Soybean oil biosynthesis: role of diacylglycerol acyltransferases

Banilas G, Karampelias M, Makariti I, Kourti A, Hatzopoulos P (2011) The olive DGAT2 gene is developmentally regulated and shares overlapping but distinct expression patterns with DGAT1. J Exp Bot 62:521–532. doi:10.1093/jxb/erq286 Bewley J, Black M (1994) Seeds: physiology of development and germination. Plenum Press, New York Bouvier-Nave P, Benvenise P, Oelkers P, Sturley S, Schaller H (2000) Expression in yeast and tobacco of plant cDNAs encoding acyl CoA:diacylglycerol acyltransferase. Eur J Biochem 267:85–96 Burgal J, Shockey J, Lu CF, Dyer J, Larson T, Graham I, Browse J (2008) Metabolic engineering of hydroxy fatty acid production in plants: RcDGAT2 drives dramatic increases in ricinoleate levels in seed oil. Plant Biotechnol J 6:819–831. doi:10.1111/j.1467-7652.2008.00361.x Carmer SG, Swanson MR (1973) Evaluation of 10 pairwise multiple comparison procedures by Monte-Carlo methods. J Am Stat Assoc 68:66–74 Cases S, Smith SJ, Zheng Y, Myers HM, Lear SR, Sande E, Novak S, Collins C, Welch CB, Lusis AJ, Erickson SK, Farese RV Jr (1998) Identification of a gene encoding an acyl CoA:diacylglycerol acyltransferase, a key enzyme in triacylglycerol synthesis. P Natl Acad Sci U S A 95:13018–13023 Chaven C, Hymowitz T, Newell C (1982) Chromosome number, oil and fatty acid content of species in the genus Glycine subgenus Glycine. J Am Oil Chem Soc 59:23–25. doi:10.1007/bf02670062 Dahlqvist A, Stahl U, Lenman M, Banas A, Lee M, Sandager L, Ronne H, 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 U S A 97:6487–6492 Durrett TP, McClosky DD, Tumaney AW, Elzinga DA, Ohlrogge J, Pollard M (2010) A distinct DGAT with sn-3 acetyltransferase activity that synthesizes unusual, reduced-viscosity oils in Euonymus and transgenic seeds. P Natl Acad Sci U S A 107:9464–9469. doi:10.1073/pnas.1001707107 Hatanaka T, Shimizu R, Hildebrand D (2004) Expression of a Stokesia laevis epoxygenase gene. Phytochemistry 65:2189–2196 He X, Chen GQ, Lin JT, McKeon TA (2004) Regulation of diacylglycerol acyltransferase in developing seeds of castor. Lipids 39:865–871 Hofmann K (2000) A superfamily of membrane-bound O-acyltransferases with implications for Wnt signaling. Trends Biochem Sci 25:111–112. doi:10.1016/s0968-0004(99)01539-x Huang AHC (1992) Oil bodies and oleosins in seeds. Annu Rev Plant Physiol Plant Mol Biol 43:177–200 Ichihara K, Takahashi T, Fujii S (1988) Diacylglycerol acyltransferase in maturing safflower seeds: its influences on the fatty acid composition of triacylglycerol and on the rate of triacylglycerol synthesis. Biochim Biophys Acta 958:125–129 Kalscheuer R, Steinbuchel A (2003) A novel bifunctional wax ester synthase/acyl-CoA:diacylglycerol acyltransferase mediates wax ester and triacylglycerol biosynthesis in Acinetobacter calcoaceticus ADP1. J Biol Chem 278:8075–8082 Katavic V, Reed DW, Taylor DC, Giblin EM, Barton DL, Zou J, Mackenzie SL, Covello PS, Kunst L (1995) Alteration of seed fatty acid composition by an ethyl methanesulfonate-induced mutation in Arabidopsis thaliana affecting diacylglycerol acyltransferase activity. Plant Physiol 108:399–409 King A, Nam JW, Han JX, Hilliard J, Jaworski JG (2007) Cuticular wax biosynthesis in petunia petals: cloning and characterization of an alcohol-acyltransferase that synthesizes wax-esters. Planta 226:381–394. doi:10.1007/s00425-007-0489-z Kroon JTM, Wei W, Simon WJ, Slabas AR (2006) Identification and functional expression of a type 2 acyl-CoA:diacylglycerol acyltransferase (DGAT2) in developing castor bean seeds which has high homology to the major triglyceride biosynthetic enzyme of fungi and animals. Phytochemistry 67:2541–2549 Kwanyuen P, Wilson RF (1986) Isolation and purification of diacylglycerol acyltransferase from germinating soybean cotyledons. Biochim Biophys Acta 877:238–245 Kwanyuen P, Wilson RF (1990) Subunit and amino acid composition of diacylglycerol acyltransferase from germinating soybean cotyledons. Biochim Biophys Acta 1039:67–72 Lardizabal K, Effertz R, Levering C, Mai J, Pedroso MC, Jury T, Aasen E, Gruys K, Bennett K (2008) Expression of Umbelopsis ramanniana DGAT2A in seed increases oil in soybean. Plant Physiol 148:89–96. doi:10.1104/pp.108.123042 Li F, Wu X, Lam P, Bird D, Zheng H, Samuels L, Jetter R, Kunst L (2008) Identification of the wax ester synthase/acyl-coenzyme a:diacylglycerol acyltransferase WSD1 required for stem wax ester biosynthesis in Arabidopsis. Plant Physiol 148:97–107. doi:10.1104/pp.108.123471 Li R, Yu K, Hatanaka T, Hildebrand DF (2010a) Vernonia DGATs increase accumulation of epoxy fatty acids in oil. Plant Biotechnol J 8:184–195 Li R, Yu K, Hildebrand D (2010b) DGAT1, DGAT2 and PDAT expression in seeds and other tissues of epoxy and hydroxy fatty acid accumulating plants. Lipids 45:145–157 Lu C, Xin Z, Ren Z, Miquel M, Browse J (2009) An enzyme regulating triacylglycerol composition is encoded by the ROD1 gene of Arabidopsis. Proc Natl Acad Sci 106:18837–18842. doi:10.1073/pnas.0908848106 Mason JM, Arndt KM (2004) Coiled coil domains: stability, specificity, and biological implications. ChemBioChem 5:170–176. doi:10.1002/cbic.200300781 McCartney AW, Dyer JM, Dhanoa PK, Kim PK, Andrews DW, McNew JA, Mullen RT (2004) Membrane-bound fatty acid desaturases are inserted co-translationally into the ER and contain different ER retrieval motifs at their carboxy termini. Plant J 37:156–173. doi:10.1111/j.1365-313X.2004.01949.x McFie PJ, Stone SL, Banman SL, Stone SJ (2010) Topological orientation of acyl-coa:diacylglycerol acyltransferase-1 (DGAT1) and identification of a putative active site histidine and the role of the N terminus in dimer/tetramer formation. J Biol Chem 285:37377–37387. doi:10.1074/jbc.M110.163691 Oelkers P, Behar A, Cromley D, Billheimer J, Sturley S (1998) Characterization of two human genes encoding acyl coenzyme A: cholesterol acyltransferase-related enzymes. J Biol Chem 273:26765–26771 Oelkers P, Tinkelenberg A, Erdeniz N, Cromley D, Billheimer JT, Sturley SL (2000) A lecithin cholesterol acyltransferase-like gene mediates diacylglycerol esterification in yeast. J Biol Chem 275:15609–15612. doi:10.1074/jbc.C000144200 Oelkers P, Cromley D, Padamsee M, Billheimer JT, Sturley SL (2002) The DGA1 gene determines a second triglyceride synthetic pathway in yeast. J Biol Chem 277:8877–8881 Ohlrogge JB, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970 Perry H, Harwood J (1993) Changes in the lipid content of developing seeds of Brassica napus. Phytochemistry 32:1411–1415 Rani SH, Krishna THA, Saha S, Negi AS, Rajasekharan R (2010) Defective in cuticular ridges (DCR) of Arabidopsis thaliana, a gene associated with surface cutin formation, encodes a soluble diacylglycerol acyltransferase. J Biol Chem 285:38337–38347. doi:10.1074/jbc.M110.133116 Routaboul J-M, Benning C, Bechtold N, Caboche M, Lepiniec L (1999) The TAG1 locus of Arabidopsis encodes for a diacylglycerol acyltransferase. Plant Physiol Biochem 37:831–840 Saha S, Enugutti B, Rajakumari S, Rajasekharan R (2006) Cytosolic triacylglycerol biosynthetic pathway in oilseeds. Molecular cloning and expression of peanut cytosolic diacylglycerol acyltransferase. Plant Physiol 141:1533–1543. doi:10.1104/pp.106.082198 Schmutz J, Cannon SB, Schlueter J, Ma JX, Mitros T, Nelson W, Hyten DL, Song QJ, Thelen JJ, Cheng JL, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu SQ, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du JC, Tian ZX, Zhu LC, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183. doi:10.1038/Nature08670 Settlage SB, Kwanyuen P, Wilson RF (1998) Relation between diacylglycerol acyltransferase activity and oil concentration in soybean. J Am Oil Chem Soc 75:775–781 Shockey JM, Gidda SK, Chapital DC, Kuan J-C, Dhanoa PK, Bland JM, Rothstein SJ, Mullen RT, Dyer JM (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. doi:10.1105/tpc.106.043695 Stoveken T, Kalscheuer R, Malkus U, Reichelt R, Steinbuchel A (2005) The wax ester synthase/acyl coenzyme A:diacylglycerol acyltransferase from Acinetobacter sp strain ADP1: characterization of a novel type of acyltransferase. J Bacteriol 187:1369–1376. doi:10.1128/Jb.187.4.1369-1376.2005 Taylor DC, Yan Z, Kumar A, Francis T, Giblin EM, Barton DL, Ferrie JR, Laroche A, Shah S, Weiming Z, Snyder CL, Hall L, Rakow G, Harwood JL, Weselake RJ (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 USDA (2012a) In: Service FA (ed) Oilseeds: world markets and trade, FOP 10-09. USDA, Washington, DC USDA (2012b) In: Service ER (ed) World agricultural supply and demand estimates, WASDE-477. USDA, Washington, DC van Heeckeren WJ, Sellers JW, Struhl K (1992) Role of the conserved leucines in the leucine zipper dimerization motif of yeast GCN4. Nucleic Acids Res 20:3721–3724. doi:10.1093/nar/20.14.3721 Wang Z, Triezenberg SJ, Thomashow MF, Stockinger EJ (2005) Multiple hydrophobic motifs in Arabidopsis CBF1 COOH-terminus provide functional redundancy in trans-activation. Plant Mol Biol 58:543–559 Wang H-W, Zhang J-S, Gai J-Y, Chen S-Y (2006) Cloning and comparative analysis of the gene encoding diacylglycerol acyltransferase from wild type and cultivated soybean. Theor Appl Genet 112:1086–1097 Yu K, McCracken C Jr, Li R, Hildebrand DF (2006) Diacylglycerol acyltransferase from Vernonia and Stokesia prefer substrates with vernolic acid. Lipids 41:557–566 Yu K, Li R, Hatanaka T, Hildebrand D (2008) Cloning and functional analysis of two type 1 diacylglycerol acyltransferases from Vernonia galamensis. Phytochemistry 69:1119–1127 Zhang M, Fan J, Taylor DC, Ohlrogge JB (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. doi:10.1105/tpc.109.071795 Zheng P, Allen WB, Roesler K, Williams ME, Zhang S, Li J, Glassman K, Ranch J, Nubel D, Solawetz W, Bhattramakki D, Llaca V, Deschamps S, Zhong G-Y, Tarczynski MC, Shen B (2008) A phenylalanine in DGAT is a key determinant of oil content and composition in maize. Nat Genet 40:367–372 Zou J, Wei Y, Taylor DC (1999) The Arabidopsis thaliana TAG1 mutant has a mutation in a diacylglycerol acyl transferase gene. Plant J 19:645–654