturase gene results in gamma-linolenic acid production in transgenic plants. Nat. Biotechnol. 14, 639-642.
89. van de Rest, O., Geleijnse, J.M., Kok, F.J., van Staveren, W.A., Dullemeijer, C., Olderikkert, M.G., Beekman, A.T. and de Groot, C.P. (2008) Effect of fish oil on cognitive performance in older subjects: a randomized, controlled trial. Neurology, 71, 430-438.
90. Robert, S., Singh, S.P., Zhou, X.R., Petrie, J.R., Blackburn, S.I., Mansour, P.M., Nichols, P.D., Liu, Q. and Green, A. (2005) Metabolic engineering of Arabidopsis to produce nutritionally important DHA in seed oil. Funct. Plant Biol. 32, 473-479.
91. Ruiz-Lopez, N., Haslam, R.P., Venegas-Calerón, M., Larson, T.R., Graham, I.A., Napier, J.A. and Sayanova, O.V. (2009) The synthesis and accumulation of stearidonic acid in transgenic plants: a novel source of 'heart-healthy' ω-3 fatty acids. Plant Biotechnol. J. 7, 704-716.
92. Ruiz-Lopez, N., Haslam, R.P., Venegas-Calerón, M., Li, T., Bauer, J., Napier, J.A. and Sayanova, O.V. (2012) Enhancing the accumulation of omega-3 long chain polyunsaturated fatty acids in transgenic Arabidopsis thaliana via iterative metabolic engineering and genetic crossing. Transgenic Res. First published 21st February doi: 10.1007/s11248-012-9596-0.
93. Saito, Y., Yokoyama, M., Origasa, H., Matsuzaki, M., Matsuzawa, Y., Ishikawa, Y., Oikawa, S., Sasaki, J., Hishida, H., Itakura, H., Kita, T., Kitabatake, A., Nakaya, N., Sakata, T., Shimada, K. and Shirato, K. (2008) Effects of EPA on coronary artery disease in hypercholesterolemic patients with multiple risk factors: sub-analysis of primary prevention cases from the Japan EPA Lipid Intervention Study (JELIS). Atherosclerosis, 200, 135-140.
94. Sakuradani, E., Ando, A., Ogawa, J. and Shimizu, S. (2009) Improved production of various polyunsaturated fatty acids through filamentous fungus Mortierella alpina breeding. Appl. Microbiol. Biotechnol. 84, 1-10.
95. Saravanan, P., Davidson, N.C., Schmidt, E.B. and Calder, P.C. (2010) Cardiovascular effects of marine omega-3 fatty acids. Lancet, 376, 540-550.
96. Sasaki, Y. and Nagano, Y. (2004) Plant acetyl-CoA carboxylase: structure, biosynthesis, regulation, and gene manipulation for plant breeding. Biosci. Biotechnol. Biochem. 68, 1175-1184.
97. Sato, S., Xing, A., Ye, X., Schweiger, B., Kinnet, A. and Clemente, T. (2004) Production of γ-linolenic acid and stearidonic acid in seeds of marker-free transgenic soybean. Crop Sci. 44, 646-652.
98. Sayanova, O.V. and Napier, J.A. (2004) Eicosapentaenoic acid: biosynthetic routes and the potential for synthesis in transgenic plants. Phytochemistry, 65, 147-158.
99. Sayanova, O.V., Smith, M.A., Lapinskas, P., Stobart, A.K., Dobson, G., Christie, W.W., Shewry, P.R. and Napier, J.A. (1997) Expression of a B. officinalis desaturase cDNA containing an N-terminal cytochrome b5 domain results in the accumulation of high levels of Δ6-desaturated fatty acids in transgenic tobacco. Proc. Natl Acad. Sci. U.S.A. 94, 4211-4216.
100. Sayanova, O.V., Beaudoin, F., Michaelson, L.V., Shewry, P.R. and Napier, J.A. (2003) Identification of Primula fatty acid Δ6-desaturases with n-3 substrate preferences. FEBS Lett. 542, 100-104.
101. 20 Δ8-desaturase from the non-photosynthetic organism Acanthamoeba castellanii is an atypical cytochrome b5-fusion desaturase. FEBS Lett. 580, 1946-1952.
102. Sayanova, O.V., Haslam, R.P., Calerón, M.V., Ruiz-López, N., Worthy, C., Rooks, P., Allen, M.J. and Napier, J.A. (2011) Identification and functional characterisation of genes encoding the omega-3 polyunsaturated fatty acid biosynthetic pathway from the coccolithophore Emiliania huxleyi. Phytochemistry, 72, 594-600.
103. Sayanova, O., Ruiz-Lopez, N., Haslam, R.P. and Napier, J.A. (2012) The role of Δ6-desaturase acyl-carrier specificity in the efficient synthesis of long-chain polyunsaturated fatty acids in plants. Plant Biotechnol. J. 10, 195-206.
104. Schmutz, J., Cannon, S.B., Schlueter, J., Ma, J., Mitros, T., Nelson, W., Hyten, D.L., Song, Q., Thelen, J.J., Cheng, J., Xu, D., Hellsten, U., May, G.D., Yu, Y., Sakurai, T., Umezawa, T., Bhattacharyya, M.K., Sandhu, D., Valliyodan, B., Lindquist, E., Peto, M., Grant, D., Shu, S., Goodstein, D., Barry, K., Futrell-Griggs, M., Abernathy, B., Du, J., Tian, Z., Zhu, L., Gill, N., Joshi, T., Libault, M., Sethuraman, A., Zhang, X.C., Shinozaki, K., Nguyen, H.T., Wing, R.A., Cregan, P., Specht, J., Grimwood, J., Rokhsar, D., Stacey, G., Shoemaker, R.C. and Jackson, S.A. (2010) Genome sequence of the palaeopolyploid soybean. Nature, 463, 178-183.
105. Scientific Advisory Committee on Nutrition (2004) Advice on Fish Consumption: Benefits and Risks. SACN/COT Report. London: The Stationery Office.
106. Severin, A.J., Woody, J.L., Bolon, Y.T., Joseph, B., Diers, B.W., Farmer, A.D., Meuhlbauer, G.J., Nelson, R.T., Grant, D., Specht, J.E., Graham, S.B., May, G.D., Vance, C.P. and Shoemaker, R.C. (2010) RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol. 10, 160.
107. Soderberg, M., Edlund, C., Kristensson, K. and Dallner, G. (1999) Fatty acid composition of brain phospholipids in aging and in Alzheimer's disease. Lipids, 26, 421-425.
108. Somerville, C. and Browse, J. (1991) Plant lipids: metabolism, mutants and membranes. Science, 252, 80-87.
109. Sprecher, H., Chen, Q. and Yin, F.Q. (1999) Regulation of the biosynthesis of 22:5 n-6 and 22:6 n-3: a complex intracellular process. Lipids, 34, 153-156.
110. Ståhl, U., Stålberg, K., Stymne, S. and Ronne, H. (2008) A family of eukaryotic lysophospholipid acyltransferases with broad specificity. FEBS Lett. 582, 305-309.
111. Sugimoto, Y., Taga, C., Nishiga, M., Fujiwara, M., Konishi, F., Tanaka, K. and Kamei, C. (2002) Effect of docosahexaenoic acid-fortified Chlorella vulgaris strain CK22 on the radial maze performance in aged mice. Biol. Pharm. Bull. 25, 1090-1092.
112. Suzuki, H., Park, S.J., Tamura, M. and Ando, S. (1998) Effect of the long-term feeding of dietary lipids on the learning ability, fatty acid composition of brain stem phospholipids and synaptic membrane fluidity in adult mice: a comparison of sardine oil diet with palm oil diet. Mech. Ageing Dev. 101, 119-128.
113. Tacon, A.G. and Metian, M. (2009) Fishing for feed or fishing for food: increasing global competition for small pelagic forage fish. Ambio, 38, 294-302.
114. Tanaka, K., Ishikawa, Y., Yokoyama, M., Origasa, H., Matsuzaki, M., Saito, Y., Matsuzawa, Y., Sasaki, J., Oikawa, S., Hishida, H., Itakura, H., Kita, T., Kitabatake, A., Nakaya, N., Sakata, T., Shimada, K., Shirato, K. and JELIS Investigators, Japan (2008) Reduction in the recurrence of stroke by eicosapentaenoic acid for hypercholesterolemic patients: subanalysis of the JELIS trial. Stroke, 39, 2052-2058.
115. Tocher, D.R. (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev. Fish. Sci. 11, 107-184.
116. Troncoso-Ponce, M.A., Kilaru, A., Cao, X., Durrett, T.P., Fan, J., Jensen, J.K., Thrower, N.A., Pauly, M., Wilkerson, C. and Ohlrogge, J.B. (2011) Comparative deep transcriptional profiling of four developing oilseeds. Plant J. 68, 1014-1027.
117. Tumaney, A.W., Shekar, S. and Rajasekharan, R. (2001) Identification, purification, and characterization of monoacylglycerol acyltransferase from developing peanut cotyledons. J. Biol. Chem. 276, 10847-10852.
118. Uauy, R. and Dangour, A.D. (2006) Nutrition in brain development and aging: role of essential fatty acids. Nutr. Rev. 64, S24-S33; discussion S72-91.
119. Ulsamer, A.G., Smith, F.R. and Korn, E.D. (1969) Lipids of Acanthamoeba castellanii. Composition and effects of phagocytosis on incorporation of radioactive precursors. J. Cell Biol. 43, 105-114.
120. Ursin, V.M. (2003) Modification of plant lipids for human health: development of functional land-based omega-3 fatty acids. J. Nutr. 133, 4271-4274.
121. Wallis, J.G. and Browse, J. (1999) The Δ8-desaturase of Euglena gracilis: an alternate pathway for synthesis of 20-carbon polyunsaturated fatty acids. Arch. Biochem. Biophys. 365, 307-316.
122. Wang, Z., Hobson, N., Galindo, L., Zhu, S., Shi, D., McDill, J., Yang, L., Hawkins, S., Neutelings, G., Datla, R., Lambert, G., Galbraith, D.W., Grassa, C.J., Geraldes, A., Cronk, Q.C., Cullis, C., Dash, P.K., Kumar, P.A., Cloutier, S., Sharpe, A.G., Wong, G., Wang, J. and Deyholos, M.K. (2012) The genome of flax (Linum usitatissimum) assembled de novo from short shotgun sequence reads. Plant J. First published. July 3rd doi: 10.1111/j.1365-313X.2012.05093.x
123. Williams, C.M. and Burdge, G. (2006) Long-chain n-3 PUFA: plant v. marine sources. Proc. Nutr. Soc. 65, 42-50.
124. Wood, C.C., Petrie, J.R., Shrestha, P., Mansour, M.P., Nichols, P.D., Green, A.G. and Singh, S.P. (2009) A leaf-based assay using interchangeable design principles to rapidly assemble multistep recombinant pathways. Plant Biotechnol. J. 7, 914-924.
125. Wu, G., Truksa, M., Datla, N., Vrinten, P., Bauer, J., Zank, T., Cirpus, P., Heinz, E. and Qiu, X. (2005) Stepwise engineering to produce high yields of very long-chain polyunsaturated fatty acids in plants. Nat. Biotechnol. 23, 1013-1017.
126. Xiao, S., Gao, W., Chen, Q.F., Chan, S.W., Zheng, S.X., Ma, J., Wang, M., Welti, R. and Chye, M.L. (2010) Overexpression of Arabidopsis Acyl-CoA binding protein ACBP3 promotes starvation-induced and age-dependent leaf senescence. Plant Cell, 22, 1463-1482.
127. Xu, X. and Akoh, C.C. (2002) Enzymatic production of betapol and other specialty fats. Chapter 22. In Lipid Biotechnology (Gardner, H.W. and Kuo, T.M. eds), pp. 461-478. Boca Raton, FL: CRC Press, ISBN: 978-0-8247-0619-7.
128. Yang, P., Li, X., Shipp, M.J., Shockey, J.M. and Cahoon, E.B. (2010a) Mining the bitter melon (Momordica charantia l.) seed transcriptome by 454 analysis of non-normalized and normalized cDNA populations for conjugated fatty acid metabolism-related genes. BMC Plant Biol. 10, 250.
129. Yang, W., Pollard, M., Li-Beisson, Y., Beisson, F., Feig, M. and Ohlrogge, J. (2010b) A distinct type of glycerol-3-phosphate acyltransferase with sn2 preference and phosphatase activity producing 2-monoacylglycerol. Proc. Natl Acad. Sci. U.S.A. 107, 12040-12045.
130. Yang, W., Simpson, J.P., Li-Beisson, Y., Beisson, F., Pollard, M.R. and Ohlrogge, J.B. (2012) A land-plant-specific glycerol-3-phosphate acyltransferase family in Arabidopsis: substrate specificity, sn-2 preference and evolution. Plant Physiol. doi: 10.1104/pp.112.201996.
131. Yen, C.L.E., Stone, S.J., Cases, S., Zhou, P. and Farese, R.V. (2002) Identification of a gene encoding MGAT1, a monoacylglycerol acyltransferase. Proc. Natl Acad. Sci. U.S.A. 99, 8512-8517.
132. Yokoyama, M., Origasa, H., Matsuzaki, M., Matsuzawa, Y., Saito, Y., Ishikawa, Y., Oikawa, S., Sasaki, J., Hishida, H., Itakura, H., Kita, T., Kitabatake, A., Nakaya, N., Sakata, T., Shimada, K., Shirato, K. and Japan EPA Lipid Intervention Study (JELIS) Investigators (2007) Effects of eicosapentaenoic acid on major coronary events in hypercholesterolaemic patients (JELIS): a randomized open-label, blinded endpoint analysis. Lancet, 369, 1090-1098.
133. Yurchenko, O.P., Nykiforuk, C.L., Moloney, M.M., Stahl, U., Banas, A., Stymne, S. and Weselake, R.J. (2009) A 10-kDa acyl-CoA-binding protein (ACBP) from Brassica napus enhances acyl exchange between acyl-CoA and phosphatidylcholine. Plant Biotechnol. J. 7, 602-610.
134. Yurko-Mauro, K., McCarthy, D., Rom, D., Nelson, E.B., Ryan, A.S., Blackwell, A., Salem Jr, N. and Stedman, M. (2010) Beneficial effects of docosahexaenoic acid on cognition in age-related cognitive decline. Alzheimers Dement. 6, 456-464.
135. Zank, T.K., Zähringer, U., Beckmann, C., Pohnert, G., Boland, W., Holtorf, H., Reski, R., Lerchl, J. and Heinz, E. (2002) Cloning and functional characterisation of an enzyme involved in the elongation of Δ6-polyunsaturated fatty acids from the moss Physcomitrella patens. Plant J. 31, 255-268.
136. Zhaohui, H., Zhanghai, R. and Lu, C. (2012) The phosphatidylcholine:diacylglycerol cholinephosphotransferase is required for efficient hydroxy fatty acid accumulation in transgenic Arabidopsis. Plant Physiol. 158, 1944-1954.
137. Zheng, Q., Li, J.Q., Kazachkou, M., Liu, K. and Zou, J. (2012) Identification of Brassica napus lysophosphatidylcholine acyltransferase genes through yeast functional screening. Phytochemistry, 75, 21-31.
138. Zhou, X.R., Robert, S.S., Petrie, J.R., Frampton, D.M.F., Mansour, M.P., Blackburn, S.I., Nichols, P.D., Green, A. and Singh, P.S. (2007) Isolation and characterization of genes from the marine microalga Pavlova salina encoding three front-end desaturases involved in docosahexaenoic acid biosynthesis. Phytochemistry, 68, 785-796.
139. Zhou, X.R., Horne, I., Damcevski, K., Haritos, V., Green, A. and Singh, P.S. (2008) Isolation and functional characterization of two independently-evolved fatty acid Δ12-desaturase genes from insects. Insect Mol. Biol. 17, 667-676.