Endoplasmic reticulum retention signaling and transmembrane channel proteins predicted for oilseed ω3 fatty acid desaturase 3 (FAD3) genes

  • Mohammad Fazel Soltani Gishini
  • Alireza ZebarjadiEmail author
  • Maryam Abdoli-nasab
  • Mokhtar Jalali Javaran
  • Danial Kahrizi
  • David HildebrandEmail author
Original Article


Oilseed crop oils contain a variety of unsaturated fatty acids that are synthesized and regulated by fatty acid desaturases (FADs). In this study, 14 FAD3 (ω3 desaturase) protein sequences from oilseeds are analyzed and presented through the application of several computational tools. The results indicated a close relationship between Brassica napus and Camelina sativa, as well as between Salvia hispanica and Perilla frutescens FAD3s, due to a high similarity in codon preferences in codon usage clusters and the phylogenetic tree. The cis-acting element results reveal that the seed-specific promoter region of BnFAD3 contains the critical conserved boxes such as HSE and ABRE, which are involved in responsiveness to heat stress and abscisic acid. The presence of the aforementioned conserved boxes may increase cold acclimation as well as tolerance to drought and high salinity. Omega(ω)3 desaturases contain a Skn-1 motif which is a cis-acting regulatory element required involved in endosperm development. In oilseed FAD3s, leucine is the most repeated amino acid in FAD3 proteins. The study conveyed that B. napus, Camelina sativa, Linum usitatissimum, Vernicia fordii, Gossypium hirsutum, S. hispanica, Cannabis sativa, and P. frutescens have retention signal KXKXX/XKXX at their c-terminus sites, which is one of the most important characteristics of FADs. Additionally, it was found that BnFAD3 is a transmembrane protein that can convert ω6 to ω3 fatty acids and may simultaneously act as a potassium ion channel in the ER.


Delta 15 desaturase Conserved histidine Retention signal Codon usage Ion channel 



Molecular graphics and analyses were performed with the UCSF Chimera package. Chimera is developed by the Resource for Biocomputing, Visualization, and Informatics at the University of California, San Francisco (supported by NIGMS P41-GM103311). Special thanks to Rebecca Caldbeck, Haleigh Whitlock, and Connor Coatney at the University of Kentucky for editing and reviewing of this manuscript.


  1. Abbadi A et al (2004) Biosynthesis of verylongchain polyunsaturated fatty acids in transgenic oilseeds: constraints on their accumulation. Plant Cell 16(10):2734–2748. PubMedPubMedCentralCrossRefGoogle Scholar
  2. Almen MS, Nordstrom KJ, Fredriksson R, Schioth HB (2009) Mapping the human membrane proteome: a majority of the human membrane proteins can be classified according to function and evolutionary origin. BMC Biol 7:50. PubMedPubMedCentralCrossRefGoogle Scholar
  3. Alonso DL and Maroto FG, Plants as 'chemical factories' for the production of polyunsaturated fatty acids, Biotechnol Adv, vol. 18, no. 6, pp. 481–497, 2000. [Online]. Available:
  4. Alonso DL, GarciaMaroto F, RodriguezRuiz J, Garrido J, Vilches M (2003) Evolution of the membranebound fatty acid desaturases. Biochem Syst Ecol 31(10):1111–1124CrossRefGoogle Scholar
  5. Arondel V, Lemieux B, Hwang I, Gibson S, Goodman HM, Somerville CR (1992) Mapbased cloning of a gene controlling omega3 fatty acid desaturation in Arabidopsis. Science 258(5086):1353–1355PubMedCrossRefGoogle Scholar
  6. Bailey TL and Elkan C, Fitting a mixture model by expectation maximization to discover motifs in biopolymers, Proc Int Conf Intell Syst Mol Biol, vol. 2, pp. 2836, 1994. [Online]. Available:
  7. Bannai H, Tamada Y, Maruyama O, Nakai K, and Miyano S (2001) Views: fundamental building blocks in the process of knowledge discovery, in FLAIRS Conference, pp. 233–238Google Scholar
  8. Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S (2002) Extensive feature detection of Nterminal protein sorting signals. Bioinformatics 18(2):298–305PubMedCrossRefGoogle Scholar
  9. Bennetzen JL and Hall BD, Codon selection in yeast, J Biol Chem, vol. 257, no. 6, pp. 3026–3031, (1982). [Online]. Available:
  10. Bidinotto LT, López de Cicco R, Russo J (2011) Omega3 fatty acids: a potential booster for tamoxifen therapy? Expert Rev Anticancer Ther 11(8):1151–1153PubMedCrossRefGoogle Scholar
  11. Boevink P, Santa Cruz S, Hawes C, Harris N, Oparka K (1996) Virusmediated delivery of the green fluorescent protein to the endoplasmic reticulum of plant cells. Plant J 10(5):935–941CrossRefGoogle Scholar
  12. Borgeson CE, de Renobales M, and Blomquist GJ, Characterization of the delta 12 desaturase in the American cockroach, Periplaneta americana: the nature of the substrate, Biochim Biophys Acta, vol. 1047, no. 2, pp. 135–140, 1990. [Online]. Available:
  13. Brändén CI, Tooze J (1999) Introduction to protein structure. Taylor & FrancisGoogle Scholar
  14. Brenna JT, Diau GY (2007) The influence of dietary docosahexaenoic acid and arachidonic acid on central nervous system polyunsaturated fatty acid composition. Prostaglandins Leukot Essent Fat Acids 77(5–6):247–250CrossRefGoogle Scholar
  15. Browse J, Somerville C (1991) Glycerolipid synthesis: biochemistry and regulation. Annu Rev Plant Biol 42(1):467–506CrossRefGoogle Scholar
  16. Burley SK, Roeder RG (1996) Biochemistry and structural biology of transcription factor IID (TFIID). Annu Rev Biochem 65:769–799. CrossRefPubMedGoogle Scholar
  17. Calder PC (2013) Omega3 polyunsaturated fatty acids and inflammatory processes: nutrition or pharmacology? Br J Clin Pharmacol 75(3):645–662PubMedPubMedCentralCrossRefGoogle Scholar
  18. Cao S et al (2013) A large and functionally diverse family of Fad2 genes in safflower (Carthamus tinctorius L.). BMC Plant Biol 13(1):5PubMedPubMedCentralCrossRefGoogle Scholar
  19. Cheng B, Wu G, Vrinten P, Falk K, Bauer J, Qiu X (2010) Towards the production of high levels of eicosapentaenoic acid in transgenic plants: the effects of different host species, genes and promoters. Transgenic Res 19(2):221–229PubMedCrossRefGoogle Scholar
  20. Chi X et al (2011) Genomewide analysis of fatty acid desaturases in soybean (Glycine max). Plant Mol Biol Report 29(4):769–783CrossRefGoogle Scholar
  21. Clemente TE, Cahoon EB (2009) Soybean oil: genetic approaches for modification of functionality and total content. Plant Physiol 151(3):1030–1040PubMedPubMedCentralCrossRefGoogle Scholar
  22. Cohen C, Parry DA (1990) Alphahelical coiled coils and bundles: how to design an alphahelical protein. Proteins 7(1):1–15. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Concino M, Goldman RA, Caruthers MH, and Weinmann R, Point mutations of the adenovirus major late promoter with different transcriptional efficiencies in vitro, J Biol Chem, vol. 258, no. 13, pp. 8493–8496, 1983. [Online]. Available:
  24. Cook HW, McMaster CR (2002) Fatty acid desaturation and chain elongation in eukaryotes, in New comprehensive biochemistry, vol 36. Elsevier, pp 181–204Google Scholar
  25. Corden J, Wasylyk B, Buchwalder A, SassoneCorsi P, Kedinger C, and Chambon P, Promoter sequences of eukaryotic proteincoding genes, Science, vol. 209, no. 4463, pp. 1406–1414, 1980. [Online]. Available:
  26. Cripps C, Borgeson C, Blomquist GJ, and de Renobales M (1990) The delta 12desaturase from the house cricket, Acheta domesticus (Orthoptera: Gryllidae):characterization and form of the substrate, Arch Biochem Biophys, vol. 278, no. 1, pp. 46–51. [Online]. Available:
  27. Dailey HA, Strittmatter P (1979) Modification and identification of cytochrome b5 carboxyl groups involved in proteinprotein interaction with cytochrome b5 reductase. J Biol Chem 254(12):5388–5396PubMedPubMedCentralGoogle Scholar
  28. Damude HG, Kinney AJ (2008) Enhancing plant seed oils for human nutrition. Plant Physiol 147(3):962–968PubMedPubMedCentralCrossRefGoogle Scholar
  29. Denecke J, EK B, Caspers M, Sinjorgo KM, Palva ET (1993) Analysis of sorting signals responsible for the accumulation of soluble reticuloplasmins in the plant endoplasmic reticulum. J Exp Bot:213–221Google Scholar
  30. Eckert H, LaVallee B, Schweiger BJ, Kinney AJ, Cahoon EB, Clemente T (2006) Coexpression of the borage ?6 desaturase and the Arabidopsis Δ15 desaturase results in high accumulation of stearidonic acid in the seeds of transgenic soybean. Planta 224(5):1050–1057PubMedCrossRefGoogle Scholar
  31. Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural networkbased method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8(5):978–984. CrossRefPubMedPubMedCentralGoogle Scholar
  32. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2(4):953–971. CrossRefPubMedGoogle Scholar
  33. Etzel MR (2004) Manufacture and use of dairy protein fractions. J Nutr 134(4):996S–1002S. CrossRefPubMedGoogle Scholar
  34. Fasano E, Serini S, Cittadini A, Calviello G (2017) Longchain n3 PUFA against breast and prostate cancer: which are the appropriate doses for intervention studies in animals and humans? Crit Rev Food Sci Nutr 57(11):2245–2262PubMedCrossRefPubMedCentralGoogle Scholar
  35. Gasteiger E, Hoogland C, Gattiker A, Wilkins MR, Appel RD, and Bairoch A (2005), Protein identification and analysis tools on the ExPASy server, in The proteomics protocols handbook: Springer, pp. 571–607Google Scholar
  36. Gomord V and Faye L (1996) Signals and mechanisms involved in intracellular transport of secreted proteins in plants, Plant Physiology and Biochemistry (France)Google Scholar
  37. Gomord V, Denmat L A, FitchetteLaine A C, SatiatJeunemaitre B, C Hawes, and Faye L., The Cterminal HDEL sequence is sufficient for retention of secretory proteins in the endoplasmic reticulum (ER) but promotes vacuolar targeting of proteins that escape the ER, Plant J, vol. 11, no. 2, pp. 313–325, 1997. [Online]. Available:
  38. Grantham R, Perrin P, Mouchiroud D (1986) Patterns in codon usage of different kinds of species. Oxford Surv Evol Biol 3:48–81Google Scholar
  39. Guo AY, Zhu QH, Chen X, and Luo JC (2007) [GSDS: a gene structure display server], Yi Chuan, vol. 29, no. 8, pp. 1023–1026. [Online]. Available:
  40. Hackett CS, Strittmatter P (1984) Covalent crosslinking of the active sites of vesiclebound cytochrome b5 and NADHcytochrome b5 reductase. J Biol Chem 259(5):3275–3282PubMedGoogle Scholar
  41. Hazel JR, Williams EE (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29(3):167–227PubMedCrossRefGoogle Scholar
  42. Herman EM, Tague BW, Hoffman LM, Kjemtrup SE, Chrispeels MJ (1990) Retention of phytohemagglutinin with carboxyterminal tetrapeptide KDEL in the nuclear envelope and the endoplasmic reticulum. Planta 182(2):305–312. CrossRefPubMedGoogle Scholar
  43. Hong H, Datla N, Reed DW, Covello PS, MacKenzie SL, Qiu X (2002) Highlevel production of gammalinolenic acid in Brassica juncea using a delta6 desaturase from Pythium irregulare. Plant Physiol 129(1):354; Hu SL and Manley JL, DNA sequence required for initiation of transcription in vitro from the major late promoter of adenovirus 2, Proc Natl Acad Sci USA, vol. 78, no. 2, pp. 820–824, 1981. [Online]. Available:
  44. Iba K (2002) Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Annu Rev Plant Biol 53(1):225–245PubMedCrossRefGoogle Scholar
  45. Iba K et al., A gene encoding a chloroplast omega3 fatty acid desaturase complements alterations in fatty acid desaturation and chloroplast copy number of the fad7 mutant of Arabidopsis thaliana, J Biol Chem, vol. 268, no. 32, pp. 24099–24105, 1993. [Online]. Available: Scholar
  46. Ito M (2000) Factors controlling cyclin B expression. In: Inzé D (ed) The plant cell cycle. Springer Netherlands, Dordrecht, pp 133–146CrossRefGoogle Scholar
  47. Ito M (2005) Conservation and diversification of threerepeat Myb transcription factors in plants. J Plant Res, journal article 118(1):61–69. CrossRefGoogle Scholar
  48. MR Jackson, Nilsson T, and Peterson PA, Retrieval of transmembrane proteins to the endoplasmic reticulum, J Cell Biol, vol. 121, no. 2, pp. 317–333, 1993. [Online]. Available:
  49. Jones AL, Lloyd D, Harwood JL (1993) Rapid induction of microsomal Δ12 (ω 6)desaturase activity in chilled Acanthamoeba castellanii. Biochem J 296(1):183–188PubMedPubMedCentralCrossRefGoogle Scholar
  50. Kahrizi D, ROSTAMI AH, and Akbarabadi A (2015) Feasibility cultivation of Camelina (Camelina sativa) as medicinaloil plant in rainfed conditions in KermanshahIran's first reportGoogle Scholar
  51. Kato K et al (2009) Preferential upregulation of G2/M phasespecific genes by overexpression of the hyperactive form of NtmybA2 lacking its negative regulation domain in tobacco BY2 cells. Plant Physiol 149(4):1945–1957. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Katsanos CS, Kobayashi H, SheffieldMoore M, Aarsland A, Wolfe RR (2006) A high proportion of leucine is required for optimal stimulation of the rate of muscle protein synthesis by essential amino acids in the elderly. Am J Physiol Endocrinol Metab 291(2):E381–E387. CrossRefPubMedGoogle Scholar
  53. Khadake R, Khonde V, Mhaske V, Ranjekar P, Harsulkar A (2011) Functional and bioinformatic characterisation of sequence variants of Fad3 gene from flax. J Sci Food Agric 91(14):2689–2696. CrossRefPubMedGoogle Scholar
  54. Kinsella JE, Lokesh B, Broughton S, Whelan J (1990) Dietary polyunsaturated fatty acids and eicosanoids: potential effects on the modulation of inflammatory and immune cells: an overview. Nutrition 6(1):24–44PubMedGoogle Scholar
  55. Knothe G (2002) Structure indices in FA chemistry. How relevant is the iodine value? J Am Oil Chem Soc 79(9):847–854. CrossRefGoogle Scholar
  56. Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305(3):567–580. CrossRefPubMedGoogle Scholar
  57. Kyriakidis NB, Katsiloulis T (2000) Calculation of iodine value from measurements of fatty acid methyl esters of some oils: comparison with the relevant American Oil Chemists Society method. J Am Oil Chem Soc, journal article 77(12):1235–1238. CrossRefGoogle Scholar
  58. Kyte J and Doolittle RF, A simple method for displaying the hydropathic character of a protein, J Mol Biol, vol. 157, no. 1, pp. 105–132, 1982. [Online]. Available:
  59. Layman DK, Role of leucine in protein metabolism during exercise and recovery, Can J Appl Physiol, vol. 27, no. 6, pp. 646–663, 2002. [Online]. Available:
  60. Layman DK (2003) The role of leucine in weight loss diets and glucose homeostasis. J Nutr 133(1):261S–267S. CrossRefPubMedGoogle Scholar
  61. Lee H, Park WJ (2014) Unsaturated fatty acids, desaturases, and human health. J Med Food 17(2):189–197PubMedCrossRefGoogle Scholar
  62. Lee KR et al (2016) Functional identification of oleate 12desaturase and ω3 fatty acid desaturase genes from Perilla frutescens var. frutescens. Plant Cell Rep 35(12):2523–2537PubMedCrossRefGoogle Scholar
  63. Lescot M et al (2002) PlantCARE, a database of plant cisacting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30(1):325–327PubMedPubMedCentralCrossRefGoogle Scholar
  64. Li Z et al (2019) Generation of. Transgenic Camelina sativa with Modified Seed Fatty Acid Composition 21(2):443–448Google Scholar
  65. Liu HL, Yin ZJ, Xiao L, Xu YN, Qu Le Q (2012) Identification and evaluation of omega3 fatty acid desaturase genes for hyperfortifying alphalinolenic acid in transgenic rice seed. J Exp Bot 63(8):3279–3287. CrossRefPubMedPubMedCentralGoogle Scholar
  66. Los DA, Murata N (1998) Structure and expression of fatty acid desaturases. Biochimica Biophys Acta 1394(1):3–15CrossRefGoogle Scholar
  67. Mackenzie KR (2006) Folding and stability of alphahelical integral membrane proteins. Chem Rev 106(5):1931–1977. CrossRefPubMedGoogle Scholar
  68. Marquardt A, Stöhr H, White K, Weber BH (2000) cDNA cloning, genomic structure, and chromosomal localization of three members of the human fatty acid desaturase family. Genomics 66(2):175–183PubMedCrossRefGoogle Scholar
  69. McConn M, James D Jr, Browse J, Miquel M (1993) Mutants of Arabidopsis deficient in the synthesis of alphalinolenate. Biochemical and genetic characterization of the endoplasmic reticulum linoleoyl desaturase 268(22):16345–16351Google Scholar
  70. McGuffin LJ, Bryson K and Jones DT The PSIPRED protein structure prediction server, Bioinformatics, vol. 16, no. 4, pp. 404–405, 2000. [Online]. Available:
  71. McKevith B (2005) Nutritional aspects of oilseeds. Nutr Bull 30(1):13–26CrossRefGoogle Scholar
  72. Menges M, de Jager SM, Gruissem W, Murray JA (2005) Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J 41(4):546–566. CrossRefPubMedGoogle Scholar
  73. Miquel MF (1994) Higholeate oilseeds fail to develop at low temperature. Plant Physiol 106(2):421–427PubMedPubMedCentralCrossRefGoogle Scholar
  74. Mitchell AG, Martin CE (1995) A novel cytochrome b5like domain is linked to the carboxyl terminus of the Saccharomyces cerevisiae ?9 fatty acid desaturase. J Biol Chem 270(50):29766–29772PubMedCrossRefGoogle Scholar
  75. Murphy DJ (1999) Production of novel oils in plants. Curr Opin Biotechnol 10(2):175–180PubMedCrossRefGoogle Scholar
  76. Nagai J, Bloch K (1966) Enzymatic desaturation of stearyl acyl carrier protein. J Biol Chem 241(8):1925–1927PubMedGoogle Scholar
  77. Napier JA (2007) The production of unusual fatty acids in transgenic plants. Annu Rev Plant Biol 58:295–319PubMedCrossRefGoogle Scholar
  78. Napier JA, Graham IA (2010) Tailoring plant lipid composition: designer oilseeds come of age. Curr Opin Plant Biol 13(3):329–336CrossRefGoogle Scholar
  79. Nayeri FD, Yarizade K (2014) Bioinformatics study of delta12 fatty acid desaturase 2 (FAD2) gene in oilseeds. Mol Biol Rep 41(8):5077–5087CrossRefGoogle Scholar
  80. Nielsen H, Engelbrecht J, Brunak S, and von Heijne G (1997), Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites, Protein Eng, vol. 10, no. 1, pp. 1–6 [Online]. Available: Scholar
  81. Nishitani S, Matsumura T, Fujitani S, Sonaka I, Miura Y, and Yagasaki K (2002), Leucine promotes glucose uptake in skeletal muscles of rats, Biochem Biophys Res Commun, vol. 299, no. 5, pp. 693–696. [Online]. Available:
  82. Niu B et al (2008) Molecular cloning, characterization, and expression of an ω3 fatty acid desaturase gene from Sapium sebiferum. J Biosci Bioeng 106(4):375–380PubMedCrossRefGoogle Scholar
  83. Nykiforuk CL et al (2012) High level accumulation of gamma linolenic acid (C18:3Delta6.9,12 cis) in transgenic safflower (Carthamus tinctorius) seeds. Transgenic Res 21(2):367–381. CrossRefPubMedGoogle Scholar
  84. Oeda K, Salinas J, and Chua NH, A tobacco bZip transcription activator (TAF1) binds to a Gboxlike motif conserved in plant genes, EMBO J, vol. 10, no. 7, pp. 1793–1802, 1991. [Online]. Available: Scholar
  85. Okuley J, Lightner J, Feldmann K, Yadav N, Lark E (1994) Arabidopsis FAD2 gene encodes the enzyme that is essential for polyunsaturated lipid synthesis. Plant Cell 6(1):147–158PubMedPubMedCentralGoogle Scholar
  86. Oura T, Kajiwara S (2004) Saccharomyces kluyveri FAD3 encodes an ω3 fatty acid desaturase. Microbiology 150(6):1983–1990PubMedCrossRefGoogle Scholar
  87. Pagny S, Lerouge P, Faye L, Gomord V (1999) Signals and mechanisms for protein retention in the endoplasmic reticulum. J Exp Bot 50(331):157–164CrossRefGoogle Scholar
  88. PellegriniCalace M, Maiwald T, Thornton JM (2009) PoreWalker: a novel tool for the identification and characterization of channels in transmembrane proteins from their threedimensional structure. PLoS Comput Biol 5(7):e1000440. CrossRefGoogle Scholar
  89. Pereira SL, Leonard AE, Mukerji P (2003) Recent advances in the study of fatty acid desaturases from animals and lower eukaryotes. Prostaglandins Leukot Essent Fat Acids 68(2):97–106CrossRefGoogle Scholar
  90. Pettersen EF et al (2004) UCSF chimera—a visualization system for exploratory research and analysis. J Comput Chem 25(13):1605–1612. CrossRefPubMedPubMedCentralGoogle Scholar
  91. PeyouNdi MM, Watts JL, Browse J (2000) Identification and characterization of an animal Δ12 fatty acid desaturase gene by heterologous expression in Saccharomyces cerevisiae. Arch Biochem Biophys 376(2):399–408CrossRefGoogle Scholar
  92. Pugh BF, Mechanisms of transcription complex assembly, Curr Opin Cell Biol, vol. 8, no. 3, pp. 303–311, 1996. [Online]. Available:
  93. Qi B et al (2004) Production of very long chain polyunsaturated omega3 and omega6 fatty acids in plants. Nat Biotechnol 22(6):739–745. CrossRefPubMedPubMedCentralGoogle Scholar
  94. Qiu X, Hong H, Datla N, MacKenzie SL, Taylor DC, Thomas TL (2002) Expression of borage Δ6 desaturase in Saccharomyces cerevisiae and oilseed crops. Can J Bot 80(1):42–49CrossRefGoogle Scholar
  95. Radovanovic N, Thambugala D, Duguid S, Loewen E, Cloutier S (2014) Functional characterization of flax fatty acid desaturase FAD2 and FAD3 isoforms expressed in yeast reveals a broad diversity in activity. Mol Biotechnol 56(7):609–620PubMedCrossRefGoogle Scholar
  96. Ramji DP, Foka P (2002) CCAAT/enhancerbinding proteins: structure, function and regulation. Biochem J 365(Pt 3):561–575. CrossRefPubMedPubMedCentralGoogle Scholar
  97. Reddy AS, Thomas TL (1996) Expression of a cyanobacterial delta 6desaturase gene results in gammalinolenic acid production in transgenic plants. Nat Biotechnol 14(5):639–642. CrossRefPubMedGoogle Scholar
  98. Román Á et al (2012) Contribution of the different omega3 fatty acid desaturase genes to the cold response in soybean. J Exp Bot 63(13):4973–4982PubMedPubMedCentralCrossRefGoogle Scholar
  99. Rombauts S, Déhais P, Van Montagu M, Rouzé P (1999) PlantCARE, a plant cisacting regulatory element database. Nucleic Acids Res 27(1):295–296PubMedPubMedCentralCrossRefGoogle Scholar
  100. Rothman JE, Orci L (1992) Molecular dissection of the secretory pathway. Nature 355(6359):409–415. CrossRefPubMedPubMedCentralGoogle Scholar
  101. Roy A, Kucukural A, Zhang Y (2010) ITASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5(4):725–738. CrossRefPubMedPubMedCentralGoogle Scholar
  102. Roynette CE, Calder PC, Dupertuis YM, Pichard C (2004) N3 polyunsaturated fatty acids and colon cancer prevention. Clin Nutr 23(2):139–151PubMedCrossRefPubMedCentralGoogle Scholar
  103. RuizLópez N, Sayanova O, Napier JA, Haslam RP (2012) Metabolic engineering of the omega3 long chain polyunsaturated fatty acid biosynthetic pathway into transgenic plants. J Exp Bot 63(7):2397–2410CrossRefGoogle Scholar
  104. Saha S, Zack J, Singh B, Raghava GP (2006) VGIchan: prediction and classification of voltagegated ion channels. Genomics Proteomics Bioinformatics 4(4):253–258. CrossRefPubMedPubMedCentralGoogle Scholar
  105. Sakamoto T et al (1994) Cloning of ?3 desaturase from cyanobacteria and its use in altering the degree of membranelipid unsaturation. Plant Mol Biol 26(1):249–263PubMedCrossRefPubMedCentralGoogle Scholar
  106. Sakuradani E, Kobayashi M, Ashikari T, Shimizu S (1999) Identification of ?12fatty acid desaturase from arachidonic acidproducing Mortierella fungus by heterologous expression in the yeast Saccharomyces cerevisiae and the fungus Aspergillus oryzae. Eur J Biochem 261(3):812–820PubMedCrossRefPubMedCentralGoogle Scholar
  107. Sakuradani E, Abe T, Iguchi K, Shimizu S (2005) A novel fungal omega3desaturase with wide substrate specificity from arachidonic acidproducing Mortierella alpina 1S4. Appl Microbiol Biotechnol 66(6):648–654. CrossRefPubMedPubMedCentralGoogle Scholar
  108. Sambrook J, Russell DW, Russell DW (2001) Molecular cloning: a laboratory manual (3volume set). Immunol 49:895–909Google Scholar
  109. Sawadogo M and Roeder RG, Interaction of a genespecific transcription factor with the adenovirus major late promoter upstream of the TATA box region, Cell, vol. 43, no. 1, pp. 165–175, 1985. [Online]. Available:
  110. Sayanova O et al., Expression of a borage desaturase cDNA containing an Nterminal cytochrome b5 domain results in the accumulation of high levels of delta6desaturated fatty acids in transgenic tobacco, Proc Natl Acad Sci U S A, vol. 94, no. 8, pp. 4211–4216, 1997. [Online]. Available:
  111. Sayanova O et al (2006) A bifunctional Δ12, Δ15desaturase from Acanthamoeba castellanii directs the synthesis of highly unusual n1 series unsaturated fatty acids. J Biol Chem 281(48):36533–36541PubMedCrossRefGoogle Scholar
  112. Schmidt H, Heinz E (1990) Involvement of ferredoxin in desaturation of lipidbound oleate in chloroplasts. Plant Physiol 94(1):214–220PubMedPubMedCentralCrossRefGoogle Scholar
  113. Shanklin J, Cahoon EB (1998) Desaturation and related modifications of fatty acids. Annu Rev Plant Biol 49(1):611–641CrossRefGoogle Scholar
  114. Shanklin J, Whittle E, Fox BG (1994) Eight histidine residues are catalytically essential in a membraneassociated iron enzyme, stearoylCoA desaturase, and are conserved in alkane hydroxylase and xylene monooxygenase. Biochemistry 33(43):12787–12794PubMedCrossRefGoogle Scholar
  115. Sharma A, Chauhan RS (2012) In silico identification and comparative genomics of candidate genes involved in biosynthesis and accumulation of seed oil in plants. Comp Funct Genomics 2012Google Scholar
  116. Shorrosh BS and Dixon RA (1991) Molecular cloning of a putative plant endomembrane protein resembling vertebrate protein disulfideisomerase and a phosphatidylinositolspecific phospholipase C, Proc Natl Acad Sci USA, vol. 88, no. 23, pp. 10941–10945. [Online]. Available:
  117. Simopoulos AP (2010) Genetic variants in the metabolism of omega6 and omega3 fatty acids: their role in the determination of nutritional requirements and chronic disease risk. Exp Biol Med 235(7):785–795CrossRefGoogle Scholar
  118. Simpson SD, Nakashima K, Narusaka Y, Seki M, Shinozaki K, and YamaguchiShinozaki K, Two different novel cisacting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and darkinduced senescence, Plant J, vol. 33, no. 2, pp. 259–270, 2003. [Online]. Available:
  119. Small I, Peeters N, Legeai F, Lurin C (2004) Predotar: a tool for rapidly screening proteomes for Nterminal targeting sequences. Proteomics 4(6):1581–1590. CrossRefPubMedGoogle Scholar
  120. Soltani MF, Hadizadeh M, Soltani Banavandi MJ, Yazdizadeh A, Alemzadeh A (2014) Bioinformatics comparison of codon usage of genes encoding phosphate transporter in terms of salt tolerance, day length, temperature and pollination in different plants. Int J Adv Biol Biomed Res 2(2):504–509Google Scholar
  121. Somerville C, Browse J (1996) Dissecting desaturation: plants prove advantageous. Trends Cell Biol 6(4):148–153PubMedCrossRefGoogle Scholar
  122. Sonnhammer EL, von Heijne G, and Krogh A, A hidden Markov model for predicting transmembrane helices in protein sequences, Proc Int Conf Intell Syst Mol Biol, vol. 6, pp. 175182, 1998. [Online]. Available:
  123. Soorni J, Kazemitabar SK, Kahrizi D, Dehestani A, Bagheri N (2017) Screening of camelina (Camelina sativa L.) doubled haploid lines for freezing tolerance in the seedling stage. Genetika 49:173–181CrossRefGoogle Scholar
  124. Sperling P, Ternes P, Zank T, Heinz E (2003) The evolution of desaturases. Prostaglandins Leukot Essent Fatty Acids 68(2):73–95PubMedCrossRefGoogle Scholar
  125. Spychalla JP, Kinney AJ (1997) Identification of an animal ?3 fatty acid desaturase by heterologous expression in Arabidopsis. Proc Natl Acad Sci 94(4):1142–1147PubMedCrossRefGoogle Scholar
  126. Stornaiuolo M et al (2003) KDEL and KKXX retrieval signals appended to the same reporter protein determine different trafficking between endoplasmic reticulum, intermediate compartment, and Golgi complex. Mol Biol Cell 14(3):889–902. CrossRefPubMedPubMedCentralGoogle Scholar
  127. Stothard P (2000) The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques 28(6):1102–1104. CrossRefGoogle Scholar
  128. Stukey JE, McDonough VM, Martin CE (1990) The OLE1 gene of Saccharomyces cerevisiae encodes the delta 9 fatty acid desaturase and can be functionally replaced by the rat stearoylCoA desaturase gene. J Biol Chem 265(33):20144–20149PubMedGoogle Scholar
  129. Superko HR et al (2014) Omega3 fatty acid blood levels clinical significance update. Curr Cardiovasc Risk Rep 8(11):407PubMedPubMedCentralCrossRefGoogle Scholar
  130. Thomas A (2000) Fats and fatty oils, Ullmann's Encyclopedia of Industrial Chemistry Tocher DR, Leaver MJ, Hodgson P (1998) Recent advances in the biochemistry and molecular biology of fatty acyl desaturases. Prog Lipid Res 37(2):73–117Google Scholar
  131. Ursin VM (2003) Modification of plant lipids for human health: development of functional landbased omega3 fatty acids. J Nutr 133(12):4271–4274. CrossRefPubMedGoogle Scholar
  132. VenegasCalerón M, Sayanova O, Napier JA (2010a) An alternative to fish oils: metabolic engineering of oilseed crops to produce omega3 long chain.
  133. VenegasCalerón M, Sayanova O, Napier JA (2010b) An alternative to fish oils: metabolic engineering of oilseed crops to produce omega3 long chain polyunsaturated fatty acids. Prog Lipid Res 49(2):108–119CrossRefGoogle Scholar
  134. Vincent MJ, Martin AS, and Compans RW, Function of the KKXX motif in endoplasmic reticulum retrieval of a transmembrane protein depends on the length and structure of the cytoplasmic domain, J Biol Chem, vol. 273, no. 2, pp. 950–956, 1998. [Online]. Available:
  135. Vitale A, Ceriotti A, Denecke J (1993) The role of the endoplasmic reticulum in protein synthesis, modification and intracellular transport. J Exp Bot 44(9):1417–1444CrossRefGoogle Scholar
  136. Vrinten P, Hu Z, Munchinsky MA, Rowland G, Qiu X (2005) Two FAD3 desaturase genes control the level of linolenic acid in flax seed. Plant Physiol 139(1):79–87PubMedPubMedCentralCrossRefGoogle Scholar
  137. Wada H, Schmidt H, Heinz E, Murata N (1993) In vitro ferredoxindependent desaturation of fatty acids in cyanobacterial thylakoid membranes. J Bacteriol 175(2):544PubMedPubMedCentralCrossRefGoogle Scholar
  138. Wandelt CI, Khan MR, Craig S, Schroeder HE, Spencer D, and Higgins TJ, Vicilin with carboxyterminal KDEL is retained in the endoplasmic reticulum and accumulates to high levels in the leaves of transgenic plants, Plant J, vol. 2, no. 2, pp. 181–192, 1992. [Online]. Available:
  139. Wang M, Chen H, Gu Z, Zhang H, Chen W, Chen YQ (2013) ?3 fatty acid desaturases from microorganisms: structure, function, evolution, and biotechnological use. Appl Microbiol Biotechnol 97(24):10255–10262PubMedPubMedCentralCrossRefGoogle Scholar
  140. Wang H et al (2015) Crystal structure of human stearoylcoenzyme A desaturase in complex with substrate. Nat Struct Mol Biol 22(7):581–585. CrossRefPubMedGoogle Scholar
  141. Warude D, Joshi K, Harsulkar A (2006) Polyunsaturated fatty acids: biotechnology. Crit Rev Biotechnol 26(2):83–93PubMedCrossRefGoogle Scholar
  142. Wu G et al (2005) Stepwise engineering to produce high yields of very longchain polyunsaturated fatty acids in plants. Nat Biotechnol 23(8):1013PubMedCrossRefGoogle Scholar
  143. Wu P et al (2013) Functional characterization of two microsomal fatty acid desaturases from Jatropha curcas L. J Plant Physiol 170(15):1360–1366PubMedCrossRefGoogle Scholar
  144. Xue Y et al (2018) Omega3 fatty acid desaturase gene family from two ω3 sources, Salvia hispanica and Perilla frutescens: Cloning, characterization and expression. PloS one 13(1):e0191432PubMedPubMedCentralCrossRefGoogle Scholar
  145. Yadav NS et al (1993) Cloning of higher plant [omega]3 fatty acid desaturases. Plant Physiol 103(2):467–476PubMedPubMedCentralCrossRefGoogle Scholar
  146. Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y (2015) The ITASSER suite: protein structure and function prediction. Nat Methods 12(1):7–8. CrossRefPubMedPubMedCentralGoogle Scholar
  147. Yin DD et al (2018) Fatty acid desaturase 3 (PsFAD3) from Paeonia suffruticosa reveals high alinolenic acid accumulation. Plant Sci 274:212–222PubMedCrossRefGoogle Scholar
  148. Zäuner S, Jochum W, Bigorowski T, Benning C (2012) A cytochrome b5containing plastidlocated fatty acid desaturase from Chlamydomonas reinhardtii. Eukaryotic cell. EC:0007912Google Scholar
  149. Zhang Y (2008) ITASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40. CrossRefPubMedPubMedCentralGoogle Scholar
  150. Zhang S, Sakuradani E, Ito K, Shimizu S (2007a) Identification of a novel bifunctional delta12/delta15 fatty acid desaturase from a basidiomycete, Coprinus cinereus TD#822–2. FEBS Lett 581(2):315–319. CrossRefPubMedGoogle Scholar
  151. Zhang Y, Guo K, LeBlanc RE, Loh D, Schwartz GJ, Yu YH (2007b) Increasing dietary leucine intake reduces dietinduced obesity and improves glucose and cholesterol metabolism in mice via multimechanisms. Diabetes 56(6):1647–1654. CrossRefPubMedGoogle Scholar
  152. Zhao YW, Su ZD, Yang W, Lin H, Chen W, Tang H (2017) IonchanPred 2.0: a tool to predict ion channels and their types. Int J Mol Sci 18(9). PubMedCentralCrossRefPubMedGoogle Scholar
  153. Zheng JS, Huang T, Yang J, Fu YQ, Li D (2012) Marine N3 polyunsaturated fatty acids are inversely associated with risk of type 2 diabetes in Asians: a systematic review and metaanalysis. PloS one 7(9):e44525PubMedPubMedCentralCrossRefGoogle Scholar
  154. Zhou XR, Green AG, Singh SP (2011) Caenorhabditis elegans Δ12desaturase FAT2 is a bifunctional desaturase able to desaturate a diverse range of fatty acid substrates at the Δ12 and Δ15 positions. J Biol Chem.

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Production Engineering and Plant Genetics, Faculty of Sciences and Agricultural Engineering, Campus of Agriculture and Natural ResourcesRazi UniversityKermanshahIran
  2. 2.Department of Biotechnology, Institute of Science, High Technology and Environmental ScienceGraduate University of Advanced TechnologyKermanIran
  3. 3.Department of Plant Breeding & Biotechnology, Faculty of AgricultureTarbiat Modarres UniversityTehranIran
  4. 4.Department of Plant & Soil SciencesUniversity of KentuckyLexingtonUSA

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