Arabidopsis SEIPIN proteins modulate triacylglycerol accumulation and influence lipid droplet proliferation

Plant Cell

Volumn 27, Issue 9, 2015, Pages 2616-2636

  Cai, Yingqi ^a   Goodman, Joel M ^b   Pyc, Michal ^c   Mullen, Robert T ^c   Dyer, John M ^d   Chapmana, Kent D ^a  

^a UNIVERSITY OF NORTH TEXAS   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF GUELPH   (Canada)

^d US ARID LAND AGRICULTURAL RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; BSCL2 PROTEIN, HUMAN; FAT DROPLET; FLD1 PROTEIN, S CEREVISIAE; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; MEMBRANE PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; TRIACYLGLYCEROL;

ARABIDOPSIS; CHEMISTRY; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PLANT LEAF; PROTEIN MOTIF; SACCHAROMYCES CEREVISIAE; TOBACCO; TRANSGENIC PLANT;

AMINO ACID MOTIFS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION, PLANT; GENETIC COMPLEMENTATION TEST; GTP-BINDING PROTEIN GAMMA SUBUNITS; LIPID DROPLETS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TOBACCO; TRIGLYCERIDES;

EID: 84943740201     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.15.00588     Document Type: Article

References (65)

1. Andrianov, V., Borisjuk, N., Pogrebnyak, N., Brinker, A., Dixon, J., Spitsin, S., Flynn, J., Matyszczuk, P., Andryszak, K., Laurelli, M., Golovkin, M., and Koprowski, H. (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. Atanassov, I.I., Atanassov, I.I., Etchells, J.P., and Turner, S.R. (2009). A simple, flexible and efficient PCR-fusion/Gateway cloning procedure for gene fusion, site-directed mutagenesis, short sequence insertion and domain deletions and swaps. Plant Methods 5: 14.
3. Bailey, T.L., Boden, M., Buske, F.A., Frith, M., Grant, C.E., Clementi, L., Ren, J., Li, W.W., and Noble, W.S. (2009). MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37: W202-W208.
4. Bartz, R., Li, W.H., Venables, B., Zehmer, J.K., Roth, M.R., Welti, R., Anderson, R.G., Liu, P., and Chapman, K.D. (2007). Lipidomics reveals that adiposomes store ether lipids and mediate phospholipid traffic. J. Lipid Res. 48: 837-847.
5. Baud, S., and Lepiniec, L. (2010). Physiological and developmental regulation of seed oil production. Prog. Lipid Res. 49: 235-249.
6. Bi, J., Wang, W., Liu, Z., Huang, X., Jiang, Q., Liu, G., Wang, Y., and Huang, X. (2014). Seipin promotes adipose tissue fat storage through the ER Ca²⁺-ATPase SERCA. Cell Metab. 19: 861-871.
7. Binns, D., Lee, S., Hilton, C.L., Jiang, Q.X., and Goodman, J.M. (2010). Seipin is a discrete homooligomer. Biochemistry 49: 10747-10755.
8. Brasaemle, D.L., and Wolins, N.E. (2012). Packaging of fat: an evolving model of lipid droplet assembly and expansion. J. Biol. Chem. 287: 2273-2279.
9. Carman, G.M. (2012). Thematic minireview series on the lipid droplet, a dynamic organelle of biomedical and commercial importance. J. Biol. Chem. 287: 2272.
10. Cartwright, B.R., and Goodman, J.M. (2012). Seipin: from human disease to molecular mechanism. J. Lipid Res. 53: 1042-1055.
11. Cartwright, B.R., Binns, D.D., Hilton, C.L., Han, S., Gao, Q., and Goodman, J.M. (2015). Seipin performs dissectible functions in promoting lipid droplet biogenesis and regulating droplet morphology. Mol. Biol. Cell 26: 726-739.
12. Chapman, K.D., Dyer, J.M., and Mullen, R.T. (2012). Biogenesis and functions of lipid droplets in plants: Thematic review series: lipid droplet synthesis and metabolism: from yeast to man. J. Lipid Res. 53: 215-226.
13. Chapman, K.D., Dyer, J.M., and Mullen, R.T. (2013). Commentary: why don’t plant leaves get fat? Plant Sci. 207: 128-134.
14. Chapman, K.D., Neogi, P.B., Hake, K.D., Stawska, A.A., Speed, T.R., Cotter, M.Q., Garrett, D.C., Kerby, T., Richardson, C.D., Ayre, B.G., Ghosh, S., and Kinney, A.J. (2008). Reduced oil accumulation in cottonseeds transformed with a Brassica nonfunctional allele of a Delta-12 Fatty Acid Desaturase (FAD2). Crop Sci. 48: 1470-1481.
15. Chapman, K.D., and Ohlrogge, J.B. (2012). Compartmentation of triacylglycerol accumulation in plants. J. Biol. Chem. 287: 2288-2294.
16. Chapman, K.D., and Trelease, R.N. (1991). Acquisition of membrane lipids by differentiating glyoxysomes: role of lipid bodies. J. Cell Biol. 115: 995-1007.
17. Clough, S.J., and Bent, A.F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
18. Cui, X., Wang, Y., Meng, L., Fei, W., Deng, J., Xu, G., Peng, X., Ju, S., Zhang, L., Liu, G., Zhao, L., and Yang, H. (2012). Overexpression of a short human seipin/BSCL2 isoform in mouse adipose tissue results in mild lipodystrophy. Am. J. Physiol. Endocrinol. Metab. 302: E705-E713.
19. Cui, X., Wang, Y., Tang, Y., Liu, Y., Zhao, L., Deng, J., Xu, G., Peng, X., Ju, S., Liu, G., and Yang, H. (2011). Seipin ablation in mice results in severe generalized lipodystrophy. Hum. Mol. Genet. 20: 3022-3030.
20. Curtis, M.D., and Grossniklaus, U. (2003). A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133: 462-469.
21. Dereeper, A., Audic, S., Claverie, J.M., and Blanc, G. (2010). BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol. Biol. 10: 8.
22. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J.F., Guindon, S., Lefort, V., Lescot, M., Claverie, J.M., and Gascuel, O. (2008). Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36: W465-W469.
23. Durrett, T.P., Benning, C., and Ohlrogge, J. (2008). Plant triacylglycerols as feedstocks for the production of biofuels. Plant J. 54: 593-607.
24. Farese, R.V., Jr., and Walther, T.C. (2009). Lipid droplets finally get a little R-E-S-P-E-C-T. Cell 139: 855-860.
25. Fei, W., Du, X., and Yang, H. (2011a). Seipin, adipogenesis and lipid droplets. Trends Endocrinol. Metab. 22: 204-210.
26. Fei, W., Li, H., Shui, G., Kapterian, T.S., Bielby, C., Du, X., Brown, A.J., Li, P., Wenk, M.R., Liu, P., and Yang, H. (2011b). Molecular characterization of seipin and its mutants: implications for seipin in triacylglycerol synthesis. J. Lipid Res. 52: 2136-2147.
27. Fei, W., Shui, G., Gaeta, B., Du, X., Kuerschner, L., Li, P., Brown, A.J., Wenk, M.R., Parton, R.G., and Yang, H. (2008). Fld1p, a functional homologue of human seipin, regulates the size of lipid droplets in yeast. J. Cell Biol. 180: 473-482.
28. Fei, W., et al. (2011c). A role for phosphatidic acid in the formation of “supersized” lipid droplets. PLoS Genet. 7: e1002201.
29. Gidda, S.K., et al. (2013). Lipid droplet-associated proteins (LDAPs) are involved in the compartmentalization of lipophilic compounds in plant cells. Plant Signal. Behav. 8: e27141.
30. Goodstein, D.M., Shu, S., Howson, R., Neupane, R., Hayes, R.D., Fazo, J., Mitros, T., Dirks, W., Hellsten, U., Putnam, N., and Rokhsar, D.S. (2012). Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40: D1178-D1186.
31. Herker, E., and Ott, M. (2012). Emerging role of lipid droplets in host/pathogen interactions. J. Biol. Chem. 287: 2280-2287.
32. Horn, P.J., James, C.N., Gidda, S.K., Kilaru, A., Dyer, J.M., Mullen, R.T., Ohlrogge, J.B., and Chapman, K.D. (2013). Identification of a new class of lipid droplet-associated proteins in plants. Plant Physiol. 162: 1926-1936.
33. Huang, A.H. (1996). Oleosins and oil bodies in seeds and other organs. Plant Physiol. 110: 1055-1061.
34. Jacquier, N., Choudhary, V., Mari, M., Toulmay, A., Reggiori, F., and Schneiter, R. (2011). Lipid droplets are functionally connected to the endoplasmic reticulum in Saccharomyces cerevisiae. J. Cell Sci. 124: 2424-2437.
35. Jacquier, N., Mishra, S., Choudhary, V., and Schneiter, R. (2013). Expression of oleosin and perilipins in yeast promotes formation of lipid droplets from the endoplasmic reticulum. J. Cell Sci. 126: 5198-5209.
36. James, C.N., Horn, P.J., Case, C.R., Gidda, S.K., Zhang, D., Mullen, R.T., Dyer, J.M., Anderson, R.G., and Chapman, K.D. (2010). Disruption of the Arabidopsis CGI-58 homologue produces Chanarin-Dorfman-like lipid droplet accumulation in plants. Proc. Natl. Acad. Sci. USA 107: 17833-17838.
37. Krahmer, N., Guo, Y., Wilfling, F., Hilger, M., Lingrell, S., Heger, K., Newman, H.W., Schmidt-Supprian, M., Vance, D.E., Mann, M., Farese, R.V., Jr., and Walther, T.C. (2011). Phosphatidylcholine synthesis for lipid droplet expansion is mediated by localized activation of CTP:phosphocholine cytidylyltransferase. Cell Metab. 14: 504-515.
38. Magré, J., et al.; BSCL Working Group (2001) Identification of the gene altered in Berardinelli-Seip congenital lipodystrophy on chromosome 11q13. Nat. Genet. 28: 365-370.
39. Miquel, M., Trigui, G., d’Andréa, S., Kelemen, Z., Baud, S., Berger, A., Deruyffelaere, C., Trubuil, A., Lepiniec, L., and Dubreucq, B. (2014). Specialization of oleosins in oil body dynamics during seed development in Arabidopsis seeds. Plant Physiol. 164: 1866-1878.
40. Murphy, D.J. (2012). The dynamic roles of intracellular lipid droplets: from archaea to mammals. Protoplasma 249: 541-585.
41. Park, S., Gidda, S.K., James, C.N., Horn, P.J., Khuu, N., Seay, D.C., Keereetaweep, J., Chapman, K.D., Mullen, R.T., and Dyer, J.M. (2013). The a/b hydrolase CGI-58 and peroxisomal transport protein PXA1 coregulate lipid homeostasis and signaling in Arabidopsis. Plant Cell 25: 1726-1739.
42. Petrie, J.R., Shrestha, P., Liu, Q., Mansour, M.P., Wood, C.C., Zhou, X.R., Nichols, P.D., Green, A.G., and Singh, S.P. (2010). Rapid expression of transgenes driven by seed-specific constructs in leaf tissue: DHA production. Plant Methods 6: 8.
43. Pol, A., Gross, S.P., and Parton, R.G. (2014). Review: biogenesis of the multifunctional lipid droplet: lipids, proteins, and sites. J. Cell Biol. 204: 635-646.
44. Rudolph, M., Schlereth, A., Körner, M., Feussner, K., Berndt, E., Melzer, M., Hornung, E., and Feussner, I. (2011). The lipoxygenase-dependent oxygenation of lipid body membranes is promoted by a patatin-type phospholipase in cucumber cotyledons. J. Exp. Bot. 62: 749-760.
45. 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.
46. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Schölkopf, B., Weigel, D., and Lohmann, J.U. (2005). A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37: 501-506.
47. Schmidt, M.A., and Herman, E.M. (2008). Suppression of soybean oleosin produces micro-oil bodies that aggregate into oil body/ER complexes. Mol. Plant 1: 910-924.
48. Schwab, R., Ossowski, S., Riester, M., Warthmann, N., and Weigel, D. (2006). Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18: 1121-1133.
49. Shockey, J.M., Gidda, S.K., Chapital, D.C., Kuan, J.C., Dhanoa, P.K., Bland, J.M., Rothstein, S.J., Mullen, R.T., and Dyer, J.M. (2006). Tung tree DGAT1 and DGAT2 have nonredundant functions in triacylglycerol biosynthesis and are localized to different subdomains of the endoplasmic reticulum. Plant Cell 18: 2294-2313.
50. Szymanski, J., Brotman, Y., Willmitzer, L., and Cuadros-Inostroza, Á. (2014). Linking gene expression and membrane lipid composition of Arabidopsis. Plant Cell 26: 915-928.
51. Szymanski, K.M., Binns, D., Bartz, R., Grishin, N.V., Li, W.P., Agarwal, A.K., Garg, A., Anderson, R.G., and Goodman, J.M. (2007). The lipodystrophy protein seipin is found at endoplasmic reticulum lipid droplet junctions and is important for droplet morphology. Proc. Natl. Acad. Sci. USA 104: 20890-20895.
52. Tian, Y., Bi, J., Shui, G., Liu, Z., Xiang, Y., Liu, Y., Wenk, M.R., Yang, H., and Huang, X. (2011). Tissue-autonomous function of Drosophila seipin in preventing ectopic lipid droplet formation. PLoS Genet. 7: e1001364.
53. Vanhercke, T., et al. (2014). Metabolic engineering of biomass for high energy density: oilseed-like triacylglycerol yields from plant leaves. Plant Biotechnol. J. 12: 231-239.
54. Voinnet, O., Rivas, S., Mestre, P., and Baulcombe, D. (2003). An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33: 949-956.
55. Wang, C.W., Miao, Y.H., and Chang, Y.S. (2014). Control of lipid droplet size in budding yeast requires the collaboration between Fld1 and Ldb16. J. Cell Sci. 127: 1214-1228.
56. White, T., Bursten, S., Federighi, D., Lewis, R.A., and Nudelman, E. (1998). High-resolution separation and quantification of neutral lipid and phospholipid species in mammalian cells and sera by multione-dimensional thin-layer chromatography. Anal. Biochem. 258: 109-117.
57. Wilfling, F., et al. (2013). Triacylglycerol synthesis enzymes mediate lipid droplet growth by relocalizing from the ER to lipid droplets. Dev. Cell 24: 384-399.
58. Wilfling, F., Haas, J.T., Walther, T.C., and Farese, R.V., Jr. (2014). Lipid droplet biogenesis. Curr. Opin. Cell Biol. 29: 39-45.
59. Winichayakul, S., Scott, R.W., Roldan, M., Hatier, J.H., Livingston, S., Cookson, R., Curran, A.C., and Roberts, N.J. (2013). In vivo packaging of triacylglycerols enhances Arabidopsis leaf biomass and energy density. Plant Physiol. 162: 626-639.
60. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V., and Provart, N.J. (2007). An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2: e718.
61. Wolinski, H., Kolb, D., Hermann, S., Koning, R.I., and Kohlwein, S.D. (2011). A role for seipin in lipid droplet dynamics and inheritance in yeast. J. Cell Sci. 124: 3894-3904.
62. Wright, R. (2000). Transmission electron microscopy of yeast. Microsc. Res. Tech. 51: 496-510.
63. Xu, N., Zhang, S.O., Cole, R.A., McKinney, S.A., Guo, F., Haas, J.T., Bobba, S., Farese, R.V., Jr., and Mak, H.Y. (2012). The FATP1-DGAT2 complex facilitates lipid droplet expansion at the ER-lipid droplet interface. J. Cell Biol. 198: 895-911.
64. Yang, H., Galea, A., Sytnyk, V., and Crossley, M. (2012). Controlling the size of lipid droplets: lipid and protein factors. Curr. Opin. Cell Biol. 24: 509-516.
65. Zehmer, J.K., Huang, Y., Peng, G., Pu, J., Anderson, R.G., and Liu, P. (2009). A role for lipid droplets in inter-membrane lipid traffic. Proteomics 9: 914-921