Regulation and enhancement of lipid accumulation in oil crops: The use of metabolic control analysis for informed genetic manipulation

European Journal of Lipid Science and Technology

Volumn 115, Issue 11, 2013, Pages 1239-1246

  Harwood, John L ^a   Ramli, Umi S ^a   Tang, Mingguo ^a   Quant, Patti A ^b   Weselake, Randall J ^c   Fawcett, Tony ^d   Guschina, Irina A ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF ALBERTA   (Canada)

^d DURHAM UNIVERSITY   (United Kingdom)

Author keywords

Metabolic control analysis; Oil crops; Regulation of oil accumulation; TAG synthesis

Indexed keywords

ANIMALIA; BRASSICA NAPUS; ELAEIS; GLYCINE MAX;

EID: 84887412351     PISSN: 14387697     EISSN: 14389312     Source Type: Journal    
DOI: 10.1002/ejlt.201300257     Document Type: Article

References (64)

1. Gunstone, F. D., Harwood, J. L., Dijkstra, A. J. (Eds.), The Lipid Handbook, 3rd Edn., Taylor and Francis, Boca Raton, FL 2007.
2. Murphy, D. J. (Ed.), Designer Oil Crops, VCH, Weinheim 1994.
3. Murphy, D. J. (Ed.), Plant Lipids: Biology, Utilisation and Manipulation, Blackwell Publishing, Oxford 2005.
4. Weselake, R. J., Taylor, D. C., Rahman, M. H., Shah, S. et al., Increasing the flow of carbon into seed oil. Biotech. Adv. 2009, 27, 866-878.
5. Bates, P. D., Stymne, S., Ohlrogge, J. B., Biochemical pathways in seed oil synthesis. Curr. Opin. Plant Biology 2013, 16, 358-364.
6. Banas, W., Garcia, A. S., Banas, A., Stymne, S., Activities of the acyl-CoA: Diacylglycerol acyltransferase (DGAT) and phospholipid: Diacylglycerol acyltransferase (PDAT) in microsomal preparations of developing sunflower and sunflower seeds. Planta 2013, 237, 1627-1636.
7. Xu, J., Carlsson, A. S., Francis, T., Zhang, M. et al., Triacylglycerol synthesis in the absence of DGAT1 activity is dependent on re-acylation of LPC by LPCAT2. BMC Plant Biol. 2012, 12, 4.
8. Pan, X., Siloto, R. M. P., Wickramarathna, A. D., Mietkiewska, E., Weselake, R. J., Identification of a pair of phospholipid:diacylglycerol acyltransferases from developing flax (Linum usitatitissiumum L.) seed catalysing the selective production of trilinolenin. J. Biol. Chem. 2013, 288, 24173-24188.
9. Gunstone, F. D. (Ed.), Rapeseed and Canola Oil - Production, Processing, Properties and Uses, Blackwell Publishing, Oxford 2004.
10. Ecke, W., Uzunova, M., Weissleder, K., Mapping the genome of rapeseed (Brassica napus L.) II. Localisation of genes controlling erucic acid synthesis and seed oil content. Theor. Appl. Genet. 1995, 91, 972-977.
11. Burns, M. J., Barnes, S. R., Bowman, J. G., Clarke, M. H. et al., QTL analysis of an intervarietal set of substitution lines in Brassica napus: (i) Seed oil content and fatty acid composition. Heredity 2003, 90, 39-48.
12. Zhao, J., Dimov, Z., Becker, H. C., Ecke, W., Mollers, C., Mapping QTL controlling fatty acid composition in a double haploid rapeseed population segregating for oil content. Mol. Breeding 2008, 21, 115-125.
13. Hobbs, D. H., Flintham, J. E., Hills, M. J., Genetic control of storage oil synthesis in seeds of Arabidopsis. Plant Physiol. 2004, 136, 3341-3349.
14. Mollers, C., Schierholt, A., Genetic variation of palmitate and oil content in a winter oilseed rape doubled haploid population segregating for oleate content. Crop Sci. 2002, 42, 379-384.
15. Focks, N., Benning, C., Wrinkled 1: A novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism. Plant Physiol. 1998, 118, 91-101.
16. Ruuska, S. A., Girke, T., Benning, C., Ohlrogge, J. B., Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell 2002, 14, 1191-1206.
17. Baud, S., Santos Mendoza, M., To, A., Lapiniec, L., Dubreucq, B., WRINKLED I specifies the regulatory action of LEAFY COTYLEDON 2 toward fatty acid metabolism during seed maturation in Arabidopsis. Plant J. 2007, 50, 825-838.
18. Cernac, A., Benning, C., WRINKLED 1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J. 2004, 40, 575-585.
19. Shen, B., Allen, W. B., Zheng, P., Li, C. et al., Expression of ZmLEC1 and ZmWRI 1 increases seed oil productions in maize. Plant Physiol. 2010, 153, 980-987.
20. To, A., Joubès, J., Barthole, G., Lécureuil, A. et al., WRINKLED transcription factors orchestrate tissue-specific regulation of fatty acid biosynthesis in Arabidopsis. Plant Cell, 2012, 24, 5007-5023.
21. Baud, S., Lepiniec, L., Physiological and developmental regulation of seed oil production. Prog. Lipid Res. 2010, 49, 235-249.
22. 14C]acetate precursor. Phytochemistry 1993, 33, 329-333.
23. Perry, H. J., Bligny, R., Gout, E., Harwood, J. L., Changes in Kennedy pathway intermediates associated with increased triacylglycerol synthesis in oil-seed rape. Phytochemistry 1999, 52, 799-804.
24. Weselake, R. J., Shah, S., Tang, M., Quant, P. et al., Metabolic control analysis is helpful for informed genetic manipulation of oilseed rape to increase seed oil content. J. Exp. Bot. 2008, 59, 3543-3549.
25. Katavic, V., Reed, D. W., Taylor, D. C., Giblin, E. M. et al., Alteration of seed fatty acid composition by a ethyl methanesulfonate-induced mutation in Arabidopsis thaliana affecting diacylglycerol acyltranferase activity. Plant Physiol. 1995, 108, 399-409.
26. Jako, C., Kumar, A., Wei, Y., Zou, J. et al., Seed-specific over-expression of an Arabidopsis cDNA encoding a diacylglycerol acyltransferase enhances seed oil content and seed weight. Plant Physiol. 2001, 126, 861-864.
27. Liu, Q., Siloto, R. M. P., Lehner, R., Stone, S. J., Weselake, R. J., Acyl-CoA: Diacylglycerol acyltransferase: Molecular biology, biochemistry and biotechnology. Prog. Lipid Res. 2012, 51, 350-377.
28. Kacser, H., Burns, J. A., The control of flux. Symp. Soc. Exp. Biol. 1973, 32, 65-104.
29. Fell, D. A., Understanding the Control of Metabolism, Portland Press, London 1997.
30. Allen, D. K., Libourel, I. G. L., Shacher-Hill, Y., Metabolic flux analysis in plants: Coping with complexity. Plant Cell Environ. 2009, 32, 1241-1257.
31. 13C metabolic flux analysis. Plant J. 2011, 67, 513-525.
32. Alonso, A. P., Dale, V. L., Shacher-Hill, Y., Understanding fatty acid synthesis in developing maize embryos using metabolic flux analysis. Metab. Eng. 2010, 12, 488-497.
33. Page, R. A., Okada, S., Harwood, J. L., Acetyl-CoA carboxylase exerts strong flux control over lipid synthesis in plants. Biochim. Biophys. Acta 1994, 1210, 369-372.
34. Morandini, P., Control limits for accumulation of plant metabolites: Brute force is no substitute for understanding. Plant Biotechnol. J. 2013, 11, 253-267.
35. Ramli, U. S., Baker, D. S., Quant, P. A., Harwood, J. L., Control mechanisms operating for lipid biosynthesis differ in oil palm and olive callus cultures. Biochem. J. 2002, 364, 385-391.
36. Ramli, U. S., Baker, D. S., Quant, P. A., Harwood, J. L., Control analysis of lipid biosynthesis in tissue cultures of oil crops shows that flux control is shared between fatty acid synthesis and lipid assembly. Biochem. J 2002, 364, 393-401.
37. Ramli, U. S., Salas, J. J., Quant, P. A., Harwood, J. L., Metabolic control analysis reveals an important role for diacylglycerol acyltransferase in olive but not oil palm lipid accumulation. FEBS J. 2005, 272, 5764-5770.
38. Ramli, U. S., Salas, J. J., Quant, P. A., Harwood, J. L., Use of metabolic control analysis to give quantitative information on the control of lipid biosynthesis in the important oil crop, Elaeis guineensis (oil palm). New Phytol. 2009, 184, 330-339.
39. Guschina, I., Kinney, A., Quant, P. A., Harwood, J. L., Regulation of lipid biosynthesis in soybean cell cultures. Proc. 16th IPLS, Budapest, 1-4th June 2004.
40. Tang, M., Guschina, I. A., O'Hara, P., Slabas, A. R. et al., Metabolic control analysis of developing oilseed rape embryos shows that lipid assembly exerts significant control over oil accumulation. New Phytol. 2012, 196, 414-429.
41. Vigeolus, H., Waldeck, P., Zank, T., Geigenberg, P., Increasing seed oil content in oil-seed rape by overexpression of yeast glycerol 3-phosphate dehydrogenase under the control of a seed-specific promoter. Plant Biotechnol. J. 2007, 5, 431-441.
42. Jain, R. K., Coffey, M., Lai, K., Kumar, A., MacKenzie, S. L., Enhancement of seed oil content by expression of glycerol 3-phosphate acyltransferase genes. Biochem. Soc. Trans. 2000, 28, 958-961.
43. Zou, J.-T., Katavic, C., Giblin, E. M., Barton, D. L. et al., Modification of seed oil content and acyl composition in Brassica by expression of a yeast sn-2 acyltransferase gene. Plant Cell 1997, 9, 909-923.
44. Zou, J., Wei, Y., Jako, C., Kumar, A. et al., The Arabidopsis thaliana TAG1 mutant has a mutation in the diacylglycerol acyltransferase gene. Plant J. 1999, 19, 645-653.
45. Roesler, K., Shintani, D., Savage, L., Boddupelli, S., Ohlrogge, J. B., Targeting of the Arabidopsis homomeric acetyl-CoA carboxylase to plastids of rapeseeds. Plant Physiol. 1997, 113, 75-81.
46. Taylor, D. C., Zhang, Y., Kumar, A., Francis, T. et al., Molecular modification of triacylglycerol accumulation by over-expression of DGAT1 to produce canola with increased seed oil content under field conditions. Botany 2009, 82, 533-543.
47. Lu, C., Napier, J. A., Clements, T. E., Cahoon, E. B., New frontiers in oilseed biotechnology: Meeting the global demand for vegetable oils for food, feed, biofuel and industrial applications. Curr. Opin. Biotechnol. 2011, 22, 252-259.
48. Li, B. H., Cheng, C., Bui, A. Q., Wagmeister, J. A. et al., Global analysis of gene activity during Arabidopsis seed development, identification of seed-specific transcription factors. Proc. Natl. Acad. Sci. USA 2010, 107, 8063-8070.
49. Gehringer, A., Friedt, W., Luhs, W., Snowdon, R. J., Genetic mapping of agronomic traits in false flax (Camelina sativa). Genome, 2006, 49, 1555-1563.
50. Putnam, D. H., Budin, J. T., Field, L. A., Breene, W. M., in: Janick, J., Simon, J. E. (Eds.), New Crops, Wiley, New York 1993, pp. 314-322.
51. Lu, C., Kang, J., Generation of transgenic plants of a potential oilseed crop Camelina sativa by Agrobacterium-mediated transformation. Plant Cell Rep. 2008, 27, 273-278.
52. Nguyen, H. T., Seivan, J. E., Podicheti, R., Macrander, J. et al. Camelina seed transcriptomic: A tool for meal, oil improvement, translational research. Plant Biotechnol. J. 2013, 11, 759-769.
53. Chapman, K., Dyer, J. M., Mullen, R. T., Commentary: Why don't leaves get fat? Plant Sci. 2013, 207, 128-134.
54. Wu, G., Traksa, M., Datla, N., Vrinten, P. et al., Stepwise engineering to produce high yields of very long-chain polyunsaturated fatty acids in plants. Nat. Biotechnol. 2005, 23, 1013-1017.
55. Cheng, B., Wu, G., Vrinteu, P., Falk, K. et al., Towards the production of high levels of eicosapentaenoic acid in transgenic plants: The effects of different host species, genes and promoters. Transgenic Res. 2010, 19, 221-229.
56. 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. 2013, 17, 30-41.
57. Patric, J. R., Shrestha, P., Zhou, X. R., Mansour, M. P. et al., Metabolic engineering plant seeds with fish oil-like levels of DHA. PLos ONE 2012, 7, e49165.
58. Vanherke, T., El Tahchy, A., Shrestha, P., Zhou, X.-R. et al., Synergistic effect of WRI1, DGAT1 coexpression on triacylglycerol biosynthesis in plants. FEBS Lett. 2013, 587, 364-369.
59. Kelly, A. A., Shaw, E., Powers, S. J., Kurup, S., Eastmond, P. J., Suppression of the SUGAR-DEPENDENT1 triacylglycerol lipase family during seed development enhances oil yield in oilseed rape. Plant Biotechnol. J. 2012, 11, 355-361.
60. Li, M., Bahn, S. C., Fan, C., Li, J. et al. Patatin-related phospholipase pPLA 111δ increase oil content with long-chain fatty acids in Arabidopsis. Plant Physiol. 2013, 162, 39-51.
61. Schwender, J., Goffman, F., Ohlrogge, J. B., Shacher-Hill. Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds. Nature 2004, 432, 779-782.
62. Harper, A. L., Trick, M., Higgins, J., Fraser, F. et al., Association transcriptomes of traits in the polyploid crop species Brassica napus. Nature Biotech. 2012, 30, 798-802.
63. Hu, Z.-Y., Hua, W., Zhang, L., Deng, L.-B. et al., Seed structure characteristics to form ultrahigh oil content in rapeseed. PLOS ONE, 2013, 8, e62099.
64. Taylor, D. C., Katavic, V., Zou, J.-T., MacKenzie, S. L. et al., Field-testing of transgenic rapeseed cv. hero transformed with a yeast sn-2 acyltransferase results in increased oil content, erucic acid content and seed yield. Mol. Breed. 2001, 8, 317-322.