An improved variant of soybean type 1 diacylglycerol acyltransferase increases the oil content and decreases the soluble carbohydrate content of soybeans

Plant Physiology

Volumn 171, Issue 2, 2016, Pages 878-893

  Roesler, Keith ^a   Shen, Bo ^a   Bermudez, Ericka ^a,b   Li, Changjiang ^a,c   Hunt, Joanne ^a   Damude, Howard G ^a   Ripp, Kevin G ^a   Everard, John D ^a   Booth, John R ^a   Castaneda, Leandro ^a   Feng, Lizhi ^a   Meyer, Knut ^a  

^a DUPONT COMPANY   (United States)

^b DuPont Pioneer   (United States)

^c JEALOTT S HILL RESEARCH STATION   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; DIACYLGLYCEROL ACYLTRANSFERASE; OLEIC ACID; PLANT PROTEIN; VEGETABLE OIL;

ENZYMOLOGY; GENETICS; HAZELNUT; KINETICS; METABOLISM; PLANT SEED; SOYBEAN;

CARBOHYDRATES; CORYLUS; DIACYLGLYCEROL O-ACYLTRANSFERASE; KINETICS; OLEIC ACID; PLANT OILS; PLANT PROTEINS; SEEDS; SOYBEANS;

EID: 84973636661     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.00315     Document Type: Article

References (69)

1. Agelet LE, Armstrong PR, Romagosa Clariana I, Hurburgh CR (2012) Measurement of single soybean seed attributes by near-infrared technologies: a comparative study. J Agric Food Chem 60: 8314-8322
2. Bao X, Ohlrogge J (1999) Supply of fatty acid is one limiting factor in the accumulation of triacylglycerol in developing embryos. Plant Physiol 120: 1057-1062
3. Bates PD, Durrett TP, Ohlrogge JB, Pollard M (2009) Analysis of acyl fluxes through multiple pathways of triacylglycerol synthesis in developing soybean embryos. Plant Physiol 150: 55-72
4. Beachy RN, Chen ZL, Horsch RB, Rogers SG, Hoffmann NJ, Fraley RT (1985) Accumulation and assembly of soybean b-conglycinin in seeds of transformed petunia plants. EMBO J 4: 3047-3053
5. Brink K, Chui CF, Cressman RF, Garcia P, Henderson N, Hong B, Maxwell CA, Meyer K, Mickelson J, Stecca KL, et al (2014) Molecular characterization, compositional analysis, and germination evaluation of a high-oleic soybean generated by the suppression of FAD2-1 expression. Crop Sci 54: 2160-2174
6. Burgal J, Shockey J, Lu C, 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
7. Burton J, Brim C (1981) Recurrent selection in soybeans. III. Selection for increased percent oil in seeds. Crop Sci 21: 31-34
8. Cahoon EB, Carlson TJ, Ripp KG, Schweiger BJ, Cook GA, Hall SE, Kinney AJ (1999) Biosynthetic origin of conjugated double bonds: production of fatty acid components of high-value drying oils in transgenic soybean embryos. Proc Natl Acad Sci USA 96: 12935-12940
9. Cao YZ, Huang AH (1986) Diacylglycerol acyltransferase in maturing oil seeds of maize and other species. Plant Physiol 82: 813-820
10. Cao YZ, Huang AH (1987) Acyl coenzyme A preference of diacylglycerol acyltransferase from the maturing seeds of cuphea, maize, rapeseed, and canola. Plant Physiol 84: 762-765
11. Chen JE, Smith AG (2012) A look at diacylglycerol acyltransferases (DGATs) in algae. J Biotechnol 162: 28-39
12. Cheng D, Meegalla RL, He B, Cromley DA, Billheimer JT, Young PR (2001) Human acyl-CoA:diacylglycerol acyltransferase is a tetrameric protein. Biochem J 359: 707-714
13. Clemente TE, Cahoon EB (2009) Soybean oil: genetic approaches for modification of functionality and total content. Plant Physiol 151: 1030-1040
14. Doyle JJ, Schuler MA, Godette WD, Zenger V, Beachy RN, Slightom JL (1986) The glycosylated seed storage proteins of Glycine max and Phaseolus vulgaris: structural homologies of genes and proteins. J Biol Chem 261: 9228-9238
15. 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. Proc Natl Acad Sci USA 107: 9464-9469
16. Eskandari M, Cober ER, Rajcan I (2013) Genetic control of soybean seed oil. II. QTL and genes that increase oil concentration without decreasing protein or with increased seed yield. Theor Appl Genet 126: 1677-1687
17. Feng L, Burton J, Carter T, Pantalone V (2004) Recurrent half-sib selection with testcross evaluation for increased oil content in soybean. Crop Sci 44: 63-69
18. Furmanek T, Demski K, Banaś W, Haslam R, Napier J, Stymne S, Banaś A (2014) The utilization of the acyl-CoA and the involvement PDAT and DGAT in the biosynthesis of erucic acid-rich triacylglycerols in Crambe seed oil. Lipids 49: 327-333
19. Gietz RD, Schiestl RH (2007) Large-scale high-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2: 38-41
20. Gillingham LG, Harris-Janz S, Jones PJ (2011) Dietary monounsaturated fatty acids are protective against metabolic syndrome and cardiovascular disease risk factors. Lipids 46: 209-228
21. Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2009) ASReml User Guide Release 30. VSN International, Hemel Hempstead, UK
22. Greenspan P, Mayer EP, Fowler SD (1985) Nile red: a selective fluorescent stain for intracellular lipid droplets. J Cell Biol 100: 965-973
23. Griffiths G, Harwood JL (1991) The regulation of triacylglycerol biosynthesis in cocoa (Theobroma cacao) L. Planta 184: 279-284
24. Gritz L, Davies J (1983) Plasmid-encoded hygromycin B resistance: the sequence of hygromycin B phosphotransferase gene and its expression in Escherichia coli and Saccharomyces cerevisiae. Gene 25: 179-188
25. Haefele D, Sevenich D, Jones D, Janni J, Wright S (2007) NIR-based analytical systems enable development of corn seed products and corn grain markets that are specific for dry-grind ethanol production. Int Sugar J 109: 154-156
26. Hara A, Radin NS (1978) Lipid extraction of tissues with a low-toxicity solvent. Anal Biochem 90: 420-426
27. Jako C, Kumar A, Wei Y, Zou J, Barton DL, Giblin EM, Covello PS, Taylor DC (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
28. Janni J, Weinstock BA, Hagen L, Wright S (2008) Novel near-infrared sampling apparatus for single kernel analysis of oil content in maize. Appl Spectrosc 62: 423-426
29. Klein T, Wolf E, Sanford J (1987) High-velocity microprojectiles for delivering nucleic acids into living cells. Nature 327: 70-73
30. Kroon JT, 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
31. 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
32. Lardizabal KD, Mai JT, Wagner NW, Wyrick A, Voelker T, Hawkins DJ (2001) DGAT2 is a new diacylglycerol acyltransferase gene family: purification, cloning, and expression in insect cells of two polypeptides from Mortierella ramanniana with diacylglycerol acyltransferase activity. J Biol Chem 276: 38862-38869
33. Larson TR, Graham IA (2001) A novel technique for the sensitive quantification of acyl CoA esters from plant tissues. Plant J 25: 115-125
34. 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
35. 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
36. Li Z, Liu ZB, Xing A, Moon BP, Koellhoffer JP, Huang L, Ward RT, Clifton E, Falco SC, Cigan AM (2015) Cas9-guide RNA directed genome editing in soybean. Plant Physiol 169: 960-970
37. Li Z, Moon BP, Xing A, Liu ZB, McCardell RP, Damude HG, Falco SC (2010b) Stacking multiple transgenes at a selected genomic site via repeated recombinase-mediated DNA cassette exchanges. Plant Physiol 154: 622-631
38. Li Z, Xing A, Moon BP, Burgoyne SA, Guida AD, Liang H, Lee C, Caster CS, Barton JE, Klein TM, et al (2007) A Cre/loxP-mediated selfactivating gene excision system to produce marker gene free transgenic soybean plants. Plant Mol Biol 65: 329-341
39. Li Z, Xing A, Moon BP, McCardell RP, Mills K, Falco SC (2009) Sitespecific integration of transgenes in soybean via recombinasemediated DNA cassette exchange. Plant Physiol 151: 1087-1095
40. Liu Q, Siloto RM, Lehner R, Stone SJ, Weselake RJ (2012) Acyl-CoA: diacylglycerol acyltransferase: molecular biology, biochemistry and biotechnology. Prog Lipid Res 51: 350-377
41. Mañas-Fernández A, Vilches-Ferrón M, Garrido-Cárdenas JA, Belarbi EH, Alonso DL, García-Maroto F (2009) Cloning and molecular characterization of the acyl-CoA:diacylglycerol acyltransferase 1 (DGAT1) gene from Echium. Lipids 44: 555-568
42. 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
43. McLeod M, Craft S, Broach JR (1986) Identification of the crossover site during FLP-mediated recombination in the Saccharomyces cerevisiae plasmid 2 microns circle. Mol Cell Biol 6: 3357-3367
44. Meyer K, Stecca KL, Ewell-Hicks K, Allen SM, Everard JD (2012) Oil and protein accumulation in developing seeds is influenced by the expression of a cytosolic pyrophosphatase in Arabidopsis. Plant Physiol 159: 1221-1234
45. Milcamps A, Tumaney AW, Paddock T, Pan DA, Ohlrogge J, Pollard M (2005) Isolation of a gene encoding a 1,2-diacylglycerol-sn-acetyl-CoA acetyltransferase from developing seeds of Euonymus alatus. J Biol Chem 280: 5370-5377
46. Morley KL, Kazlauskas RJ (2005) Improving enzyme properties: when are closer mutations better? Trends Biotechnol 23: 231-237
47. Ness JE, Kim S, Gottman A, Pak R, Krebber A, Borchert TV, Govindarajan S, Mundorff EC, Minshull J (2002) Synthetic shuffling expands functional protein diversity by allowing amino acids to recombine independently. Nat Biotechnol 20: 1251-1255
48. Oakes J, Brackenridge D, Colletti R, Daley M, Hawkins DJ, Xiong H, Mai J, Screen SE, Val D, Lardizabal K, et al (2011) Expression of fungal diacylglycerol acyltransferase2 genes to increase kernel oil in maize. Plant Physiol 155: 1146-1157
49. Padgette SR, Taylor NB, Nida DL, Bailey MR, MacDonald J, Holden LR, Fuchs RL (1996) The composition of glyphosate-tolerant soybean seeds is equivalent to that of conventional soybeans. J Nutr 126: 702-716
50. Parcerisa J, Boatella J, Codony R, Rafecas M, Castellote AI, Garcia J, Lopez A, Romero A (1995) Comparison of fatty acid and triacylglycerol compositions of different hazelnut varieties (Corylus avellana L.) cultivated in Catalonia (Spain). J Agric Food Chem 43: 13-16
51. Roesler K, Meyer K, Damude HG, Shen B, Li C, Bermudez E, Tarczynski MC, inventors. January 24, 2012. DGAT genes for increased seed storage lipid production and altered fatty acid profiles in oilseed plants. US Patent Application No. 8101819 B2
52. 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
53. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463: 178-183
54. Settlage S, Kwanyuen P, Wilson R (1998) Relation between diacylglycerol acyltransferase activity and oil concentration in soybean. J Am Oil Chem Soc 75: 775-781
55. Shockey JM, Gidda SK, Chapital DC, Kuan JC, 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
56. Siloto RM, Madhavji M, Wiehler WB, Burton TL, Boora PS, Laroche A, Weselake RJ (2008) An N-terminal fragment of mouse DGAT1 binds different acyl-CoAs with varying affinity. Biochem Biophys Res Commun 373: 350-354
57. Siloto RM, Truksa M, Brownfield D, Good AG, Weselake RJ (2009) Directed evolution of acyl-CoA:diacylglycerol acyltransferase: development and characterization of Brassica napus DGAT1 mutagenized libraries. Plant Physiol Biochem 47: 456-461
58. Slack C, Roughan P, Browse J, Gardiner S (1985) Some properties of cholinephosphotransferase from developing safflower cotyledons. Biochim Biophys Acta 833: 438-448
59. Smith R, Weber C (1968) Mass selection by specific gravity for protein and oil in soybean populations. Crop Sci 8: 373-377
60. Sonah H, O’Donoughue L, Cober E, Rajcan I, Belzile F (2015) Identification of loci governing eight agronomic traits using a GBS-GWAS approach and validation by QTL mapping in soya bean. Plant Biotechnol J 13: 211-221
61. Stemmer WP (1994) DNA shuffling by random fragmentation and reassembly: in vitro recombination for molecular evolution. Proc Natl Acad Sci USA 91: 10747-10751
62. Taylor DC, Zhang Y, Kumar A, Francis T, Giblin EM, Barton DL, Ferrie JR, Laroche A, Shah S, Zhu W, 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
63. Wang Z, Huang W, Chang J, Sebastian A, Li Y, Li H, Wu X, Zhang B, Meng F, Li W (2014) Overexpression of SiDGAT1, a gene encoding acyl-CoA:diacylglycerol acyltransferase from Sesamum indicum L. increases oil content in transgenic Arabidopsis and soybean. Plant Cell Tissue Organ Cult 119: 399-410
64. Weselake RJ, Madhavji M, Szarka SJ, Patterson NA, Wiehler WB, Nykiforuk CL, Burton TL, Boora PS, Mosimann SC, Foroud NA, et al (2006) Acyl-CoA-binding and self-associating properties of a recombinant 13.3 kDa N-terminal fragment of diacylglycerol acyltransferase-1 from oilseed rape. BMC Biochem 7: 24
65. Weselake RJ, Shah S, Tang M, Quant PA, Snyder CL, Furukawa-Stoffer TL, Zhu W, Taylor DC, Zou J, Kumar A, et al (2008) Metabolic control analysis is helpful for informed genetic manipulation of oilseed rape (Brassica napus) to increase seed oil content. J Exp Bot 59: 3543-3549
66. Williams P, Norris K (1987) Near-Infrared Technology in the Agricultural and Food Industries. American Association of Cereal Chemists St. Paul, MN
67. Xu J, Francis T, Mietkiewska E, Giblin EM, Barton DL, Zhang Y, Zhang M, Taylor DC (2008) Cloning and characterization of an acyl-CoAdependent diacylglycerol acyltransferase 1 (DGAT1) gene from Tropaeolum majus, and a study of the functional motifs of the DGAT protein using site-directed mutagenesis to modify enzyme activity and oil content. Plant Biotechnol J 6: 799-818
68. Zhang C, Iskandarov U, Klotz ET, Stevens RL, Cahoon RE, Nazarenus TJ, Pereira SL, Cahoon EB (2013) A thraustochytrid diacylglycerol acyltransferase 2 with broad substrate specificity strongly increases oleic acid content in engineered Arabidopsis thaliana seeds. J Exp Bot 64: 3189-3200
69. Zheng P, Allen WB, Roesler K, Williams ME, Zhang S, Li J, Glassman K, Ranch J, Nubel D, Solawetz W, et al (2008) A phenylalanine in DGAT is a key determinant of oil content and composition in maize. Nat Genet 40: 367-372