FUSCA3 activates triacylglycerol accumulation in Arabidopsis seedlings and tobacco BY2 cells

Plant Journal

Volumn 88, Issue 1, 2016, Pages 95-107

  Zhang, Meng ^a,b   Cao, Xia ^b,c   Jia, Qingli ^a   Ohlrogge, John ^b  

^a NORTHWEST A F UNIVERSITY   (China)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c BAYER CROPSCIENCE   (United States)

Author keywords

arabidopsis; FUSCA3; microarray; tobacco; triacylglycerol; vegetative tissue

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; FATTY ACIDS; FOOD STORAGE; GLYCEROL; HISTOLOGY; MICROARRAYS; OILS AND FATS; PLANTS (BOTANY); SUGAR (SUCROSE); TISSUE; TOBACCO; TRANSCRIPTION;

ARABIDOPSIS; ARABIDOPSIS SEEDLINGS; DIACYLGLYCEROL ACYLTRANSFERASES; FATTY ACID BIOSYNTHESIS; FUSCA3; TOBACCO BY-2 CELLS; TRIACYLGLYCEROLS; VEGETATIVE TISSUE;

SEED;

FUSCA3 PROTEIN, ARABIDOPSIS; TRANSCRIPTION FACTOR; TRIACYLGLYCEROL;

ARABIDOPSIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SEEDLING; TOBACCO; TRANSGENIC PLANT;

ARABIDOPSIS; GENE EXPRESSION REGULATION, PLANT; PLANTS, GENETICALLY MODIFIED; SEEDLINGS; TOBACCO; TRANSCRIPTION FACTORS; TRIGLYCERIDES;

EID: 84983483262     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13233     Document Type: Article

References (60)

1. Andrianov, V., Borisjuk, N., Pogrebnyak, N. 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. 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.
3. Bates, P.D., Stymne, S. and Ohlrogge, J. (2013) Biochemical pathways in seed oil synthesis. Curr. Opin. Plant Biol. 16, 358–364.
4. 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.
5. Beaudoin, F., Sayanova, O., Haslam, R.P., Bancroft, I. and Napier, J.A. (2014) Oleaginous crops as integrated production platforms for food, feed, fuel and renewable industrial feedstock – manipulation of plant lipid composition via metabolic engineering and new opportunities from association genetics for crop improvement and valorisation of co-products. OCL, 21, D606.
6. Beisson, F., Koo, A.J., Ruuska, S. et al. (2003) Arabidopsis genes involved in acyl lipid metabolism. A 2003 census of the candidates, a study of the distribution of expressed sequence tags in organs, and a web-based database. Plant Physiol. 132, 681–697.
7. 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.
8. Braybrook, S.A. and Harada, J.J. (2008) LECs go crazy in embryo development. Trends Plant Sci. 13, 624–630.
9. Brocard-Gifford, I.M., Lynch, T.J. and Finkelstein, R.R. (2003) Regulatory networks in seeds integrating developmental, abscisic acid, sugar, and light signaling. Plant Physiol. 131, 78–92.
10. Brundrett, M.C., Kendrick, B. and Peterson, C.A. (1991) Efficient lipid staining in plant material with Sudan Red 7B or fluorol [correction of fluoral] yellow 088 in polyethylene glycol-glycerol. Biotech. Histochem. 66, 111–116.
11. Casson, S.A. and Lindsey, K. (2006) The turnip mutant of Arabidopsis reveals that LEAFY COTYLEDON1 expression mediates the effects of auxin and sugars to promote embryonic cell identity. Plant Physiol. 142, 526–541.
12. 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.
13. Chen, M.X., Xuan, L.J., Wang, Z., Zhou, L.H., Li, Z.L., Du, X., Ali, E., Zhang, G.P. and Jiang, L.X. (2014) TRANSPARENT TESTA8 inhibits seed fatty acid accumulation by targeting several seed development regulators in Arabidopsis. Plant Physiol. 165, 905–916.
14. Chen, M., Zhang, B., Li, C., Kulaveerasingam, H., Chew, F.T. and Yu, H. (2015) TRANSPARENT TESTA GLABRA 1 regulates the accumulation of seed storage reserves in Arabidopsis. Plant Physiol. 169, 391–402.
15. Curaba, J., Moritz, T., Blervaque, R., Parcy, F., Raz, V., Herzog, M. and Vachon, G. (2004) AtGA3ox2, a key gene responsible for bioactive gibberellin biosynthesis, is regulated during embryogenesis by LEAFY COTYLEDON2 and FUSCA3 in Arabidopsis. Plant Physiol. 136, 3660–3669.
16. Dahlqvist, A., Stahl, U., Lenman, M., Banas, A., Lee, M., Sandager, L., Ronne, H. and Stymne, S. (2000) Phospholipid:diacylglycerol acyltransferase: an enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants. Proc. Natl Acad. Sci. USA, 97, 6487–6492.
17. Durrett, T.P., Benning, C. and Ohlrogge, J. (2008) Plant triacylglycerols as feedstocks for the production of biofuels. Plant J. 54, 593–607.
18. Fan, J., Yan, C., Zhang, X. and Xu, C. (2013) Dual role for phospholipid:diacylglycerol acyltransferase: enhancing fatty acid synthesis and diverting fatty acids from membrane lipids to triacylglycerol in Arabidopsis leaves. Plant Cell, 25, 3506–3518.
19. 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.
20. Gazzarrini, S., Tsuchiya, Y., Lumba, S., Okamoto, M. and McCourt, P. (2004) The transcription factorFUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid. Dev. Cell. 7, 373–385.
21. Hara, A. and Radin, N.S. (1978) Lipid extraction of tissues with a low-toxicity solvent. Anal. Biochem. 90, 420–426.
22. Jako, C., Kumar, A., Wei, Y., Zou, J., Barton, D.L., Giblin, E.M., Covello, P.S. and Taylor, D.C. (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.
23. Kagaya, Y., Toyoshima, R., Okuda, R., Usui, H., Yamamoto, A. and Hattori, T. (2005a) LEAFY COTYLEDON1 controls seed storage protein genes through its regulation of FUSCA3 and ABSCISIC ACID INSENSITIVE3. Plant Cell Physiol. 46, 399–406.
24. Keith, K., Kraml, M., Dengler, N.G. and McCourt, P. (1994) fusca3: a heterochronic mutation affecting late embryo development in Arabidopsis. Plant Cell, 6, 589–600.
25. Li-Beisson, Y.E.A. (2010) Acyl-lipid metabolism Online. 8, e0133. doi: 10.1199/tab.0133.
26. Lu, C. and Hills, M.J. (2002) Arabidopsis mutants deficient in diacylglycerol acyltransferase display increased sensitivity to abscisic acid, sugars, and osmotic stress during germination and seedling development. Plant Physiol. 129, 1352–1358.
27. Masaki, T., Mitsui, N., Tsukagoshi, H., Nishii, T., Morikami, A. and Nakamura, K. (2005) ACTIVATOR of Spomin:LUC1/WRINKLED1 of Arabidopsis thaliana transactivates sugar-inducible promoters. Plant Cell Physiol. 46, 547–556.
28. Meinke, D.W., Franzmann, L.H., Nickle, T.C. and Yeung, E.C. (1994) Leafy cotyledon mutants of Arabidopsis. Plant Cell, 6, 1049–1064.
29. Mu, J., Tan, H., Zheng, Q. et al. (2008) LEAFY COTYLEDON1 is a key regulator of fatty acid biosynthesis in Arabidopsis. Plant Physiol. 148, 1042–1054.
30. Nagata, T., Nemoto, Y. and Hasezawa, S. (1992) Tobacco BY-2 cell line as the ‘HeLa’ cell in the cell biology of higher plants. Int. Rev. Cytol. 132, 1–30.
31. Nagato, N.Y. and Hazezawa, S. (1992) Tobacco BY2 cell line as the ‘HeLa’ cell in the cell biology of higher plants. Int. Rev. Cytol. 132, 1–30.
32. Ogas, J., Cheng, J.C., Sung, Z.R. and Somerville, C. (1997) Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. Science, 277, 91–94.
33. Ohlrogge, J., Allen, D., Berguson, B., Dellapenna, D., Shachar-Hill, Y. and Stymne, S. (2009) Energy. Driving on biomass. Science, 324, 1019–1020.
34. Parcy, F., Valon, C., Kohara, A., Misera, S. and Giraudat, J. (1997) The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development. Plant Cell, 9, 1265–1277.
35. Reidt, W., Wohlfarth, T., Ellerstrom, M., Czihal, A., Tewes, A., Ezcurra, I., Rask, L. and Baumlein, H. (2000) Gene regulation during late embryogenesis: the RY motif of maturation-specific gene promoters is a direct target of the FUS3 gene product. Plant J. 21, 401–408.
36. Reina-Pinto, J.J., Voisin, D., Kurdyukov, S. et al. (2009) Misexpression of FATTY ACID ELONGATION1 in the Arabidopsis epidermis induces cell death and suggests a critical role for phospholipase A2 in this process. Plant Cell, 21, 1252–1272.
37. Roscoe, T.T., Guilleminot, J., Bessoule, J.J., Berger, F. and Devic, M. (2015) Complementation of seed maturation phenotypes by ectopic expression of ABSCISIC ACID INSENSITIVE3, FUSCA3 and LEAFY COTYLEDON2 in Arabidopsis. Plant Cell Physiol. 56, 1215–1228.
38. Sanjaya, Durrett, T.P., Weise, S.E. and Benning, C. (2011) Increasing the energy density of vegetative tissues by diverting carbon from starch to oil biosynthesis in transgenic Arabidopsis. Plant Biotechnol. J. 9, 874–883.
39. 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.
40. Shaul, O., Mironov, V., Burssens, S., Van Montagu, M. and Inze, D. (1996) Two Arabidopsis cyclin promoters mediate distinctive transcriptional oscillation in synchronized tobacco BY-2 cells. Proc. Natl Acad. Sci. USA, 93, 4868–4872.
41. Shen, B., Allen, W.B., Zheng, P., Li, C., Glassman, K., Ranch, J., Nubel, D. and Tarczynski, M.C. (2010) Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol., 153, 980–987.
42. Stone, S.L., Braybrook, S.A., Paula, S.L., Kwong, L.W., Meuser, J., Pelletier, J., Hsieh, T.F., Fischer, R.L., Goldberg, R.B. and Harada, J.J. (2008) Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: implications for somatic embryogenesis. Proc. Natl Acad. Sci. USA, 105, 3151–3156.
43. Tan, H., Yang, X., Zhang, F. et al. (2011) Enhanced seed oil production in canola by conditional expression of Brassica napus LEAFY COTYLEDON1 and LEC1-LIKE in developing seeds. Plant Physiol. 156, 1577–1588.
44. Taylor, D.C., Zhang, Y., Kumar, A. et al. (2009) Molecular modification of triacylglycerol accumulation by over-expression of DGAT1 to produce canola with increased seed oil content under field conditions. Botany, 87, 533–543.
45. Tiedemann, J., Rutten, T., Monke, G. et al. (2008) Dissection of a complex seed phenotype: novel insights of FUSCA3 regulated developmental processes. Dev. Biol. 317, 1–12.
46. To, A., Joubes, J., Barthole, G., Lecureuil, A., Scagnelli, A., Jasinski, S., Lepiniec, L. and Baud, S. (2012) WRINKLED transcription factors orchestrate tissue-specific regulation of fatty acid biosynthesis in Arabidopsis. Plant Cell, 24, 5007–5023.
47. Tsukagoshi, H., Morikami, A. and Nakamura, K. (2007) Two B3 domain transcriptional repressors prevent sugar-inducible expression of seed maturation genes in Arabidopsis seedlings. Proc. Natl Acad. Sci. USA, 104, 2543–2547.
48. Vanhercke, T., Wood, C.C., Stymne, S., Singh, S.P. and Green, A.G. (2013) Metabolic engineering of plant oils and waxes for use as industrial feedstocks. Plant Biotechnol. J. 11, 197–210.
49. Vanhercke, T., El Tahchy, A., Liu, Q. et al. (2014) Metabolic engineering of biomass for high energy density: oilseed-like triacylglycerol yields from plant leaves. Plant Biotechnol. J. 12, 231–239.
50. Vicient, C.M., Bies-Etheve, N. and Delseny, M. (2000) Changes in gene expression in the leafy cotyledon1 (lec1) and fusca3 (fus3) mutants of Arabidopsis thaliana L. J. Exp. Bot. 51, 995–1003.
51. Wang, F. and Perry, S.E. (2013) Identification of direct targets of FUSCA3, a key regulator of Arabidopsis seed development. Plant Physiol. 161, 1251–1264.
52. Wang, H., Guo, J., Lambert, K.N. and Lin, Y. (2007) Developmental control of Arabidopsis seed oil biosynthesis. Planta, 226, 773–783.
53. Wang, Z., Chen, M.X., Chen, T.L., Xuan, L.J., Li, Z.L., Du, X., Zhou, L.H., Zhang, G.P. and Jiang, L.X. (2014) TRANSPARENT TESTA2 regulates embryonic fatty acid biosynthesis by targeting FUSCA3 during the early developmental stage of Arabidopsis seeds. Plant J. 77, 757–769.
54. 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.
55. Xu, C. and Shanklin, J. (2016) Triacylglycerol metabolism, function, and accumulation in plant vegetative tissues. Annu. Rev. Plant Biol. 67, 179–206.
56. Yamamoto, A., Kagaya, Y., Usui, H., Hobo, T., Takeda, S. and Hattori, T. (2010) Diverse roles and mechanisms of gene regulation by the Arabidopsis seed maturation master regulator FUS3 revealed by microarray analysis. Plant Cell Physiol. 51, 2031–2046.
57. Zale, J., Jung, J.H., Kim, J.Y. et al. (2016) Metabolic engineering of sugarcane to accumulate energy-dense triacylglycerols in vegetative biomass. Plant Biotechnol. J. 14, 661–669.
58. Zhang, M., Fan, J., Taylor, D.C. and Ohlrogge, J.B. (2009) DGAT1 and PDAT1 acyltransferases have overlapping functions in Arabidopsis triacylglycerol biosynthesis and are essential for normal pollen and seed development. Plant Cell, 21, 3885–3901.
59. 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.
60. Zuo, J., Niu, Q.W. and Chua, N.H. (2000) Technical advance: an estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J. 24, 265–273.