A nutritionally-enhanced oil from transgenic Camelina sativa effectively replaces fish oil as a source of eicosapentaenoic acid for fish

Scientific Reports

Volumn 5, Issue , 2015, Pages 8104-

  Betancor, M B ^a   Sprague, M ^a   Usher, S ^b   Sayanova, O ^b   Campbell, P J ^c   Napier, J A ^b   Tocher, D R ^a  

^a UNIVERSITY OF STIRLING   (United Kingdom)

^b ROTHAMSTED RESEARCH   (United Kingdom)

^c BioMar Group   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DOCOSAHEXAENOIC ACID; FISH OIL; ICOSAPENTAENOIC ACID; TRANSCRIPTOME; VEGETABLE OIL;

ANIMAL; ANIMAL FOOD; BRASSICACEAE; CECUM; CHEMISTRY; DIET; DNA MICROARRAY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIVER; METABOLISM; MUSCLE; NUTRITIONAL VALUE; PLANT SEED; REPRODUCIBILITY; SALMO SALAR; SURVIVAL ANALYSIS; TRANSGENIC PLANT;

ANIMAL FEED; ANIMALS; BRASSICACEAE; CECUM; DIET; DNA; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; FISH OILS; GENE EXPRESSION PROFILING; LIVER; MUSCLES; NUTRITIVE VALUE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT OILS; PLANTS, GENETICALLY MODIFIED; REPRODUCIBILITY OF RESULTS; SALMO SALAR; SEEDS; SURVIVAL ANALYSIS; TRANSCRIPTOME;

EID: 84922998544     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep08104     Document Type: Article

References (59)

1. Calder, P. C. n-3 Fatty acids, inflammation and immunity: new mechanisms to explain old actions. Proc. Nutr. Soc. 72, 326-336 (2013).
2. Gil, A., Serra-Majem, L., Calder, P. C. & Uauy, R. Systematic reviews of the role of omega-3 fatty acids in the prevention and treatment of disease. Br. J. Nutr. 107, S1-S2 (2012).
3. Campoy, C., Escolano-Margarit, V., Anjos, T., Szajewska, H. & Uauy, R. Omega 3 fatty acids on child growth, visual acuity and neurodevelopment. Br. J. Nutr. 107, S85-S106 (2012).
4. Delgado-Lista, J., Perez-Martinez, P., Lopez-Miranda, J. & Perez-Jimenez, F. Long chain omega-3 fatty acids and cardiovascular disease: a systematic review. Br. J. Nutr. 107, S201-S213 (2012).
5. Miles, E. A. & Calder, P. C. Influence of marine n-3 polyunsaturated fatty acids on immune function and a systematic review of their effects on clinical outcomes in rheumatoid arthritis. Br. J. Nutr. 107, S171-S184 (2012).
6. Rangel-Huerta, O. D.,Aguilera, C. M.,Mesa, M. D.&Angel Gil, A. Omega-3 longchain polyunsaturated fatty acids supplementation on inflammatory biomakers: a systematic review of randomised clinical trials. Br. J. Nutr. 107, S159-S170 (2012).
7. Laviano, A., Rianda, S., Molfino, A. & Rossi Fanelli, F. Omega-3 fatty acids in cancer. Curr. Opin. Clin. Nutr. Metabolic Care 16, 156-161 (2013).
8. Raatz, S. K., Silverstein, J. T., Jahns, L. & Picklow,M. J. Issues of fish consumption for cardiovascular disease risk reduction. Nutrients 5, 1081-1097 (2013).
9. Cunnane, S. et al. Recommendations for intake of polyunsaturated fatty acids in healthy adults, (2004) Date of access: 08/06/2004, at http://www.issfal.org/newslinks/resources/publications/PUFAIntakeReccomdFinalReport.pdf.
10. Naylor, R. L. et al. Feeding aquaculture in an era of finite resources. Proc. Natl. Acad. Sci. U.S.A. 106, 15103-15110 (2009).
11. Harwood, J. L. & Guschina, I. A. The versatility of algae and their lipid metabolism. Biochimie 91, 679-684 (2009).
12. Tur, J. A., Bibiloni, M. M., Sureda, A. & Pons, A. Dietary sources of omega 3 fatty acids: public health risks and benefits. Br. J. Nutr. 107, S23-S52 (2012).
13. Worms, B. et al. Impacts of biodiversity loss on ocean ecosystem services. Science 314, 787-790 (2006).
14. FAO. State of World Fisheries and Aquaculture 2014. Food and Agriculture Organization of the United Nations, Rome (2014). Date of access: 20/06/2014, at http://www.fao.org/3/a-i3720e.pdf.
15. Tocher, D. R. Metabolism and functions of lipids and fatty acids in teleost fish. Rev. Fisheries Sci. 11, 107-184 (2003).
16. Tacon, A. G. J. & Metian, M. Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: Trends and future prospects. Aquaculture 285, 146-158 (2008).
17. National Research Council (NRC). Nutrient Requirements of Fish and Shrimp. The National Academies Press, Washington, DC (2011).
18. Turchini, G. M., Ng, W.-K. & Tocher, D. R. (Eds) Fish Oil Replacement and Alternative Lipid Sources in Aquaculture Feeds. Taylor & Francis, CRC Press (2010).
19. Tocher, D. R. Issues surrounding fish as a source of omega-3 long-chain polyunsaturated fatty acids. Lipid Technol. 21, 13-16 (2009).
20. Wu, G. et al. Stepwise engineering to produce high yields of very long-chain polyunsaturated fatty acids in plants. Nat. Biotechnol. 23, 1013-1017 (2005).
21. Venegas-Caleron, M., Sayanova, O. & Napier, J. A. An alternative to fish oils: Metabolic engineering of oil-seed crops to produce omega-3 long chain polyunsaturated fatty acids. Prog. Lipid Res. 49, 108-119 (2010).
22. Xue, Z. et al. Production of omega-3 eicosapentaenoic acid by metabolic engineering of Yarrowia lipolytica. Nat. Biotechnol. 31, 734-740 (2013).
23. Hamilton, M. L., Haslam, R. P., Napier, J. A. & Sayanova, O. Metabolic engineering of Phaeodactylum tricornutum for the enhanced accumulation of omega-3 long chain polyunsaturated fatty acids. Metab. Eng. 22, 3-9 (2014).
24. Salunkhe, D. K., Adsule, R. N., Chavan, J. K. & Kadam, S. S. World Oilseeds: Chemistry, Technology and Utilization. Van Nostrand Reinhold Company (1992).
25. Sayanova,O.&Napier, J. A. 2011. Transgenic oilseed crops as an alternative to fish oils. Prostaglandins Leukotrienes Essent. Fatty Acids 85, 253-260 (2011).
26. Haslam, R. P. et al. The modification of plant oil composition via metabolic engineering - better nutrition by design. Plant Biotechnol. J. 11, 157-168 (2013).
27. Petrie, J. R. et al.Metabolic engineering plant seeds with fish oil-like levels of DHA. PLoS ONE 7, e49165 (2012).
28. Ruiz-Lopez, N., Haslam, R. P., Usher, S. L., Napier, J. A. & Sayanova, O. Reconstitution of EPA and DHA biosynthesis in Arabidopsis: iterative metabolic engineering for the synthesis of n-3 LC-PUFAs in transgenic plants. Metab. Eng. 17, 30-41 (2013).
29. Petrie, J. R. et al.Metabolic engineering Camelina sativa with fish oil-like levels of DHA. PLoS ONE 9, e85061 (2014).
30. Ruiz-Lopez, N., Haslam, R. P., Napier, J. A. & Sayanova, O. Successful high-level accumulation of fish oil omega-3 long-chain polyunsaturated fatty acids in a transgenic oilseed crop. Plant J. 77, 198-208 (2014).
31. rd Ed. Taylor & Francis, CRC Press (2007).
32. Morais, S., Edvardsen, R. B., Tocher, D. R. & Bell, J. G. Transcriptomic analyses if intestinal gene expression of juvenile Atlantic cod (Gadus morhua) fed diets with Camelina oil as replacement for fish oil. Comp. Biochem. Physiol. B 161, 283-293 (2012).
33. Hixson, S. M., Parrish, C. C. & Anderson, D. M. Full substitution of fish oil with camelina (Camelina sativa) oil, with partial substitution of fish meal with camelinameals, in diets for farmed Atlantic salmon (Salmo salar) and its effect on tissue lipids and sensory quality. Food Chem. 157, 51-61 (2014a).
34. Hixson, S. M. & Parrish, C. C. Substitution of fish oil with camelina oil and inclusion of camelina meal in diets fed to Atlantic cod (Gadus morhua) and their effects on growth, tissue lipid classes and fatty acids. J. Anim. Sci. doi: 10.2527/jas.2013-7146 (2014b).
35. Glencross, B. D. Exploring the nutritional demand for essential fatty acids by aquaculture species. Rev. Aquaculture 1, 71-124 (2009).
36. Bendiksen, E. A., Johnsen, C. A., Olsen, H. J. & Jobling, M. Sustainable aquafeeds: progress towards reduced reliance upon marine ingredients in diets for farmed Atlantic salmon (Salmo salar L.). Aquaculture 314, 132-139 (2011).
37. Torstensen, B. E., Espe, M., Stubhaug, I. & Lie, O. Dietary plant proteins and vegetable oil blends increase adiposity and plasma lipids in Atlantic salmon (Salmo salar L.). Br. J. Nutr. 106, 633-647 (2011).
38. Kim, H. K., Della-Fera, M., Lin, J. & Baile, C. A. Docosahexaenoic acid inhibits adipocyte differentiation and induces apoptosis in 3T3-L1 preadipocytes. J. Nutr. 136, 2965-2969 (2006).
39. Todorcević, M. et al. Changes in fatty acids metabolism during differentiation of Atlantic salmon preadipocytes; effects of n-3 and n-9 fatty acids. Biochim. Biophys. Acta 1781, 326-335 (2008).
40. Izquierdo, M. S. et al. Dietary lipid sources for seabream and seabass: growth performance, tissue composition and flesh quality. Aquacult. Nutr. 9, 397-407 (2003).
41. Menoyo, D. et al. Adaptation of lipid metabolism, tissue composition and flesh quality in gilthead sea bream (Sparus aurata) to the replacement of dietary fish oil by linseed and soyabean oils. Br. J. Nutr. 92, 41-52 (2004).
42. 2α immune function and effectiveness of a fish oil finishing diet. Aquacult. Nutr. 11, 25-40 (2005).
43. Bell, J. G., Henderson, R. J., Tocher, D. R. & Sargent, J. R. Replacement of dietary fish oil with increasing levels of linseed oil: modification of flesh fatty acid compositions in Atlantic salmon (Salmo salar) using a fish oil finishing diet. Lipids 39, 223-232 (2004).
44. Bell, J. G. et al. Growth, flesh adiposity and fatty acid composition of Atlantic salmon (Salmo salar) families with contrasting flesh adiposity: Effects of replacement of dietary fish oil with vegetable oils. Aquaculture 306, 225-232 (2010).
45. Buzzi, M., Henderson, R. J. & Sargent, J. R. Biosynthesis of docosahexaenoic acid in trout hepatocytes proceeds via 24-carbon intermediates. Comp. Biochem. Physiol. B 116, 263-267 (1997).
46. Thomassen, M. S., Berge, R. D., Gerd, M., Østbyestbye, T. K. & Ruyter, B. High dietary EPA does not inhibit D5 and D6 desaturases in Atlantic salmon (Salmo salar L.) fed rapeseed oil diets. Aquaculture 360-361, 78-85 (2012).
47. Leaver, M. J. et al. Functional genomics reveals increases in cholesterol biosynthetic genes and highly unsaturated fatty acid biosynthesis after dietary substitution of fish oil with vegetable oils in Atlantic salmon (Salmo salar). BMC Genomics 9, 299 (2008).
48. Morais, S. et al. Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: a liver transcriptomic analysis. BMC Genomics 12, 255 (2011a).
49. Morais, S. et al. Diet x genotype interactions in hepatic cholesterol and lipoprotein metabolism in Atlantic salmon (Salmo salar) in response to replacement of dietary fish oil with vegetable oil. Br. J. Nutr. 106, 1457-1469 (2011b).
50. Calduch-Giner, J. A. et al. Dietary vegetable oils do not alter the intestine transcriptome of gilthead sea bream (Sparus aurata), but modulate the transcriptomic response to infection with Enteromyxum leei. BMC Genomics 13, 470 (2012).
51. Limtipsuntorn, U.,Haga, Y., Kondo, H.,Hirono, I.& Satoh, S.Microarray analysis of hepatic gene expression in juvenile japanses flounder Paralichthys olivaceus fed diets supplemented with fish or vegetable oils. Mar Biotechnol 16, 88-102 (2014).
52. Gilman, C. I., Leusch, F. D., Breckenridge, W. C. & MacLatchy, D. L. Effects of a phytosterol mixture on male fish plasma lipoprotein fractions and testis P450scc activity. Gen. Comp. Endocrinol. 130, 172-184 (2003).
53. Mackay, D. S. & Jones, P. J. H. Phytosterols in human nutrition: Type, formulation, delivery, and physiological function. Eur. J. Lipid Sci. Tech. 113, 1427-1432 (2011).
54. AOAC. Official Methods of Analysis. Association of Official Analytical Chemists, Washington, DC (2000).
55. Folch, J., Lees, N. & Sloane-Stanley, G. H. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226, 497-509 (1957).
56. Henderson, R. J. & Tocher, D. R. Thin-layer chromatography. Lipid Analysis. [Hamilton, R. J. & Hamilton, S. (eds.)] [65-111] (Oxford University Press, Oxford, 1992.
57. rd Ed. Oily Press, Bridgwater (2003).
58. Tocher, D. R. & Harvie, D. G. Fatty acid compositions of the major phosphoglycerides from fish neural tissues; (n-3) and (n-6) polyunsaturated fatty acids in rainbow trout (Salmo gairdneri) and cod (Gadus morhua) brains and retinas. Fish Physiol. Biochem. 5, 229-239 (1988).
59. Pfaffl, M. W., Morgan, G. W. & Dempfle, L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36 (2002).