Genetic enhancement of oil content in potato tuber (Solanum tuberosum L.) through an integrated metabolic engineering strategy

Plant Biotechnology Journal

Volumn 15, Issue 1, 2017, Pages 56-67

  Liu, Qing ^a   Guo, Qigao ^a,b   Akbar, Sehrish ^a,c   Zhi, Yao ^a,d   El Tahchy, Anna ^a   Mitchell, Madeline ^a   Li, Zhongyi ^a   Shrestha, Pushkar ^a   Vanhercke, Thomas ^a   Ral, Jean Philippe ^a   Liang, Guolu ^b   Wang, Ming Bo ^a   White, Rosemary ^a   Larkin, Philip ^a   Singh, Surinder ^a   Petrie, James ^a  

^a CSIRO   (Australia)

^b SOUTHWEST UNIVERSITY   (China)

^c NATIONAL UNIVERSITY OF SCIENCES AND TECHNOLOGY   (Pakistan)

^d HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

DGAT1; oleosin; potato; Solanum tuberosum; triacylglycerol; WRI1

Indexed keywords

CARBOHYDRATE; DIGALACTOSYLDIACYLGLYCEROL; FATTY ACID; GALACTOLIPID; PHOSPHOLIPID; PLANT PROTEIN; STARCH; TRIACYLGLYCEROL; VEGETABLE OIL;

CHEMISTRY; CYTOLOGY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETIC ENHANCEMENT; GENETIC TRANSFORMATION; GENETICS; METABOLIC ENGINEERING; METABOLISM; PLANT GENE; PLANT TUBER; POTATO; PROCEDURES; SCANNING ELECTRON MICROSCOPY; TRANSGENIC PLANT; TRANSMISSION ELECTRON MICROSCOPY;

CARBOHYDRATES; FATTY ACIDS; GALACTOLIPIDS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC ENHANCEMENT; METABOLIC ENGINEERING; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; PHOSPHOLIPIDS; PLANT OILS; PLANT PROTEINS; PLANT TUBERS; PLANTS, GENETICALLY MODIFIED; SOLANUM TUBEROSUM; STARCH; TRANSFORMATION, GENETIC; TRIGLYCERIDES;

EID: 84978886104     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12590     Document Type: Article

References (57)

1. Andrianov, V., Borisjuk, N., Pogrebnyak, N., Brinker, A., Dixon, J., Spitsin, S., Flynn, J. et al. (2010) Tobacco as a production platform for biofuel: overexpression of Arabidopsis DGAT and LEC2 genes increases accumulation and shifts the composition of lipids in green biomass. Plant Biotechnol. J. 8, 277–287.
2. Baud, S., Mendoza, M.S., To, A., Harscoet, E., Lepiniec, L. and Dubreucq, B. (2007) WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis. Plant J. 50, 825–838.
3. Bourgis, F., Kilaru, A., Cao, X., Ngando-Ebongue, G.F., Drira, N., Ohlrogge, J.B. and Arondel, V. (2011) Comparative transcriptome and metabolite analysis of oil palm and date palm mesocarp that differ dramatically in carbon partitioning. Proc. Natl Acad. Sci. USA, 108, 12527–12532.
4. Bouvier-Nave, P., Benveniste, P., Oelkers, P., Sturley, S.L. and Schaller, H. (2000) Expression in yeast and tobacco of plant cDNAs encoding acyl CoA:diacylglycerol acyltransferase. Eur. J. Biochem. 267, 85–96.
5. Cernac, A. and Benning, C. (2004) WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J. 40, 575–585.
6. Chapman, K.D. and Ohlrogge, J.B. (2012) Compartmentation of triacylglycerol accumulation in plants. J. Biol. Chem. 287, 2288–2294.
7. Fan, J., Yan, C., Roston, R., Shanklin, J. and Xu, C. (2014) Arabidopsis lipins, PDAT1 acyltransferase, and SDP1 triacylglycerol lipase synergistically direct fatty acids toward beta-oxidation, thereby maintaining membrane lipid homeostasis. Plant Cell, 26, 4119–4134.
8. Focks, N. and Benning, C. (1998) wrinkled1: A novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism. Plant Physiol. 118, 91–101.
9. Galliard, T. (1970) The enzymic breakdown of lipids in potato tuber by phospholipid- and galactolipid-acyl hydrolase activities and by lipoxygenase. Phytochemistry, 9, 1725.
10. Galliard, T. (1972) Fatty acid composition of immature potato tubers. Phytochemistry, 11, 1899–1903.
11. Grierson, C., Du, J.S., de Torres Zabala, M., Beggs, K., Smith, C., Holdsworth, M. and Bevan, M. (1994) Separate cis sequences and trans factors direct metabolic and developmental regulation of a potato tuber storage protein gene. Plant J. 5, 815–826.
12. Harwood, J.L. (2005) Fatty acid biosynthesis. In Plant Lipids: Biology, Utilization and Manipulation (Murphy, D.J., ed.), pp. 27–66. Oxford: Blackwell Publishing.
13. Hoefgen, R. and Willmitzer, L. (1990) Biochemical and genetic-analysis of different patatin isoforms expressed in various organs of potato (Solanum tuberosum). Plant Sci. 66, 221–230.
14. Hofvander, P., Ischebeck, T., Turesson, H., Kushwaha, S.K., Feussner, I., Carlsson, A.S. and Andersson, M. (2016) Potato tuber expression of Arabidopsis WRINKLED1 increase triacylglycerol and membrane lipids while affecting central carbohydrate metabolism. Plant Biotechnol. J. doi: 10.1111/pbi.12550.
15. Horn, P.J., James, C.N., Gidda, S.K., Kilaru, A., Dyer, J.M., Mullen, R.T., Ohlrogge, J.B. et al. (2013) Identification of a new class of lipid droplet-associated proteins in plants. Plant Physiol. 162, 1926–1936.
16. Hsieh, K. and Huang, A.H. (2004) Endoplasmic reticulum, oleosins, and oils in seeds and tapetum cells. Plant Physiol. 136, 3427–3434.
17. Jako, C., Kumar, A., Wei, Y., Zou, J., Barton, D.L., Giblin, E.M., Covello, P.S. et al. (2001) Seed-specific over-expression of an Arabidopsis cDNA encoding a diacylglycerol acyltransferase enhances seed oil content and seed weight. Plant Physiol. 126, 861–874.
18. Jobling, S.A., Westcott, R.J., Tayal, A., Jeffcoat, R. and Schwall, G.P. (2002) Production of a freeze-thaw-stable potato starch by antisense inhibition of three starch synthase genes. Nat. Biotechnol. 20, 295–299.
19. Kilaru, A., Cao, X., Dabbs, P.B., Sung, H.-J., Rahman, M.M., Thrower, N., Zynda, G. et al. (2015) Oil biosynthesis in a basal angiosperm: transcriptome analysis of Persea Americana mesocarp. BMC Plant Biol. 15, 1–19.
20. Klaus, D., Ohlrogge, J.B., Neuhaus, H.E. and Dormann, P. (2004) Increased fatty acid production in potato by engineering of acetyl-CoA carboxylase. Planta, 219, 389–396.
21. Krahmer, N., Guo, Y., Wilfling, F., Hilger, M., Lingrell, S., Heger, K., Newman, H.W. et al. (2011) Phosphatidylcholine synthesis for lipid droplet expansion is mediated by localized activation of CTP:phosphocholine cytidylyltransferase. Cell Metab. 14, 504–515.
22. Linssen, J.P.H., Cozijnsen, J.L. and Pilnik, W. (1989) Chufa (Cyperus esculentus): a new source of dietary fibre. J. Sci. Food Agric. 49, 291–296.
23. Liu, J., Hua, W., Zhan, G., Wei, F., Wang, X., Liu, G. and Wang, H. (2010) Increasing seed mass and oil content in transgenic Arabidopsis by the overexpression of WRI1-like gene from Brassica napus. Plant Physiol. Biochem. 48, 9–15.
24. −ΔΔCt) Method. Methods, 25, 402–408.
25. Lung, S.C. and Weselake, R.J. (2006) Diacylglycerol acyltransferase: a key mediator of plant triacylglycerol synthesis. Lipids 41, 1073–1088.
26. Ma, W., Kong, Q., Arondel, V., Kilaru, A., Bates, P.D., Thrower, N.A., Benning, C. et al. (2013) WRINKLED1, A ubiquitous regulator in oil accumulating tissues from Arabidopsis embryos to oil palm mesocarp. PLoS ONE, 8, e68887.
27. Madoka, Y., Tomizawa, K.-I., Mizoi, J., Nishida, I., Nagano, Y. and Sasaki, Y. (2002) Chloroplast transformation with modified accD operon increases Acetyl-CoA Carboxylase and causes extension of leaf longevity and increase in seed yield in tobacco. Plant Cell Physiol. 43, 1518–1525.
28. Maeo, K., Tokuda, T., Ayame, A., Mitsui, N., Kawai, T., Tsukagoshi, H., Ishiguro, S. et al. (2009) An AP2-type transcription factor, WRINKLED1, of Arabidopsis thaliana binds to the AW-box sequence conserved among proximal upstream regions of genes involved in fatty acid synthesis. Plant J. 60, 476–487.
29. Martin, S. and Parton, R.G. (2006) Lipid droplets: a unified view of a dynamic organelle. Nat. Rev. Mol. Cell Biol. 7, 373–378.
30. Nicot, N., Hausman, J.F., Hoffmann, L. and Evers, D. (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J. Exp. Bot. 56, 2907–2914.
31. Regina, A., Kosar-Hashemi, B., Ling, S., Li, Z.Y., Rahman, S. and Morell, M. (2010) Control of starch branching in barley defined through differential RNAi suppression of starch branching enzyme IIa and IIb. J. Exp. Bot. 61, 1469–1482.
32. Rocha-Sosa, M., Sonnewald, U., Frommer, W., Stratmann, M., Schell, J. and Willmitzer, L. (1989) Both developmental and metabolic signals activate the promoter of a class I patatin gene. EMBO J. 8, 23–29.
33. Rogalski, M. and Carrer, H. (2011) Engineering plastid fatty acid biosynthesis to improve food quality and biofuel production in higher plants. Plant Biotechnol. J. 9, 554–564.
34. van Rooijen, G.J. and Moloney, M.M. (1995) Structural requirements of oleosin domains for subcellular targeting to the oil body. Plant Physiol. 109, 1353–1361.
35. Ruuska, S.A., Girke, T., Benning, C. and Ohlrogge, J.B. (2002) Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell, 14, 1191–1206.
36. Santos Mendoza, M., Dubreucq, B., Miquel, M., Caboche, M. and Lepiniec, L. (2005) LEAFY COTYLEDON 2 activation is sufficient to trigger the accumulation of oil and seed specific mRNAs in Arabidopsis leaves. FEBS Lett. 579, 4666–4670.
37. 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.
38. Shaik, S.S., Obata, T., Hebelstrup, K.H., Schwahn, K., Fernie, A.R., Mateiu, R.V. and Blennow, A. (2016) Starch granule re-structuring by starch branching enzyme and glucan water dikinase modulation affects caryopsis physiology and metabolism. PLoS ONE, 11, e0149613.
39. Shen, B., Allen, W.B., Zheng, P., Li, C., Glassman, K., Ranch, J., Nubel, D. et al. (2010) Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol. 153, 980–987.
40. Siloto, R.M., Findlay, K., Lopez-Villalobos, A., Yeung, E.C., Nykiforuk, C.L. and Moloney, M.M. (2006) The accumulation of oleosins determines the size of seed oil bodies in Arabidopsis. Plant Cell, 18, 1961–1974.
41. Slocombe, S.P., Cornah, J., Pinfield-Wells, H., Soady, K., Zhang, Q., Gilday, A., Dyer, J.M. et al. (2009) Oil accumulation in leaves directed by modification of fatty acid breakdown and lipid synthesis pathways. Plant Biotechnol. J. 7, 694–703.
42. Spurr, A.R. (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26, 31–43.
43. Thiam, A.R., Antonny, B., Wang, J., Delacotte, J., Wilfling, F., Walther, T.C., Beck, R. et al. (2013) COPI buds 60-nm lipid droplets from reconstituted water-phospholipid-triacylglyceride interfaces, suggesting a tension clamp function. Proc. Natl Acad. Sci. USA, 110, 13244–13249.
44. Ting, J.T., Lee, K., Ratnayake, C., Platt, K.A., Balsamo, R.A. and Huang, A.H. (1996) Oleosin genes in maize kernels having diverse oil contents are constitutively expressed independent of oil contents. Size and shape of intracellular oil bodies are determined by the oleosins/oils ratio. Planta, 199, 158–165.
45. To, A., Joubès, J., Barthole, G., Lécureuil, A., Scagnelli, A., Jasinski, S., Lepiniec, L. et al. (2012) WRINKLED transcription factors orchestrate tissue-specific regulation of fatty acid biosynthesis in Arabidopsis. Plant Cell, 24, 5007–5023.
46. Turesson, H., Marttila, S., Gustavsson, K.-E., Hofvander, P., Olsson, M.E., Bülow, L., Stymne, S. et al. (2010) Characterization of oil and starch accumulation in tubers of Cyperus esculentus var. sativus (Cyperaceae): a novel model system to study oil reserves in nonseed tissues. Am. J. Bot. 97, 1884–1893.
47. Vanhercke, T., El Tahchy, A., Shrestha, P., Zhou, X.R., Singh, S.P. and Petrie, J.R. (2013) Synergistic effect of WRI1 and DGAT1 coexpression on triacylglycerol biosynthesis in plants. FEBS Lett. 587, 364–369.
48. Vanhercke, T., El Tahchy, A., Liu, Q., Zhou, X.-R., Shrestha, P., Divi, U.K., Ral, J.-P. et al. (2014) Metabolic engineering of biomass for high energy density: oilseed-like triacylglycerol yields from plant leaves. Plant Biotechnol. J. 12, 231–239.
49. Vigeolas, H., Waldeck, P., Zank, T. and Geigenberger, P. (2007) Increasing seed oil content in oil-seed rape (Brassica napus L.) by over-expression of a yeast glycerol-3-phosphate dehydrogenase under the control of a seed-specific promoter. Plant Biotechnol. J. 5, 431–441.
50. Weselake, R.J., Taylor, D.C., Rahman, M.H., Shah, S., Laroche, A., McVetty, P.B. and Harwood, J.L. (2009) Increasing the flow of carbon into seed oil. Biotechnol. Adv. 27, 866–878.
51. Winichayakul, S., Scott, R.W., Roldan, M., Hatier, J.-H.B., Livingston, S., Cookson, R., Curran, A.C. et al. (2013) In vivo packaging of triacylglycerols enhances Arabidopsis leaf biomass and energy density. Plant Physiol. 162, 626–639.
52. Wischmann, B., Ahmt, T., Bandsholm, O., Blennow, A., Young, N., Jeppesen, L. and Thomsen, L. (2007) Testing properties of potato starch from different scales of isolations -A ring test. J. Food Eng. 79, 970–978.
53. Yatsu, L.Y. and Jacks, T.J. (1972) Spherosome membranes: half unit-membranes. Plant Physiol. 49, 937–943.
54. Yemm, E.W. and Willis, A.J. (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem. J. 57, 508–514.
55. Zale, J., Jung, J.H., Kim, J.Y., Pathak, B., Karan, R., Liu, H., Chen, X. et al. (2016) Metabolic engineering of sugarcane to accumulate energy-dense triacylglycerols in vegetative biomass. Plant Biotechnol. J. 14, 661–669.
56. Zheng, P., Allen, W.B., Roesler, K., Williams, M.E., Zhang, S., Li, J., Glassman, K. et al. (2008) A phenylalanine in DGAT is a key determinant of oil content and composition in maize. Nat. Genet. 40, 367–372.
57. Zou, J., Wei, Y., Jako, C., Kumar, A., Selvaraj, G. and Taylor, D.C. (1999) The Arabidopsis thaliana tag1 mutant has a mutation in a diacylglycerol acyltransferase gene. Plant J. 19, 645–653.