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Review Article

Transport and transcriptional regulation of oil production in plants

, , , & ORCID Icon
Pages 641-655 | Received 10 Jul 2015, Accepted 03 May 2016, Published online: 23 Aug 2016

References

  • Fahy E, Subramaniam S, Murphy RC, et al. Update of the LIPID MAPS comprehensive classification system for lipids. J Lipid Res. 2009;50:9–14.
  • Dyer JM, Stymne S, Green AG, et al. High-value oils from plants. Plant J. 2008;54:640–655.
  • Li N, Xu C, Li-Beisson Y, et al. 2016. Fatty acid and lipid transport in plant cells. Trends Plant Sci. 2016;21:145–158.
  • Hurlock AK, Roston RL, Wang K, et al. Lipid trafficking in plant cells. Traffic. 2014;15:915–932.
  • Allen DK, Bates PD, Tjellström H. Tracking the metabolic pulse of plant lipid production with isotopic labeling and flux analyses: past, present and future. Prog Lipid Res. 2015;58:97–120.
  • Fan J, Zhai Z, Yan C, et al. Arabidopsis trigalactosyldiacylglycerol5 Interacts with TGD1, TGD2, and TGD4 to facilitate lipid transfer from the endoplasmic reticulum to plastids. Plant Cell. 2015;10:2941–2955.
  • Deruyffelaere C, Bouchez I, Morin H, et al. Ubiquitin-mediated proteasomal degradation of oleosins is involved in oil body mobilization during post-germinative seedling growth in Arabidopsis. Plant Cell Physiol. 2015;56:1374–1387.
  • Yu L, Tan X, Jiang B, et al. A peroxisomal long-chain acyl-CoA synthetase from Glycine max involved in lipid degradation. PLoS One. 2014;9:e100144.
  • Roscoe TT, Guilleminot J, Bessoule JJ, et al. Complementation of seed maturation phenotypes by ectopic expression of ABSCISIC ACID INSENSITIVE3, FUSCA3 and LEAFY COTYLEDON2 in Arabidopsis. Plant Cell Physiol. 2015;56:1215–1228.
  • Dehesh K, Tai H, Edwards P, et al. Overexpression of 3-ketoacyl-acyl-carrier protein synthase IIIs in plants reduces the rate of lipid synthesis. Plant Physiol. 2001;125:1103–1114.
  • Wu GZ, Xue HW. Arabidopsis β-ketoacyl-[acyl carrier protein] synthase i is crucial for fatty acid synthesis and plays a role in chloroplast division and embryo development. Plant Cell. 2010;22:3726–3744.
  • Sánchez-García A, Moreno-Pérez AJ, Muro-Pastor AM, et al. Acyl-ACP thioesterases from castor (Ricinus communis L.): an enzymatic system appropriate for high rates of oil synthesis and accumulation. Phytochem. 2010;71:860–869.
  • Zhang LH, Jia B, Zhuo RY, et al. An acyl-carrier protein thioesterase gene isolated from wintersweet (Chimonanthus praecox), CpFATB, enhances drought tolerance in transgenic tobacco (Nicotiana tobaccum). Plant Mol Biol Rep. 2012;30:433–442.
  • Dong S, Huang J, Li Y, et al. Cloning, characterization, and expression analysis of acyl–acyl carrier protein (ACP)-thioesterase B from seeds of Chinese Spicehush (Lindera communis). Gene. 2014;542:16–22.
  • Murad AM, Vianna GR, Machado AM, et al. Mass spectrometry characterisation of fatty acids from metabolically engineered soybean seeds. Anal Bioanal Chem. 2014;406:2873–2883.
  • Ohlrogge JB, Browse J, Somerville CR. The genetics of plant lipids. Biochim Biophys Acta. 1991;1082:1–26.
  • Routaboul JM, Skidmore C, Wallis JG, et al. Arabidopsis mutants reveal that short- and long-term thermotolerance have different requirements for trienoic fatty acids. J Exp Bot. 2012;63:1435–1443.
  • Boudiere L, Michaud M, Petroutsos D, et al. Glycerolipids in photosynthesis: composition, synthesis and trafficking. Biochim Biophys Acta. 2014;1837:470–480.
  • Kobayashi K, Awai K, Nakamura M, et al. Type-B monogalactosyldiacylglycerol synthases are involved in phosphate starvation-induced lipid remodeling, and are crucial for low-phosphate adaptation. Plant J. 2009;57:322–331.
  • Wang Z, Anderson NS, Benning C. The phosphatidic acid binding site of the Arabidopsis trigalactosyldiacylglycerol 4 (TGD4) protein required for lipid Import into chloroplasts. J Biol Chem. 2013;288:4763–4771.
  • Yang W, Pollard M, Li-Beisson Y, et al. A distinct type of glycerol-3-phosphate acyltransferase with sn-2 preference and phosphatase activity producing 2-monoacylglycerol. Proc Natl Acad Sci USA. 2010;107:12040–12045.
  • Bates PD, Browse J. The significance of different diacylgycerol synthesis pathways on plant oil composition and bioengineering. Front Plant Sci. 2012;3:147.
  • Zhao J, Davis LC, Verpoorte R. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv. 2005;23:283–333.
  • Zhao J. Phospholipase D and phosphatidic acid in plant defence response: from protein–protein and lipid–protein interactions to hormone signalling. J Exp Bot. 2015;66:1721–1736.
  • Wang L, Kazachkov M, Shen W, et al. Deciphering the roles of Arabidopsis LPCAT and PAH in phosphatidylcholine homeostasis and pathway coordination for chloroplast lipid synthesis. Plant J. 2014;80:965–976.
  • Chen B, Wang J, Zhang G, et al. Two types of soybean diacylglycerol acyltransferases are differentially involved in triacylglycerol biosynthesis and response to environmental stresses and hormones. Scientific Reports. 2016;6:28541.
  • Andrianov V, Borisjuk N, Pogrebnyak N, et al. 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. 2010;8:277–287.
  • Fan J, Yan C, Zhang X, et al. Dual role for phospholipid:diacylglycerol acyltransferase: enhancing fatty acid synthesis and diverting fatty acids from membrane lipids to triacylglycerol in Arabidopsis leaves. Plant Cell. 2013;25:3506–3518.
  • Yoon K, Han D, Li Y, et al. Phospholipid:diacylglycerol acyltransferase is a multifunctional enzyme involved in membrane lipid turnover and degradation while synthesizing triacylglycerol in the unicellular green microalga Chlamydomonas reinhardtii. Plant Cell. 2012;24:3708–3724.
  • Schmidt MA, Herman EM. Suppression of soybean oleosin produces micro-oil bodies that aggregate into oil body/ER complexes. Mol Plant. 2008;1:910–924.
  • Kunz HH, Scharnewski M, Feussner K, et al. The ABC transporter PXA1 and peroxisomal beta-oxidation are vital for metabolism in mature leaves of Arabidopsis during extended darkness. Plant Cell. 2009;21:2733–2749.
  • De Marcos Lousa C, van Roermund CW, Postis VL, et al. Intrinsic acyl-CoA thioesterase activity of a peroxisomal ATP binding cassette transporter is required for transport and metabolism of fatty acids. Proc Natl Acad Sci USA. 2013;110:1279–1284.
  • James CN, Horn PJ, Case CR, et al. Disruption of the Arabidopsis CGI-58 homologue produces Chanarin–Dorfman-like lipid droplet accumulation in plants. Proc Natl Acad Sci USA. 2010;107:17833–17838.
  • Park S, Gidda SK, James CN, et al. The α/β hydrolase CGI-58 and peroxisomal transport protein PXA1 coregulate lipid homeostasis and signaling in Arabidopsis. Plant Cell. 2013;25:1726–1739.
  • Mendiondo GM, Medhurst A, van Roermund CW, et al. Barley has two peroxisomal ABC transporters with multiple functions in β-oxidation. J Exp Bot. 2014;65:4833–4847.
  • Lopez-Marques RL, Theorin L, Palmgren MG, et al. P4-ATPases: lipid flippases in cell membranes. Pflugers Arch. 2014;466:1227–1240.
  • Quazi F, Molday RS. Differential phospholipid substrates and directional transport by ATP-binding cassette proteins ABCA1, ABCA7, and ABCA4 and disease-causing mutants. J Biol Chem. 2013;288:34414–34426.
  • Poulsen LR, Lopez-Marques RL, Pedas PR, et al. A phospholipid uptake system in the model plant Arabidopsis thaliana. Nature Commun. 2015;6:7649.
  • Volinsky R, Cwiklik L, Jurkiewicz P, et al. D Oxidized phosphatidylcholines facilitate phospholipid flip-flop in liposomes. Biophys. J. 2011;101:1376–1384.
  • Li N, Gügel IL, Giavalisco P, et al. FAX1, a novel membrane protein mediating plastid fatty acid export. PLoS Biol. 2015;13:e1002053.
  • Kim S, Yamaoka Y, Ono H, et al. AtABCA9 transporter supplies fatty acids for lipid synthesis to the endoplasmic reticulum. Proc Natl Acad Sci USA. 2013;110:773–778.
  • Zhao J. Flavonoid transport mechanisms: where to go, and with whom. Trends Plant Sci. 2015;20:576–585.
  • Li Q, Zheng Q, Shen W, et al. Understanding the biochemical basis of temperature-induced lipid pathway adjustments in plants. Plant Cell. 2015;27:86–103.
  • Pulsifer IP, Kluge S, Rowland O. Arabidopsis long-chain acyl-CoA synthetase 1 (LACS1), LACS2, and LACS3 facilitate fatty acid uptake in yeast. Plant Physiol Biochem. 2012;51:31–39.
  • Jessen D, Roth C, Wiermer M, et al. Two activities of long-chain acyl-coenzyme A synthetase are involved in lipid trafficking between the endoplasmic reticulum and the plastid in Arabidopsis. Plant Physiol. 2015;167:351–366.
  • Schnurr JA, Shockey JM, de Boer GJ, et al. Fatty acid export from the chloroplast. Molecular characterization of a major plastidial acyl-coenzyme A synthetase from Arabidopsis. Plant Physiol. 2002;129:1700–1709.
  • Zhao L, Katavic V, Li F, et al. Insertional mutant analysis reveals that long chain acyl-CoA synthetase 1 (LACS1), but not LACS8, functionally overlaps with LACS9 in Arabidopsis seed oil biosynthesis. Plant J. 2010;64:1048–1058.
  • Samuels L, Kunst L, Jetter R. Sealing plant surfaces: cuticular wax formation by epidermal cells. Annu Rev Plant Biol. 2008;59:683–707.
  • Jessen D, Olbrich A, Knüfer J, et al. Combined activity of LACS1 and LACS4 is required for proper pollen coat formation in Arabidopsis. Plant J. 2011;68:715–726.
  • Hsiao AS, Yeung EC, Ye ZW, et al. The Arabidopsis cytosolic Acyl-CoA-binding proteins play combinatory roles in pollen development. Plant Cell Physiol. 2015;56:322–333.
  • McFarlane HE, Shin JJ, Bird DA, et al. Arabidopsis ABCG transporters, which are required for export of diverse cuticular lipids, dimerize in different combinations. Plant Cell. 2010;22:3066–3075.
  • Panikashvili D, Shi JX, Schreiber L, et al. The Arabidopsis ABCG13 transporter is required for flower cuticle secretion and patterning of the petal epidermis. New Phytol. 2011;190:113–124.
  • Bessire M, Borel S, Fabre G, et al. A member of the pleiotropic drug resistance family of ATP binding cassette transporters is required for the formation of a functional cuticle in Arabidopsis. Plant Cell. 2011;23:1958–1970.
  • Chen G, Komatsuda T, Ma JF, et al. An ATP-binding cassette subfamily G full transporter is essential for the retention of leaf water in both wild barley and rice. Proc Natl Acad Sci USA. 2011;108:12354–12359.
  • Xue Y, Xiao S, Kim J, et al. Arabidopsis membrane-associated acyl-CoA-binding protein ACBP1 is involved in stem cuticle formation. J Exp Bot. 2014;65:5473–5483.
  • Yadav V, Molina I, Ranathunge K, et al. ABCG transporters are required for suberin and pollen wall extracellular barriers in Arabidopsis. Plant Cell. 2014;26:3569–3588.
  • Huang MD, Chen TL, Huang AH. Abundant type III lipid transfer proteins in Arabidopsis tapetum are secreted to the locule and become a constituent of the pollen exine. Plant Physiol. 2013;163:1218–1229.
  • Quilichini TD, Friedmann MC, Samuels AL, et al. ATP-Binding Cassette transporter G26 is required for male fertility and pollen exine formation in Arabidopsis. Plant Physiol. 2010;154:678–690.
  • Wu L, Guan Y, Wu Z, et al. OsABCG15 encodes a membrane protein that plays an important role in anther cuticle and pollen exine formation in rice. Plant Cell Rep. 2014;33:1881–1899.
  • Choi H, Ohyama K, Kim YY, et al. The role of Arabidopsis ABCG9 and ABCG31 ATP binding cassette transporters in pollen fitness and the deposition of steryl glycosides on the pollen coat. Plant Cell. 2014;26:310–324.
  • Stone SL, Braybrook SA, Paula SL, et al. Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: implications for somatic embryogenesis. Proc Natl Acad Sci USA. 2008;105:3151–3156.
  • Chiu RS, Nahal H, Provart NJ, et al. The role of the Arabidopsis FUSCA3 transcription factor during inhibition of seed germination at high temperature. BMC Plant Biol. 2012;12:15.
  • Ahmad M, Rim Y, Chen H, et al. Functional characterization of Arabidopsis Dof transcription factor AtDof4.1. Russ J Plant Physiol. 2013;60:116–123.
  • Zhang J, Hao Q, Bai L, et al. Overexpression of the soybean transcription factor GmDof4 significantly enhances the lipid content of Chlorella ellipsoidea. Biotechnol Biofuels. 2014;7:128.
  • Mu J, Tan H, Zheng Q, et al. LEAFY COTYLEDON1 is a key regulator of fatty acid biosynthesis in Arabidopsis. Plant Physiol. 2008;148:1042–1054.
  • Shen B, Allen WB, Zheng P, et al. Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol. 2010;153:980–987.
  • Tan H, Yang X, Zhang F, et al. Enhanced seed oil production in canola by conditional expression of Brassica napus LEAFY COTYLEDON1 and LEC1-LIKE in developing seeds. Plant Physiol. 2011;156:1577–1588.
  • Baud S, Wuillème S, To A, et al. Role of WRINKLED1 in the transcriptional regulation of glycolytic and fatty acid biosynthetic genes in Arabidopsis. Plant J. 2009;60:933–947.
  • Vanhercke T, El Tahchy A, Liu Q, et al. Metabolic engineering of biomass for high energy density: oilseed-like triacylglycerol yields from plant leaves. Plant Biotechnol J. 2014;12:231–239.
  • Kim HU, Lee KR, Jung SJ, et al. Senescence-inducible LEC2 enhances triacylglycerol accumulation in leaves without negatively affecting plant growth. Plant Biotechnol J. 2015;13:1346–1359.
  • Kim HU, Jung SJ, Lee KR, et al. Ectopic overexpression of castor bean LEAFY COTYLEDON2 (LEC2) in Arabidopsis triggers the expression of genes that encode regulators of seed maturation and oil body proteins in vegetative tissues. FEBS Open Bio. 2014;4:25–32.
  • Nowak K, Wójcikowska B, Gaj MD. ERF022 impacts the induction of somatic embryogenesis in Arabidopsis through the ethylene-related pathway. Planta. 2015;241:967–985.
  • Finkelstein R, Reeves W, Ariizumi T, et al. Molecular aspects of seed dormancy. Annu Rev Plant Biol. 2008;59:387–415.
  • Mönke G, Seifert M, Keilwagen J, et al. Toward the identification and regulation of the Arabidopsis thaliana ABI3 regulon. Nucleic Acids Res. 2012;40:8240–8254.
  • Zeng Y, Zhao T, Kermode AR. A conifer ABI3-interacting protein plays important roles during key transitions of the plant life cycle . Plant Physiol. 2013;161:179–195.
  • Wang F, Perry SE. Identification of direct targets of FUSCA3, a key regulator of Arabidopsis seed development. Plant Physiol. 2013;161:1251–1264.
  • Tsai AY, Gazzarrini S. AKIN10 and FUSCA3 interact to control lateral organ development and phase transitions in Arabidopsis. Plant J. 2012;69:809–821.
  • Delmas F, Sankaranarayanan S, Deb S, et al. ABI3 controls embryo degreening through Mendel's I locus. Proc Natl Acad Sci USA. 2013;110:E3888–E3894.
  • Pouvreau B, Baud S, Vernoud V, et al. Duplicate maize Wrinkled1 transcription factors activate target genes involved in seed oil biosynthesis. Plant Physiol. 2011;156:674–686.
  • Yang Y, Munz J, Cass C, et al. Ectopic expression of WRINKLED1 affects fatty acid homeostasis in Brachypodium distachyon vegetative tissues. Plant Physiol. 2015;169:1836–1847.
  • Baud S, Feria Bourrellier AB, Azzopardi M, et al. PII is induced by WRINKLED1 and fine-tunes fatty acid composition in seeds of Arabidopsis thaliana. Plant J. 2010;64:291–303.
  • To A, Joubès J, Barthole G, et al. WRINKLED transcription factors orchestrate tissue-specific regulation of fatty acid biosynthesis in Arabidopsis. Plant Cell. 2012;26:5007–5023.
  • Wang HW, Zhang B, Hao YJ, et al. The soybean Dof-type transcription factor genes, GmDof4 and GmDof11, enhance lipid content in the seeds of transgenic Arabidopsis plants. Plant J. 2007;52:716–729.
  • Ibáñez-Salazar A, Rosales-Mendoza S, Rocha-Uribe A, et al. Over-expression of Dof-type transcription factor increases lipid production in Chlamydomonas reinhardtii. J Biotechnol. 2014;184:27–38.
  • Alonso R, Oñate-Sánchez L, Weltmeier F, et al. A pivotal role of the basic leucine zipper transcription factor bzip53 in the regulation of Arabidopsis seed maturation gene expression based on heterodimerization and protein complex formation. Plant Cell. 2009;21:1747–1761.
  • Song QX, Li QT, Liu YF, et al. Soybean GmbZIP123 gene enhances lipid content in the seeds of transgenic Arabidopsis plants. J Exp Bot. 2013;64:4329–4341.
  • Yamamoto A, Kagaya Y, Toyoshima R, et al. Arabidopsis NF-YB subunits LEC1 and LEC1-LIKE activate transcription by interacting with seed-specific ABRE-binding factors. Plant J. 2009;58:843–856.
  • Liu YF, Li QT, Lu X, et al. Soybean GmMYB73 promotes lipid accumulation in transgenic plants. BMC Plant Biol. 2014;14:73.
  • Raffaele S, Vailleau F, Léger A, et al. A MYB transcription factor regulates very long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis. Plant Cell. 2008;20:752–767.
  • SeoPJ, Lee SB, Suh MC, et al. The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell. 2011;3:1138–1152.
  • Shi L, Katavic V, Yu Y, et al. Arabidopsis glabra2 mutant seeds deficient in mucilage biosynthesis produce more oil. Plant J. 2012;69:37–46.
  • Zhang H, Bishop B, Ringenberg W, et al. The CHD3 remodeler PICKLE associates with genes enriched for trimethylation of histone H3 lysine 27. Plant Physiol. 2012;159:418–432.
  • Veerappan V, Chen N, Reichert AI, et al. HSI2/VAL1 PHD-like domain promotes H3K27 trimethylation to repress the expression of seed maturation genes and complex transgenes in Arabidopsis seedlings. BMC Plant Biol. 2014;14:293.
  • Wang Z, Chen M, Chen T, et al. TRANSPARENT TESTA2 regulates embryonic fatty acid biosynthesis by targeting FUSCA3 during the early developmental stage of Arabidopsis seeds. Plant J. 2014;77:757–769.
  • Gao MJ, Lydiate DJ, Li X, et al. Repression of seed maturation genes by a trihelix transcriptional repressor in Arabidopsis seedlings. Plant Cell. 2009;21:54–71.
  • Ohto MA, Floyd SK, Fischer RL, et al. Effects of APETALA2 on embryo, endosperm, and seed coat development determine seed size in Arabidopsis. Sex Plant Reprod. 2009;22:277–289.
  • Chapman KD, Ohlrogge JB. Compartmentation of triacylglycerol accumulation in plants. J Biol Chem. 2012;287:2288–2294.
  • Zale J, Jung JH, Kim JY, et al. Metabolic engineering of sugarcane to accumulate energy-dense triacylglycerols in vegetative biomass. Plant Biotechnol J. 2015;14:661–669.
  • Fan J, Yan C, Roston R, et al. Arabidopsis lipins, PDAT1 acyltransferase, and SDP1 triacylglycerol lipase synergistically direct fatty acids toward β-oxidation, thereby maintaining membrane lipid homeostasis. Plant Cell. 2014;26:4119–4134.
  • Singer SD, Weselake RJ, Rahman H. Development and characterization of low α-linolenic acid Brassica oleracea lines bearing a novel mutation in a 'class a' fatty acid desaturase 3 gene. BMC Genet. 2014;15:94.
  • Dhakal KH, Jung KH, Chae JH, et al. Variation of unsaturated fatty acids in soybean sprout of high oleic acid accessions. Food Chem. 2014;164:70–73.
  • Ruiz-Lopez N, Haslam RP, Usher S, et al. An alternative pathway for the effective production of the omega-3 long-chain polyunsaturates EPA and ETA in transgenic oilseeds. Plant Biotechnol J. 2015;13:1264–1275.
  • Pan X, Siloto RM, Wickramarathna AD, et al. Identification of a pair of phospholipid:diacylglycerol acyltransferases from developing flax (Linum usitatissimum L.) seed catalyzing the selective production of trilinolenin. J Biol Chem. 2013;288:24173–24188.
  • Nguyen HT, Park H, Koster KL, et al. Redirection of metabolic flux for high levels of omega-7 monounsaturated fatty acid accumulation in Camelina seeds. Plant Biotechnol J. 2015;13:38–50.
  • Tsai CH, Warakanont J, Takeuchi T, et al. The protein compromised hydrolysis of triacylglycerols 7 (CHT7) acts as a repressor of cellular quiescence in Chlamydomonas. Proc Natl Acad Sci USA. 2014;111:15833–15838.
  • Tanaka T, Maeda Y, Veluchamy A, et al. Oil accumulation by the oleaginous diatom fistulifera solaris as revealed by the genome and transcriptome. Plant Cell. 2015;27:162–176.