Genetic Manipulation of Non-Classic Oilseed Plants for Enhancement of Their Potential as a Biofactory for Triacylglycerol Production

Xiao-Yu Xu, Hong-Kun Yang, Surinder P. Singh, Peter J. Sharp, Qing Liu

Engineering ›› 2018, Vol. 4 ›› Issue (4) : 523-533.

PDF(1066 KB)
PDF(1066 KB)
Engineering ›› 2018, Vol. 4 ›› Issue (4) : 523-533. DOI: 10.1016/j.eng.2018.07.002
Research
Research Crop Genetics and Breeding—Review

Genetic Manipulation of Non-Classic Oilseed Plants for Enhancement of Their Potential as a Biofactory for Triacylglycerol Production

Author information +
History +

Abstract

Global demand for vegetable oil is anticipated to double by 2030. The current vegetable oil production platforms, including oil palm and temperate oilseeds, are unlikely to produce such an expansion. Therefore, the exploration of novel vegetable oil sources has become increasingly important in order to make up this future vegetable oil shortfall. Triacylglycerol (TAG), as the dominant form of vegetable oil, has recently attracted immense interest in terms of being produced in plant vegetative tissues via genetic engineering technologies. Multidiscipline-based “-omics” studies are increasingly enhancing our understanding of plant lipid biochemistry and metabolism. As a result, the identification of biochemical pathways and the annotation of key genes contributing to fatty acid biosynthesis and to lipid assembly and turnover have been effectively updated. In recent years, there has been a rapid development in the genetic enhancement of TAG accumulation in high-biomass plant vegetative tissues and oilseeds through the genetic manipulation of the key genes and regulators involved in TAG biosynthesis. In this review, current genetic engineering strategies ranging from single-gene manipulation to multigene stacking aimed at increasing plant biomass TAG accumulation are summarized. New directions and suggestions for plant oil production that may help to further alleviate the potential shortage of edible oil and biodiesel are discussed.

Keywords

Plant vegetable oil / Triacylglycerol / Genetic engineering / Edible oil / Biodiesel

Cite this article

Download citation ▾
Xiao-Yu Xu, Hong-Kun Yang, Surinder P. Singh, Peter J. Sharp, Qing Liu. Genetic Manipulation of Non-Classic Oilseed Plants for Enhancement of Their Potential as a Biofactory for Triacylglycerol Production. Engineering, 2018, 4(4): 523‒533 https://doi.org/10.1016/j.eng.2018.07.002

References

[1]
Harwood J.L., Ramli U.S., Tang M., Quant P.A., Weselake R.J., Fawcett T., . Regulation and enhancement of lipid accumulation in oil crops: the use of metabolic control analysis for informed genetic manipulation. Eur J Lipid Sci Technol. 2013; 115(11): 1239-1246.
[2]
Murphy D.J.. The future of oil palm as a major global crop: opportunities and challenges. J Oil Palm Res. 2014; 26(1): 1-24.
[3]
Carlsson A.S., Yilmaz J.L., Green A.G., Stymne S., Hofvander P.. Replacing fossil oil with fresh oil—with what and for what?. Eur J Lipid Sci Technol. 2011; 113(7): 812-831.
[4]
Atabani A.E., Silitonga A.S., Ong H.C., Mahlia T.M.I., Masjuki H.H., Badruddin I.A., . Non-edible vegetable oils: a critical evaluation of oil extraction, fatty acid compositions, biodiesel production, characteristics, engine performance and emissions production. Renew Sustain Energy Rev. 2013; 18: 211-245.
[5]
Alptekin E., Canakci M., Sanli H.. Biodiesel production from vegetable oil and waste animal fats in a pilot plant. Waste Manag. 2014; 34(11): 2146-2154.
[6]
Castillo López B., Esteban Cerdán L., Robles Medina A., Navarro López E., Martín Valverde L., Hita Peña E., . Production of biodiesel from vegetable oil and microalgae by fatty acid extraction and enzymatic esterification. J Biosci Bioeng. 2015; 119(6): 706-711.
[7]
Fan Y., Wu G., Su F., Li K., Xu L., Han X., . Lipase oriented-immobilized on dendrimer-coated magnetic multi-walled carbon nanotubes toward catalyzing biodiesel production from waste vegetable oil. Fuel. 2016; 178: 172-178.
[8]
Araújo K., Mahajan D., Kerr R., da Silva M.. Global biofuels at the crossroads: an overview of technical, policy, and investment complexities in the sustainability of biofuel development. Agriculture. 2017; 7(4): 32.
[9]
Castiblanco C., Etter A., Aide T.M.. Oil palm plantations in Colombia: a model of future expansion. Environ Sci Policy. 2013; 27: 172-183.
[10]
Carlson K.M., Curran L.M., Asner G.P., Pittman A.M.D., Trigg S.N., Marion Adeney J.. Carbon emissions from forest conversion by Kalimantan oil palm plantations. Nat Clim Chang. 2013; 3(3): 283-287.
[11]
Faruk A., Belabut D., Ahmad N., Knell R.J., Garner T.W.. Effects of oil-palm plantations on diversity of tropical anurans. Conserv Biol. 2013; 27(3): 615-624.
[12]
Vargas L.E.P., Laurance W.F., Clements G.R., Edwards W.. The impacts of oil palm agriculture on Colombia’s biodiversity: what we know and still need to know. Trop Conserv Sci. 2015; 8(3): 828-845.
[13]
Yue S., Brodie J.F., Zipkin E.F., Bernard H.. Oil palm plantations fail to support mammal diversity. Ecol Appl. 2015; 25(8): 2285-2292.
[14]
Yang Z., Ohlrogge J.B.. Turnover of fatty acids during natural senescence of Arabidopsis, Brachypodium, and switchgrass and in Arabidopsis β-oxidation mutants. Plant Physiol. 2009; 150(4): 1981-1989.
[15]
Fan J., Yan C., Zhang X., Xu C.. 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(9): 3506-3518.
[16]
Chapman K.D., Ohlrogge J.B.. Compartmentation of triacylglycerol accumulation in plants. J Biol Chem. 2012; 287(4): 2288-2294.
[17]
Vanhercke T., Divi U.K., El Tahchy A., Liu Q., Mitchell M., Taylor M.C., . Step changes in leaf oil accumulation via iterative metabolic engineering. Metab Eng. 2017; 39: 237-246.
[18]
Vanhercke T., El Tahchy A., Liu Q., Zhou X.R., Shrestha P., Divi U.K., . Metabolic engineering of biomass for high energy density: oilseed-like triacylglycerol yields from plant leaves. Plant Biotechnol J. 2014; 12(2): 231-239.
[19]
Zale J., Jung J.H., Kim J.Y., Pathak B., Karan R., Liu H., . Metabolic engineering of sugarcane to accumulate energy-dense triacylglycerols in vegetative biomass. Plant Biotechnol J. 2016; 14(2): 661-669.
[20]
Hofvander P., Ischebeck T., Turesson H., Kushwaha S.K., Feussner I., Carlsson A.S., . Potato tuber expression of Arabidopsis WRINKLED1 increase triacylglycerol and membrane lipids while affecting central carbohydrate metabolism. Plant Biotechnol J. 2016; 14(9): 1883-1898.
[21]
Liu Q., Guo Q., Akbar S., Zhi Y., El Tahchy A., Mitchell M., . Genetic enhancement of oil content in potato tuber (Solanum tuberosum L.) through an integrated metabolic engineering strategy. Plant Biotechnol J. 2017; 15(1): 56-67.
[22]
Saito K., Matsuda F.. Metabolomics for functional genomics, systems biology, and biotechnology. Annu Rev Plant Biol. 2010; 61(1): 463-489.
[23]
Nakamura Y., Teo N.Z., Shui G., Chua C.H., Cheong W.F., Parameswaran S., . Transcriptomic and lipidomic profiles of glycerolipids during Arabidopsis flower development. New Phytol. 2014; 203(1): 310-322.
[24]
Napier J.A., Haslam R.P., Beaudoin F., Cahoon E.B.. Understanding and manipulating plant lipid composition: metabolic engineering leads the way. Curr Opin Plant Biol. 2014; 19: 68-75.
[25]
Chen G., Woodfield H.K., Pan X., Harwood J.L., Weselake R.J.. Acyl-trafficking during plant oil accumulation. Lipids. 2015; 50(11): 1057-1068.
[26]
Bates P.D.. Understanding the control of acyl flux through the lipid metabolic network of plant oil biosynthesis. Biochim Biophys Acta. 2016; 1861(9 Pt B): 1214-1225.
[27]
Li N., Shi J., Wang X., Liu G., Wang H.. A combined linkage and regional association mapping validation and fine mapping of two major pleiotropic QTLs for seed weight and silique length in rapeseed (Brassica napus L.). BMC Plant Biol. 2014; 14(1): 114.
[28]
Abbadi A., Leckband G.. Rapeseed breeding for oil content, quality, and sustainability. Eur J Lipid Sci Technol. 2011; 113(10): 1198-1206.
[29]
Jestin C., Lodé M., Vallée P., Domin C., Falentin C., Horvais R., . Association mapping of quantitative resistance for Leptosphaeria maculans in oilseed rape (Brassica napus L.). Mol Breed. 2011; 27(3): 271-287.
[30]
Wang N., Li F., Chen B., Xu K., Yan G., Qiao J., . Genome-wide investigation of genetic changes during modern breeding of Brassica napus. Theor Appl Genet. 2014; 127(8): 1817-1829.
[31]
Raman H., Dalton-Morgan J., Diffey S., Raman R., Alamery S., Edwards D., . SNP markers-based map construction and genome-wide linkage analysis in Brassica napus. Plant Biotechnol J. 2014; 12(7): 851-860.
[32]
Li F., Chen B., Xu K., Wu J., Song W., Bancroft I., . Genome-wide association study dissects the genetic architecture of seed weight and seed quality in rapeseed (Brassica napus L.). DNA Res. 2014; 21(4): 355-367.
[33]
Snowdon R.J., Iniguez Luy F.L.. Potential to improve oilseed rape and canola breeding in the genomics era. Plant Breed. 2012; 131(3): 351-360.
[34]
Stamp P., Visser R.. The twenty-first century, the century of plant breeding. Euphytica. 2012; 186(3): 585-591.
[35]
Qu C., Hasan M., Lu K., Liu L., Zhang K., Fu F., . Identification of QTL for seed coat colour and oil content in Brassica napus by association mapping using SSR markers. Can J Plant Sci. 2014; 95(2): 387-395.
[36]
Körber N., Bus A., Li J., Parkin I.A., Wittkop B., Snowdon R.J., . Agronomic and seed quality traits dissected by genome-wide association mapping in Brassica napus. Front Plant Sci. 2016; 7(7): 386.
[37]
Liu S., Fan C., Li J., Cai G., Yang Q., Wu J., . A genome-wide association study reveals novel elite allelic variations in seed oil content of Brassica napus. Theor Appl Genet. 2016; 129(6): 1203-1215.
[38]
Qi Z., Wu Q., Han X., Sun Y., Du X., Liu C., . Soybean oil content QTL mapping and integrating with meta-analysis method for mining genes. Euphytica. 2011; 179(3): 499-514.
[39]
Moose S.P., Dudley J.W., Rocheford T.R.. Maize selection passes the century mark: a unique resource for 21st century genomics. Trends Plant Sci. 2004; 9(7): 358-364.
[40]
Frey K.J., Holland J.B.. Nine cycles of recurrent selection for increased groat-oil content in oat. Crop Sci. 1999; 39(6): 1636-1641.
[41]
Holland J.B., Frey K.J., Hammond E.G.. Correlated responses of fatty acid composition, grain quality, and agronomic traits to nine cycles of recurrent selection for increased oil content in oat. Euphytica. 2001; 122(1): 69-79.
[42]
Wilcove D.S., Koh L.P.. Addressing the threats to biodiversity from oil-palm agriculture. Biodivers Conserv. 2010; 19(4): 999-1007.
[43]
Wong C.K., Bernardo R.. Genomewide selection in oil palm: increasing selection gain per unit time and cost with small populations. Theor Appl Genet. 2008; 116(6): 815-824.
[44]
Montoya C., Lopes R., Flori A., Cros D., Cuellar T., Summo M., . Quantitative trait loci (QTL) analysis of palm oil fatty acid composition in an interspecific pseudo-backcross from Elaeis oleifera (H.B.K) Cortés and oil palm (Elaeis guineensis Jacq.). Tree Genet Genomes. 2013; 9(5): 1207-1225.
[45]
Ting N.C., Jansen J., Mayes S., Massawe F., Sambanthamurthi R., Ooi L.C., . High density SNP and SSR-based genetic maps of two independent oil palm hybrids. BMC Genomics. 2014; 15(1): 309.
[46]
Singh R., Low E.T., Ooi L.C., Ong-Abdullah M., Ting N.C., Nagappan J., . The oil palm SHELL gene controls oil yield and encodes a homologue of SEEDSTICK. Nature. 2013; 500(7462): 340-344.
[47]
Andersen M.M., Landes X., Xiang W., Anyshchenko A., Falhof J., Østerberg J.T., . Feasibility of new breeding techniques for organic farming. Trends Plant Sci. 2015; 20(7): 426-434.
[48]
Shih P.M., Liang Y., Loqué D.. Biotechnology and synthetic biology approaches for metabolic engineering of bioenergy crops. Plant J. 2016; 87(1): 103-117.
[49]
Achten W.M.J., Mathijs E., Verchot L., Singh V.P., Aerts R., Muys B.. Jatropha biodiesel fueling sustainability?. Biofuel Bioprod Bior. 2007; 1(4): 283-291.
[50]
Carlsson A.S.. Plant oils as feedstock alternatives to petroleum—a short survey of potential oil crop platforms. Biochimie. 2009; 91(6): 665-670.
[51]
Akbar E., Yaakob Z., Kamarudin S.K., Ismail M., Salimon J.. Characteristic and composition of Jatropha curcas oil seed from Malaysia and its potential as biodiesel feedstock. Eur J Sci Res. 2009; 29(3): 396-403.
[52]
Divakara B.N., Upadhyaya H.D., Wani S.P., Gowda C.L.L.. Biology and genetic improvement of Jatropha curcas L.: a review. Appl Energy. 2010; 87(3): 732-742.
[53]
Jubinsky G., Anderson L.C.. The invasive potential of Chinese tallow-tree (Sapium sebiferum Roxb.) in the southeast. Castanea. 1996; 61(3): 226-231.
[54]
Atadashi I.M., Aroua M.K., Aziz A.A.. High quality biodiesel and its diesel engine application: a review. Renew Sust Energ Rev. 2010; 14(7): 1999-2008.
[55]
Picou L., Boldor D.. Thermophysical characterization of the seeds of invasive Chinese tallow tree: importance for biofuel production. Environ Sci Technol. 2012; 46(20): 11435-11442.
[56]
Zhang X., Huang W.. Biodiesel fuel production through transesterification of Chinese tallow kernel oil using KNO3/MgO catalyst. Procedia Environ Sci. 2011; 11(Part B): 757-762.
[57]
Boldor D., Kanitkar A., Terigar B.G., Leonardi C., Lima M., Breitenbeck G.A.. Microwave assisted extraction of biodiesel feedstock from the seeds of invasive Chinese tallow tree. Environ Sci Technol. 2010; 44(10): 4019-4025.
[58]
Yang X.Q., Pan H., Zeng T., Shupe T.F., Hse C.Y.. Extraction and characterization of seed oil from naturally grown Chinese tallow trees. J Am Oil Chem Soc. 2013; 90(3): 459-466.
[59]
Divi U.K.. Oil accumulation in non-seed tissue: transcriptome analysis of Chinese tallow. Gene Transl Bioinf. 2016; 2: 1-12.
[60]
Gao R., Su Z., Yin Y., Sun L., Li S.. Germplasm, chemical constituents, biological activities, utilization, and control of Chinese tallow (Triadica sebifera (L.) Small). Biol Invasions. 2016; 18(3): 809-829.
[61]
Oderinde R.A., Tairu O.A.. Evaluation of the properties of yellow nutsedge (Cyperus esculentus) tuber oil. Food Chem. 1988; 28(3): 233-237.
[62]
Pascual B., Maroto J.V., LóPez-Galarza S.A., Sanbautista A., Alagarda J.. Chufa (Cyperus esculentus L. var. sativus Boeck.): an unconventional crop. Studies related to applications and cultivation. Econ Bot. 2000; 54(4): 439-448.
[63]
Bangarwa S.K., Norsworthy J.K., Mattice J.D., Gbur E.E.. Yellow nutsedge interference in polyethylene-mulched bell pepper as influenced by turnip soil amendment. Weed Technol. 2011; 25(3): 466-472.
[64]
Westendorff N., Agostinetto D., Ulguim A.R., Langaro A.C., Thürmer L.. Initial growth and competitive ability of yellow nutsedge and irrigated rice. Planta Daninha. 2013; 31(4): 813-821.
[65]
Turesson H., Marttila S., Gustavsson K.E., Hofvander P., Olsson M.E., Bülow L., . Characterization of oil and starch accumulation in tubers of Cyperus esculentus var. sativus (Cyperaceae): a novel model system to study oil reserves in nonseed tissues. Am J Bot. 2010; 97(11): 1884-1893.
[66]
Thieffry A.. RNA-Seq: Yellow nutsedge (Cyperus esculentus) transcriptome analysis of lipid-accumulating tubers from early to late developmental stages [dissertation].
[67]
Yang Y., Shi J., Wang X., Liu G., Wang H.. Genetic architecture and mechanism of seed number per pod in rapeseed: elucidated through linkage and near-isogenic line analysis. Sci Rep. 2016; 6(1): 24124.
[68]
Xu C., Shanklin J.. Triacylglycerol metabolism, function, and accumulation in plant vegetative tissues. Annu Rev Plant Biol. 2016; 67(1): 179-206.
[69]
Kunst L., Browse J., Somerville C.. Altered chloroplast structure and function in a mutant of Arabidopsis deficient in plastid glycerol-3-phosphate acyltransferase activity. Plant Physiol. 1989; 90(3): 846-853.
[70]
Gidda S.K., Shockey J.M., Rothstein S.J., Dyer J.M., Mullen R.T.. Arabidopsis thaliana GPAT8 and GPAT9 are localized to the ER and possess distinct ER retrieval signals: functional divergence of the dilysine ER retrieval motif in plant cells. Plant Physiol Biochem. 2009; 47(10): 867-879.
[71]
Wang Z., Benning C.. Chloroplast lipid synthesis and lipid trafficking through ER-plastid membrane contact sites. Biochem Soc Trans. 2012; 40(2): 457-463.
[72]
Singer S.D., Chen G., Mietkiewska E., Tomasi P., Jayawardhane K., Dyer J.M., . Arabidopsis GPAT9 contributes to synthesis of intracellular glycerolipids but not surface lipids. J Exp Bot. 2016; 67(15): 4627-4638.
[73]
Shockey J., Regmi A., Cotton K., Adhikari N., Browse J., Bates P.D.. Identification of Arabidopsis GPAT9 (At5g60620) as an essential gene involved in triacylglycerol biosynthesis. Plant Physiol. 2016; 170(1): 163-179.
[74]
Dahlqvist A., Ståhl U., Lenman M., Banas A., Lee M., Sandager L., . Phospholipid:diacylglycerol acyltransferase: an enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants. Proc Natl Acad Sci USA. 2000; 97(12): 6487-6492.
[75]
Cagliari A., Margis-Pinheiro M., Loss G., Mastroberti A.A., de Araujo Mariath J.E., Margis R.. Identification and expression analysis of castor bean (Ricinus communis) genes encoding enzymes from the triacylglycerol biosynthesis pathway. Plant Sci. 2010; 179(5): 499-509.
[76]
Huang A.H.. Oleosins and oil bodies in seeds and other organs. Plant Physiol. 1996; 110(4): 1055-1061.
[77]
Gidda S.K., Park S., Pyc M., Yurchenko O., Cai Y., Wu P., . Lipid droplet-associated proteins (LDAPs) are required for the dynamic regulation of neutral lipid compartmentation in plant cells. Plant Physiol. 2016; 170(4): 2052-2071.
[78]
Shimada T.L., Takano Y., Shimada T., Fujiwara M., Fukao Y., Mori M., . Leaf oil body functions as a subcellular factory for the production of a phytoalexin in Arabidopsis. Plant Physiol. 2014; 164(1): 105-118.
[79]
Horn P.J., James C.N., Gidda S.K., Kilaru A., Dyer J.M., Mullen R.T., . Identification of a new class of lipid droplet-associated proteins in plants. Plant Physiol. 2013; 162(4): 1926-1936.
[80]
Hillebrand A., Post J.J., Wurbs D., Wahler D., Lenders M., Krzyzanek V., . Down-regulation of small rubber particle protein expression affects integrity of rubber particles and rubber content in Taraxacum brevicorniculatum. PLoS One. 2012; 7(7): e41874.
[81]
Sookmark U., Pujade-Renaud V., Chrestin H., Lacote R., Naiyanetr C., Seguin M., . Characterization of polypeptides accumulated in the latex cytosol of rubber trees affected by the tapping panel dryness syndrome. Plant Cell Physiol. 2002; 43(11): 1323-1333.
[82]
Gidda S.K., Park S., Pyc M., Yurchenko O., Cai Y., Wu P., . Lipid droplet-associated proteins (LDAPs) are required for the dynamic regulation of neutral lipid compartmentation in plant cells. Plant Physiol. 2016; 170: 2052-2071.
[83]
Pyc M., Cai Y., Gidda S.K., Yurchenko O., Park S., Kretzschmar F.K., . Arabidopsis lipid droplet-associated protein (LDAP)-interacting protein (LDIP) influences lipid droplet size and neutral lipid homeostasis in both leaves and seeds. Plant J. 2017; 92: 1182-1201.
[84]
Huang A.H.. Plant lipid droplets and their associated proteins: potential for rapid advances. Plant Physiol. 2018; 176: 1894-1918.
[85]
Li Q., Shao J., Tang S., Shen Q., Wang T., Chen W., . Wrinkled1 accelerates flowering and regulates lipid homeostasis between oil accumulation and membrane lipid anabolism in Brassica napus. Front Plant Sci. 2015; 6: 1015.
[86]
Yang Y., Munz J., Cass C., Zienkiewicz A., Kong Q., Ma W., . Ectopic expression of WRI1 affects fatty acid homeostasis in Brachypodium distachyon vegetative tissues. Plant Physiol. 2015; 169: 1836-1847.
[87]
Kim H.U., Jung S.J., Lee K.R., Kim E.H., Lee S.M., Roh K.H., . 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. 2013; 4(1): 25-32.
[88]
Kim H.U., Lee K.R., Jung S.J., Shin H.A., Go Y.S., Suh M.C., . Senescence-inducible LEC2 enhances triacylglycerol accumulation in leaves without negatively affecting plant growth. Plant Biotechnol J. 2015; 13(9): 1346-1359.
[89]
Klaus D., Ohlrogge J.B., Neuhaus H.E., Dörmann P.. Increased fatty acid production in potato by engineering of acetyl-CoA carboxylase. Planta. 2004; 219(3): 389-396.
[90]
Wang Z., Huang W., Chang J., Sebastian A., Li Y., Li H., . Overexpression of SiDGAT1, a gene encoding acyl-CoA: diacylglycerol acyltransferase from Sesamum indicum L. increases oil content in transgenic Arabidopsis and soybean. Plant Cell Tiss Org. 2014; 119(2): 399-410.
[91]
Fan J., Yan C., Roston R., Shanklin J., Xu C.. Arabidopsis lipins, PDAT1 acyltransferase, and SDP1 triacylglycerol lipase synergistically direct fatty acids toward β-oxidation, thereby maintaining membrane lipid homeostasis. Plant Cell. 2014; 26(10): 4119-4134.
[92]
Banaś W., Carlsson A.S., Banas A.. Effect of overexpression of PDAT gene on Arabidopsis growth rate and seed oil content. J Agric Sci. 2014; 6(5): 65-79.
[93]
Van Erp H., Bates P.D., Burgal J., Shockey J., Browse J.. Castor phospholipid:diacylglycerol acyltransferase facilitates efficient metabolism of hydroxy fatty acids in transgenic Arabidopsis. Plant Physiol. 2011; 155(2): 683-693.
[94]
Kelly A.A., Shaw E., Powers S.J., Kurup S., Eastmond P.J.. Suppression of the SUGAR-DEPENDENT1 triacylglycerol lipase family during seed development enhances oil yield in oilseed rape (Brassica napus L.). Plant Biotechnol J. 2013; 11(3): 355-361.
[95]
Kim M.J., Yang S.W., Mao H.Z., Veena S.P., Yin J.L., Chua N.H.. Gene silencing of sugar-dependent 1 (JcSDP1), encoding a patatin-domain triacylglycerol lipase, enhances seed oil accumulation in Jatropha curcas. Biotechnol Biofuels. 2014; 7(1): 36.
[96]
Vijayakumar A., Vijayaraj P., Vijayakumar A.K., Rajasekharan R.. The Arabidopsis ABHD11 mutant accumulates polar lipids in leaves as a consequence of absent acylhydrolase activity. Plant Physiol. 2016; 170(1): 180-193.
[97]
Park S., Gidda S.K., James C.N., Horn P.J., Khuu N., Seay D.C., . The α/β hydrolase CGI-58 and peroxisomal transport protein PXA1 coregulate lipid homeostasis and signaling in Arabidopsis. Plant Cell. 2013; 25(5): 1726-1739.
[98]
Kunz H.H., Scharnewski M., Feussner K., Feussner I., Flügge U.I., Fulda M., . The ABC transporter PXA1 and peroxisomal β-oxidation are vital for metabolism in mature leaves of Arabidopsis during extended darkness. Plant Cell. 2009; 21(9): 2733-2749.
[99]
Slocombe S.P., Cornah J., Pinfield-Wells H., Soady K., Zhang Q., Gilday A., . Oil accumulation in leaves directed by modification of fatty acid breakdown and lipid synthesis pathways. Plant Biotechnol J. 2009; 7(7): 694-703.
[100]
Cai Y., Goodman J.M., Pyc M., Mullen R.T., Dyer J.M., Chapman K.D.. Arabidopsis SEIPIN proteins modulate triacylglycerol accumulation and influence lipid droplet proliferation. Plant Cell. 2015; 27(9): 2616-2636.
[101]
Focks N., Benning C.. Wrinkled1: a novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism. Plant Physiol. 1998; 118(1): 91-101.
[102]
Cernac A., Benning C.. Wrinkled1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J. 2004; 40(4): 575-585.
[103]
Ruuska S.A., Girke T., Benning C., Ohlrogge J.B.. Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell. 2002; 14(6): 1191-1206.
[104]
Baud S., Mendoza M.S., To A., Harscoët E., Lepiniec L., Dubreucq B.. Wrinkled1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis. Plant J. 2007; 50(5): 825-838.
[105]
To A., Joubès J., Barthole G., Lécureuil A., Scagnelli A., Jasinski S., . WRINKLED transcription factors orchestrate tissue-specific regulation of fatty acid biosynthesis in Arabidopsis. Plant Cell. 2012; 24(12): 5007-5023.
[106]
Pouvreau B., Baud S., Vernoud V., Morin V., Py C., Gendrot G., . Duplicate maize Wrinkled1 transcription factors activate target genes involved in seed oil biosynthesis. Plant Physiol. 2011; 156(2): 674-686.
[107]
Wu X.L., Liu Z.H., Hu Z.H., Huang R.Z.. BnWRI1 coordinates fatty acid biosynthesis and photosynthesis pathways during oil accumulation in rapeseed. J Integr Plant Biol. 2014; 56(6): 582-593.
[108]
Sanjaya Durrett TP, Weise S.E.. Benning C. Increasing the energy density of vegetative tissues by diverting carbon from starch to oil biosynthesis in transgenic Arabidopsis. Plant Biotechnol J. 2011; 9(8): 874-883.
[109]
Bourgis F., Kilaru A., Cao X., Ngando-Ebongue G.F., Drira N., Ohlrogge J.B., . Comparative transcriptome and metabolite analysis of oil palm and date palm mesocarp that differ dramatically in carbon partitioning. Proc Natl Acad Sci USA. 2011; 108(30): 12527-12532.
[110]
Voelker T.. Secrets of palm oil biosynthesis revealed. Proc Natl Acad Sci USA. 2011; 108(30): 12193-12194.
[111]
Maeo K., Tokuda T., Ayame A., Mitsui N., Kawai T., Tsukagoshi H., . An AP2-type transcription factor, WRINKLED1, of Arabidopsis thaliana binds to the AW-box sequence conserved among proximal upstream regions of genes involved in fatty acid synthesis. Plant J. 2009; 60(3): 476-487.
[112]
Ma W., Kong Q., Mantyla J.J., Yang Y., Ohlrogge J.B., Benning C.. 14-3-3 protein mediates plant seed oil biosynthesis through interaction with AtWRI1. Plant J. 2016; 88(2): 228-235.
[113]
Prescha A., Świedrych A., Biernat J., Szopa J.. Increase in lipid content in potato tubers modified by 14-3-3 gene overexpression. J Agric Food Chem. 2001; 49(8): 3638-3643.
[114]
Wójcikowska B., Jaskóła K., Gąsiorek P., Meus M., Nowak K., Gaj M.D.. LEAFY COTYLEDON 2 (LEC2) promotes embryogenic induction in somatic tissues of Arabidopsis, via YUCCA-mediated auxin biosynthesis. Planta. 2013; 238(3): 425-440.
[115]
Santos Mendoza M., Dubreucq B., Miquel M., Caboche M., Lepiniec L.. LEAFY COTYLEDON 2 activation is sufficient to trigger the accumulation of oil and seed specific mRNAs in Arabidopsis leaves. FEBS Lett. 2005; 579(21): 4666-4670.
[116]
Xie W.W., Gao S., Wang S.H., Zhu J.Q., Xu Y., Tang L., . Cloning and expression analysis of carboxyltransferase of acetyl-coA carboxylase from Jatropha curcas. Z Naturforsch C. 2010; 65(1–2): 103-108.
[117]
Rolletschek H., Koch K., Wobus U., Borisjuk L.. Positional cues for the starch/lipid balance in maize kernels and resource partitioning to the embryo. Plant J. 2005; 42(1): 69-83.
[118]
El Tahchy A., Reynolds K.B., Petrie J.R., Singh S.P., Vanhercke T.. Thioesterase overexpression in Nicotiana benthamiana leaf increases the fatty acid flux into triacylgycerol. FEBS Lett. 2017; 591(2): 448-456.
[119]
Ohlrogge J., Browse J.. Lipid biosynthesis. Plant Cell. 1995; 7(7): 957-970.
[120]
Lin W., Oliver D.J.. Role of triacylglycerols in leaves. Plant Sci. 2008; 175(3): 233-237.
[121]
Lung S.C., Weselake R.J.. Diacylglycerol acyltransferase: a key mediator of plant triacylglycerol synthesis. Lipids. 2006; 41(12): 1073-1088.
[122]
Dyer J.M., Stymne S., Green A.G., Carlsson A.S.. High-value oils from plants. Plant J. 2008; 54(4): 640-655.
[123]
Kroon J.T., Wei W., Simon W.J., Slabas A.R.. 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. 2006; 67(23): 2541-2549.
[124]
Napier J.A.. The production of unusual fatty acids in transgenic plants. Annu Rev Plant Biol. 2007; 58(1): 295-319.
[125]
Bates P.D., Stymne S., Ohlrogge J.. Biochemical pathways in seed oil synthesis. Curr Opin Plant Biol. 2013; 16(3): 358-364.
[126]
Chi X., Hu R., Zhang X., Chen M., Chen N., Pan L., . Cloning and functional analysis of three diacylglycerol acyltransferase genes from peanut (Arachis hypogaea L.). PLoS One. 2014; 9(9): e105834.
[127]
Shockey J.M., Gidda S.K., Chapital D.C., Kuan J.C., Dhanoa P.K., Bland J.M., . Tung tree DGAT1 and DGAT2 have nonredundant functions in triacylglycerol biosynthesis and are localized to different subdomains of the endoplasmic reticulum. Plant Cell. 2006; 18(9): 2294-2313.
[128]
Li R., Yu K., Hildebrand D.F.. DGAT1, DGAT2 and PDAT expression in seeds and other tissues of epoxy and hydroxy fatty acid accumulating plants. Lipids. 2010; 45(2): 145-157.
[129]
Fan J., Yan C., Xu C.. Phospholipid:diacylglycerol acyltransferase-mediated triacylglycerol biosynthesis is crucial for protection against fatty acid-induced cell death in growing tissues of Arabidopsis. Plant J. 2013; 76(6): 930-942.
[130]
Yoon K., Han D., Li Y., Sommerfeld M., Hu Q.. 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(9): 3708-3724.
[131]
Higashi Y., Okazaki Y., Myouga F., Shinozaki K., Saito K.. Landscape of the lipidome and transcriptome under heat stress in Arabidopsis thaliana. Sci Rep. 2015; 5(1): 10533.
[132]
Bates P.D., Browse J.. The significance of different diacylgycerol synthesis pathways on plant oil composition and bioengineering. Front Plant Sci. 2012; 3: 147.
[133]
Jacquier N., Mishra S., Choudhary V., Schneiter R.. Expression of oleosin and perilipins in yeast promotes formation of lipid droplets from the endoplasmic reticulum. J Cell Sci. 2013; 126(Pt 22): 5198-5209.
[134]
Laibach N., Post J., Twyman R.M., Gronover C.S., Prüfer D.. The characteristics and potential applications of structural lipid droplet proteins in plants. J Biotechnol. 2015; 201: 15-27.
[135]
Dichlberger A., Kovanen P.T., Schneider W.J.. Mast cells: from lipid droplets to lipid mediators. Clin Sci (Lond). 2013; 125(3): 121-130.
[136]
Hsieh K., Huang A.H.. Lipid-rich tapetosomes in Brassica tapetum are composed of oleosin-coated oil droplets and vesicles, both assembled in and then detached from the endoplasmic reticulum. Plant J. 2005; 43(6): 889-899.
[137]
Siloto R.M., Findlay K., Lopez-Villalobos A., Yeung E.C., Nykiforuk C.L., Moloney M.M.. The accumulation of oleosins determines the size of seed oilbodies in Arabidopsis. Plant Cell. 2006; 18(8): 1961-1974.
[138]
Liu Q., Cao S., Zhou X.R., Wood C., Green A., Singh S.. Nonsense-mediated mRNA degradation of CtFAD2-1 and development of a perfect molecular marker for olol mutation in high oleic safflower (Carthamus tinctorius L.). Theor Appl Genet. 2013; 126(9): 2219-2231.
[139]
Winichayakul S., Scott R.W., Roldan M., Hatier J.H., Livingston S., Cookson R., . In vivo packaging of triacylglycerols enhances Arabidopsis leaf biomass and energy density. Plant Physiol. 2013; 162(2): 626-639.
[140]
Velázquez A.P., Tatsuta T., Ghillebert R., Drescher I., Graef M.. Lipid droplet-mediated ER homeostasis regulates autophagy and cell survival during starvation. J Cell Biol. 2016; 212(6): 621-631.
[141]
Lee J.H., Kong J., Jang J.Y., Han J.S., Ji Y., Lee J., . Lipid droplet protein LID-1 mediates ATGL-1-dependent lipolysis during fasting in Caenorhabditis elegans. Mol Cell Biol. 2014; 34(22): 4165-4176.
[142]
Moellering E.R., Benning C.. RNA interference silencing of a major lipid droplet protein affects lipid droplet size in Chlamydomonas reinhardtii. Eukaryot Cell. 2010; 9(1): 97-106.
[143]
Kim E.Y., Seo Y.S., Lee H., Kim W.T.. Constitutive expression of CaSRP1, a hot pepper small rubber particle protein homolog, resulted in fast growth and improved drought tolerance in transgenic Arabidopsis plants. Planta. 2010; 232(1): 71-83.
[144]
Eastmond P.J.. SUGAR-DEPENDENT1 encodes a patatin domain triacylglycerol lipase that initiates storage oil breakdown in germinating Arabidopsis seeds. Plant Cell. 2006; 18(3): 665-675.
[145]
Kelly A.A., Feussner I.. Oil is on the agenda: lipid turnover in higher plants. Biochim Biophys Acta. 2016; 1861(9 Pt B): 1253-1268.
[146]
Thazar-Poulot N., Miquel M., Fobis-Loisy I., Gaude T.. Peroxisome extensions deliver the Arabidopsis SDP1 lipase to oil bodies. Proc Natl Acad Sci USA. 2015; 112(13): 4158-4163.
[147]
Quettier A.L., Eastmond P.J.. Storage oil hydrolysis during early seedling growth. Plant Physiol Biochem. 2009; 47(6): 485-490.
[148]
Hernández M.L., Whitehead L., He Z., Gazda V., Gilday A., Kozhevnikova E., . A cytosolic acyltransferase contributes to triacylglycerol synthesis in sucrose-rescued Arabidopsis seed oil catabolism mutants. Plant Physiol. 2012; 160(1): 215-225.
[149]
Hsiao A.S., Haslam R.P., Michaelson L.V., Liao P., Napier J.A., Chye M.L.. Gene expression in plant lipid metabolism in Arabidopsis seedlings. PLoS One. 2014; 9(9): e107372.
[150]
Mach J.. Lipids in leaves: fatty acid β-oxidation affects lipid homeostasis. Plant Cell. 2014; 26(10): 3827.
[151]
Zolman B.K., Silva I.D., Bartel B.. The Arabidopsis pxa1 mutant is defective in an ATP-binding cassette transporter-like protein required for peroxisomal fatty acid β-oxidation. Plant Physiol. 2001; 127(3): 1266-1278.
[152]
Ghosh A.K., Chauhan N., Rajakumari S., Daum G., Rajasekharan R.. At4g24160, a soluble acyl-coenzyme A-dependent lysophosphatidic acid acyltransferase. Plant Physiol. 2009; 151(2): 869-881.
[153]
Baker A., Carrier D.J., Schaedler T., Waterham H.R., van Roermund C.W., Theodoulou F.L.. Peroxisomal ABC transporters: functions and mechanism. Biochem Soc Trans. 2015; 43(5): 959-965.
[154]
Theodoulou F.L., Eastmond P.J.. Seed storage oil catabolism: a story of give and take. Curr Opin Plant Biol. 2012; 15(3): 322-328.
[155]
Park S., Keereetaweep J., James C.N., Gidda S.K., Chapman K.D., Mullen R.T., . CGI-58, a key regulator of lipid homeostasis and signaling in plants, also regulates polyamine metabolism. Plant Signal Behav. 2014; 9(2): e27723.
[156]
Liu F., Zhao Q., Mano N., Ahmed Z., Nitschke F., Cai Y., . Modification of starch metabolism in transgenic Arabidopsis thaliana increases plant biomass and triples oilseed production. Plant Biotechnol J. 2016; 14(3): 976-985.
[157]
Dyer J., Yurchenko O., Park S., Gidda S., Cai Y., Shockey J., . Production of oil in plant vegetative tissues. FASEB J. 2015; 29(1): 485.2
[158]
Kromer K., Kreitschitz A., Kleinteich T., Gorb S.N., Szumny A.. Oil secretory system in vegetative organs of three Arnica taxa: essential oil synthesis, distribution and accumulation. Plant Cell Physiol. 2016; 57(5): 1020-1037.
[159]
Wood C.C., Petrie J.R., Shrestha P., Mansour M.P., Nichols P.D., Green A.G., . A leaf-based assay using interchangeable design principles to rapidly assemble multistep recombinant pathways. Plant Biotechnol J. 2009; 7(9): 914-924.
[160]
Li X., van Loo E.N., Gruber J., Fan J., Guan R., Frentzen M., . Development of ultra-high erucic acid oil in the industrial oil crop Crambe abyssinica. Plant Biotechnol J. 2012; 10(7): 862-870.
[161]
Chen Y., Cui Q., Xu Y., Yang S., Gao M., Wang Y.. Effects of tung oilseed FAD2 and DGAT2 genes on unsaturated fatty acid accumulation in Rhodotorula glutinis and Arabidopsis thaliana. Mol Genet Genomics. 2015; 290(4): 1605-1613.
[162]
Van Erp H., Kelly A.A., Menard G., Eastmond P.J.. Multigene engineering of triacylglycerol metabolism boosts seed oil content in Arabidopsis. Plant Physiol. 2014; 165(1): 30-36.
[163]
Zaheer K., Akhtar M.H.. Potato production, usage, and nutrition—a review. Crit Rev Food Sci Nutr. 2016; 56(5): 711-721.
[164]
Athenstaedt K., Daum G.. The life cycle of neutral lipids: synthesis, storage and degradation. Cell Mol Life Sci. 2006; 63(12): 1355-1369.
[165]
Ricroch A.E., Bergé J.B., Kuntz M.. Evaluation of genetically engineered crops using transcriptomic, proteomic, and metabolomic profiling techniques. Plant Physiol. 2011; 155(4): 1752-1761.
[166]
Séralini G.E., Mesnage R., Clair E., Gress S., de Vendômois J.S., Cellier D.. Genetically modified crops safety assessments: present limits and possible improvements. Environ Sci Eur. 2011; 23: 10.
[167]
Domingo J.L., Giné Bordonaba J.. A literature review on the safety assessment of genetically modified plants. Environ Int. 2011; 37(4): 734-742.
[168]
Juven-Gershon T., Kadonaga J.T.. Regulation of gene expression via the core promoter and the basal transcriptional machinery. Dev Biol. 2010; 339(2): 225-229.
[169]
Doherty C.J., Kay S.A.. Circadian control of global gene expression patterns. Annu Rev Genet. 2010; 44: 419-444.
[170]
Troncoso-Ponce M.A., Cao X., Yang Z., Ohlrogge J.B.. Lipid turnover during senescence. Plant Sci. 2013; 205–206:
[171]
Leshem Y.Y.. Plant senescence processes and free radicals. Free Radic Biol Med. 1988; 5(1): 39-49.
[172]
Thompson J.E., Froese C.D., Madey E., Smith M.D., Hong Y.. Lipid metabolism during plant senescence. Prog Lipid Res. 1998; 37(2–3): 119-141.
[173]
Xie Q., Michaeli S., Peled-Zehavi H., Galili G.. Chloroplast degradation: one organelle, multiple degradation pathways. Trends Plant Sci. 2015; 20(5): 264-265.
[174]
Thomas H., Stoddart J.L.. Leaf senescence. Annu Rev Plant Physiol. 1980; 31: 83-111.
[175]
Branham S.E., Wright S.J., Reba A., Linder C.R.. Genome-wide association study of Arabidopsis thaliana identifies determinants of natural variation in seed oil composition. J Hered. 2016; 107(3): 248-256.
[176]
Divi U.K., Zhou X.R., Wang P., Butlin J., Zhang D.M., Liu Q., . Deep sequencing of the fruit transcriptome and lipid accumulation in a non-seed tissue of Chinese tallow, a potential biofuel crop. Plant Cell Physiol. 2016; 57(1): 125-137.
[177]
Mitchell M., Pritchard J., Okada S., Larroque O., Yulia D., Pettolino F., . Oil accumulation in transgenic potato tubers alters starch quality and nutritional profile. Front Plant Sci. 2017; 8: 554.
[178]
Vigeolas H., Waldeck P., Zank T., Geigenberger P.. Increasing seed oil content in oil-seed rape (Brassica napus L.) by over-expression of a yeast glycerol-3-phosphate dehydrogenase under the control of a seed-specific promoter. Plant Biotechnol J. 2007; 5(3): 431-441.
[179]
Waterhouse P.M., Graham M.W., Wang M.B.. Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA. Proc Natl Acad Sci USA. 1998; 95(23): 13959-13964.
[180]
Andrianov V., Borisjuk N., Pogrebnyak N., Brinker A., Dixon J., Spitsin S., . 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(3): 277-287.
[181]
James C.N., Horn P.J., Case C.R., Gidda S.K., Zhang D., Mullen R.T., . Disruption of the Arabidopsis CGI-58 homologue produces Chanarin-Dorfman-like lipid droplet accumulation in plants. Proc Natl Acad Sci USA. 2010; 107(41): 17833-17838.
[182]
Hong Y., Zhang W., Wang X.. Phospholipase D and phosphatidic acid signalling in plant response to drought and salinity. Plant Cell Environ. 2010; 33(4): 627-635.
[183]
Li M., Hong Y., Wang X.. Phospholipase D- and phosphatidic acid-mediated signaling in plants. Biochim Biophys Acta. 2009; 1791(9): 927-935.
[184]
Schillberg S., Twyman R.M., Fischer R.. Opportunities for recombinant antigen and antibody expression in transgenic plants—technology assessment. Vaccine. 2005; 23(15): 1764-1769.
[185]
Parrott W., Chassy B., Ligon J., Meyer L., Petrick J., Zhou J., . Application of food and feed safety assessment principles to evaluate transgenic approaches to gene modulation in crops. Food Chem Toxicol. 2010; 48(7): 1773-1790.
[186]
Dwivedi S.L., Britt A.B., Tripathi L., Sharma S., Upadhyaya H.D., Ortiz R.. Haploids: constraints and opportunities in plant breeding. Biotechnol Adv. 2015; 33(6 Pt 1): 812-829.
[187]
Rugini E., Cristofori V., Silvestri C.. Genetic improvement of olive (Olea europaea L.) by conventional and in vitro biotechnology methods. Biotechnol Adv. 2016; 34(5): 687-696.
[188]
Fan J., Yu L., Xu C.. A central role for triacylglycerol in membrane lipid breakdown, fatty acid β-oxidation, and plant survial under extended darkness. Plant Physiol. 2017; 174(3): 1517-1530.
Acknowledgements

Xiao-Yu Xu wishes to thank the China Scholarship Council (CSC) for financial support.

Compliance with ethics guidelines

Xiao-Yu Xu, Hong-Kun Yang, Surinder P. Singh, Peter J. Sharp, and Qing Liu declare that they have no conflict of interest or financial conflicts to disclose.

AI Summary AI Mindmap
PDF(1066 KB)

Accesses

Citations

Detail

Sections
Recommended

/