Abstract
Microalgae have gained the attention of the scientific community, particularly lipid biochemists and microalgal biotechnologists, as a source of valuable nutritional ingredients, such as long-chain polyunsaturated fatty acids (LC-PUFA) and carotenoids, as well as precursors for biodiesel production. The field of microalgal lipids, particularly with respect to the identification of gene functions and the regulation of lipid biosynthetic pathways, is in its infancy. However, a wealth of biochemical and physiological data had been previously acquired. The last few years have witnessed substantial progress toward understanding the biochemical reactions of lipid biosynthesis in microalgae, supported by comprehensive knowledge acquired in the field of plant lipid biochemistry, as well as immense systems biology studies. Intensive investigations focusing on the biochemistry and enzymology of triacylglycerol formation in microalgal cells have already revealed some novel gene functions and cellular features, indicating that lipid metabolism in microalgae might differ in some aspects from that in higher plants. A better understanding of the remarkable diversity, complex evolutionary history and ecological distribution of microalgae would further accelerate functional genomic studies of model and non-model species and shed more light on their versatile lipid biosynthesis pathways. Recent advances in the genetic transformation as well as in genome-editing technologies, now permit the genomes of microalgae to be manipulated in order to expand their use in biotechnology. A thorough understanding of the lipid biosynthetic pathways in different groups of microalgae is a prerequisite for the genetic engineering of microalgae toward enhanced lipid production and modifications in fatty acid composition.
This chapter covers the biochemistry and physiology of lipid metabolism in microalgae. It summarizes the current knowledge in the field acquired over the last two decades, noting some of the earlier seminal works. The first aspect to be covered is the diversity of fatty acid and lipid classes in microalgae; next, the major lipid biosynthesis routes and pathways of fatty acid modification are outlined. In the last part of the chapter, we address the effects of environmental and nutritional factors, as well as stressful conditions, on lipid metabolism in microalgae.
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Notes
- 1.
Wherever possible the currently accepted names for species are used. The name used in the paper cited is also indicated. For details of names see chapter “Systematics, Taxonomy and Species Names: Do They Matter?” of this book (Borowitzka 2016).
References
Abbadi A, Domergue F, Bauer J, Napier JA, Welti R, Zahringer U, Cirpus P, Heinz E (2004) Biosynthesis of very-long-chain polyunsaturated fatty acids in transgenic oilseeds: constraints on their accumulation. Plant Cell 16:2734–2748
Abida H, Dolch LJ, Meï C, Villanova V, Conte M et al (2015) Membrane glycerolipid remodeling triggered by nitrogen and phosphorus starvation in Phaeodactylum tricornutum. Plant Physiol 167:118–136
Abida H, Dolch LJ, Meï C, Villanova V, Conte M, Block MA, Finazzi G, Bastien O, Tirichine L, Bowler C, Rébeillé F, Petroutsos D, Jouhet J, Maréchal E (2015) Membrane glycerolipid remodeling triggered by nitrogen and phosphorus starvation in Phaeodactylum tricornutum. Plant Physiol 167:118–136
Adeyo O, Horn PJ, Lee S, Binns DD, Chandrahas A, Chapman KD, Goodman JM (2011) The yeast lipin orthologue Pah1p is important for biogenesis of lipid droplets. J Cell Biol 192:1043–1055
Adlerstein D, Bigogno C, Khozin I, Cohen Z (1997) The effect of growth temperature and culture density on the molecular species composition of the galactolipids in the red microalga Porphyridium cruentum (Rhodophyta). J Phycol 33:975–979
Andersson MX, Stridh MH, Larsson KE, Lijenberg C, Sandelius AS (2003) Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol. FEBS Lett 5378:128–132
Andersson MX, Kjellberg JM, Sandelius AS (2004) The involvement of cytosolic lipases in converting phosphatidyl choline to substrate for galactolipid synthesis in the chloroplast envelope. Biochim Biophys Acta 1684:46–53
Andersson MX, Larsson KE, Tjellström H, Liljenberg C, Sandelius AS (2005) Phosphate-limited oat. The plasma membrane and the tonoplast as major targets for phospholipid-to-glycolipid replacement and stimulation of phospholipases in the plasma membrane. J Biol Chem 2808:27578–27586
Andre C, Froehlich JE, Moll MR, Benning C (2007) A heteromeric plastidic pyruvate kinase complex involved in seed oil biosynthesis in Arabidopsis. Plant Cell 19:2006–2022
Andre C, Haslam RP, Shanklin J (2012) Feedback regulation of plastidic acetyl-CoA carboxylase by 18:1-acyl carrier protein in Brassica napus. Proc Natl Acad Sci U S A 109:10107–10112
Andrews J, Ohlrogge JB, Keegstra K (1985) Final step of phosphatidic acid synthesis in pea chloroplasts occurs in the inner envelope membrane. Plant Physiol 78:459–465
Andrianov V, Borisjuk N, Pogrebnyak N, Brinker A, Dixon J, Spitsin S, Flynn J, Matyszczuk P, Andryszak K, Laurelli M, Golovkin M, Koprowski H (2010) 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 8:277–287
Aoki M, Tsuzuki M, Sato N (2012) Involvement of sulfoquinovosyl diacylglycerol in DNA synthesis in Synechocystis sp. PCC 6803. BMC Res Notes 5:98
Araki S, Eichenberger W, Sakurai T, Sato N (1991) Distribution of diacylglyceryl-hydroxymethyltrimethyl-β-alanine (DGTA) and phosphatidylcholine in brown algae. Plant Cell Physiol 32:623–628
Arao T, Sakaki T, Yamada M (1994) Biosynthesis of polyunsaturated lipids in the diatom, Phaeodactylum tricornutum. Phytochemistry 36:629–635
Arisz SA, van Himbergen JA, Musgrave A, van den Ende H, Munnik T (2000) Polar glycerolipids of Chlamydomonas moewusii. Phytochemistry 53:265–270
Armada I, Hachero-Cruzado I, Mazuelos N, Ríos JL, Manchado M, Cañavate JP (2013) Differences in betaine lipids and fatty acids between Pseudoisochrysis paradoxa VLP and Diacronema vlkianum VLP isolates (Haptophyta). Phytochemistry 95:224–33
Aronsson H, Schöttler MA, Kelly AA, Sundqvist C, Dörmann P, Karim S, Jarvis P (2008) Monogalactosyldiacylglycerol deficiency in Arabidopsis affects pigment composition in the prolamellar body and impairs thylakoid membrane energization and photoprotection in leaves. Plant Physiol 148:580–592
Atteia A, van Lis R, Gelius-Dietrich G, Adrait A, Garin J, Joyard J, Rolland N, Martin W (2006) Pyruvate formate-lyase and a novel route of eukaryotic ATP synthesis in Chlamydomonas mitochondria. J Biol Chem 281:9909–9918
Avidan O, Brandis A, Rogachev I, Pick U (2015) Enhanced acetyl-CoA production is associated with increased triglyceride accumulation in the green alga Chlorella desiccata. J Exp Bot 66:3725–3735
Awai K, Maréchal E, Block MA, Brun D, Masuda T, Shimada H, Takamiya K, Ohta H, Joyard J (2001) Two types of MGDG synthase genes, found widely in both 16:3 and 18:3 plants, differentially mediate galactolipid syntheses in photosynthetic and nonphotosynthetic tissues in Arabidopsis thaliana. Proc Natl Acad Sci U S A 98:10960–10965
Awai K, Kakimoto T, Awai C, Kaneko T, Nakamura Y, Takamiya K, Wada H, Ohta H (2006) Comparative genomic analysis revealed a gene for monoglucosyldiacylglycerol synthase, an enzyme for photosynthetic membrane lipid synthesis in cyanobacteria. Plant Physiol 141:1120–1127
Baba M, Ioki M, Nakajima N, Shiraiwa Y, Watanabe M (2012) Transcriptome analysis of an oil-rich race A strain of Botryococcus braunii (BOT-88-2) by de novo assembly of pyrosequencing cDNA reads. Bioresour Technol 109:282–286
Babiychuk E, Müller F, Eubel H, Braun HP, Frentzen M, Kushnir S (2003) Arabidopsis phosphatidylglycerophosphate synthase 1 is essential for chloroplast differentiation, but is dispensable for mitochondrial function. Plant J 33:899–909
Banaś A, Dahlqvist A, Ståhl U, Lenman M, Stymne S (2000) The involvement of phospholipid: diacylglycerol acyltransferases in triacylglycerol production. Biochem Soc Trans 28:703–705
Banskota AH, Stefanova R, Gallant P, McGinn PJ (2013a) Mono- and digalactosyldiacylglycerols: potent nitric oxide inhibitors from the marine microalga Nannochloropsis granulata. J Appl Phycol 25:349–357
Banskota AH, Stefanova R, Gallant P, McGinn PJ (2013b) Nitric oxide inhibitory activity of monogalactosylmonoacylglycerols from a freshwater microalgae Chlorella sorokiniana. Nat Prod Res 27:1028–1031
Bates PD, Browse J (2012) The significance of different diacylgycerol synthesis pathways on plant oil composition and bioengineering. Front Plant Sci 3:147. doi:10.3389/fpls.2012.00147/fpls.2012.00147
Bates PD, Durrett TP, Ohlrogge JB, Pollard M (2009) Analysis of acyl fluxes through multiple pathways of triacylglycerol synthesis in developing soybean embryos. Plant Physiol 150:55–72
Bates PD, Stymne S, Ohlrogge J (2013) Biochemical pathways in seed oil synthesis. Curr Opin Plant Biol 16:358–364
Baud S, Lepiniec L (2010) Physiological and developmental regulation of seed oil production. Prog Lipid Res 49:235–249
Baud S, Guyon V, Kronenberger J, Wuillème S, Miquel M, Caboche M, Lepiniec L, Rochat C (2003) Multifunctional acetyl-CoA carboxylase 1 is essential for very long chain fatty acid elongation and embryo development in Arabidopsis. Plant J 33:75–86
Baud S, Wuillème S, Dubreucq B, de Almeida A, Vuagnat C, Lepiniec L, Miquel M, Rochat C (2007) Function of plastidial pyruvate kinases in seeds of Arabidopsis thaliana. Plant J 52:405–419
Beer LL, Boyd ES, Peters JW, Posewitz MC (2009) Engineering algae for biohydrogen and biofuel production. Curr Opin Biotechnol 20:264–271
Beller M, Thiel K, Thul PJ, Jäckle H (2010) Lipid droplets: a dynamic organelle moves into focus. FEBS Lett 584:2176–2182
Benemann JR (1992) Microalgae aquaculture feeds. J Appl Phycol 4:233–245
Benning C (1998) Biosynthesis and function of the sulfolipid sulfoquinovosyl diacylglycerol. Annu Rev Plant Physiol Plant Mol Biol 49:53–75
Benning C (2009) Mechanisms of lipid transport involved in organelle biogenesis in plant cells. Annu Rev Cell Dev Biol 25:71–91
Benning C, Ohta H (2005) Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. J Biol Chem 280:2397–2400
Benning C, Beatty JT, Prince RC, Somerville CR (1993) The sulfolipid sulfoquinovosyldiacylglycerol is not required for photosynthetic electron transport in Rhodobacter sphaeroides but enhances growth under phosphate limitation. Proc Natl Acad Sci U S A 90:1561–1565
Bhattacharya D, Price DC, Chan CX, Qiu H, Rose N, Ball S, Weber AP, Arias MC, Henrissat B, Coutinho PM, Krishnan A, Zäuner S, Morath S, Hilliou F, Egizi A, Perrineau MM, Yoon HS (2013) Genome of the red alga Porphyridium purpureum. Nat Commun 4:1941. doi:10.1038/ncomms2931
Bickel PE, Tansey JT, Welte MA (2009) PAT proteins, an ancient family of lipid droplet proteins that regulate cellular lipid stores. Biochim Biophys Acta 1791:419–440
Biester EM, Hellenbrand J, Frentzen M (2012) Multifunctional acyltransferases from Tetrahymena thermophila. Lipids 47:371–381
Bigogno C, Khozin-Goldberg I, Adlerstein D, Cohen Z (2002a) Biosynthesis of arachidonic acid in the oleaginous microalga Parietochloris incisa (Chlorophyceae): radiolabeling studies. Lipids 37:209–216
Bigogno C, Khozin-Goldberg I, Boussiba S, Vonshak A, Cohen Z (2002b) Lipid and fatty acid composition of the green alga Parietochloris incisa, the richest plant source of arachidonic acid. Phytochemistry 60:497–503
Bigogno C, Khozin-Goldberg I, Cohen Z (2002c) Accumulation of arachidonic acid and triacylglycerols in the microalga Parietochloris incisa (Trebuxiophyceae, Chlorophyta). Phytochemistry 60:135–143
Blaby IK, Glaesener AG, Mettler T, Fitz-Gibbon ST, Gallaher SD, Liu B, Boyle NR, Kropat J, Stitt M, Johnson S, Benning C, Pellegrini M, Casero D, Merchant SS (2013) Systems-level analysis of nitrogen starvation-induced modifications of carbon metabolism in a Chlamydomonas reinhardtii starchless mutant. Plant Cell 25:4305–4423
Blanchette-Mackie EJ, Dwyer NK, Barber T, Coxey RA, Takeda T, Rondinone CM, Theodorakis JL, Greenberg AS, Londos C (1995) Perilipin is located on the surface layer of intracellular lipid droplets in adipocytes. J Lipid Res 36:1211–1226
Blatti JL, Beld J, Behnke CA, Mendez M, Mayfield SP, Burkart MD (2012) Manipulating fatty acid biosynthesis in microalgae for biofuel through protein-protein interactions. PLoS One 7(9):e42949
Block MA, Dorne AJ, Joyard J, Douce R (1983) Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. II. Biochemical characterization. J Biol Chem 258:13281–13286
Block MA, Douce R, Joyard J, Rolland N (2007) Chloroplast envelope membranes: a dynamic interface between plastids and the cytosol. Photosynth Res 92:225–244
Bogen C, Al-Dilaimi A, Albersmeier A, Wichmann J, Grundmann M, Rupp O, Lauersen KJ, Blifernez-Klassen O, Kalinowski J, Goesmann A, Mussgnug JH, Kruse O (2013) Reconstruction of the lipid metabolism for the microalga Monoraphidium neglectum from its genome sequence reveals characteristics suitable for biofuel production. BMC Genomics 14(1):926
Bogos B, Ughy B, Domonkos I, Laczkó-Dobos H, Komenda J, Abasova L, Cser K, Vass I, Sallai A, Wada H, Gombos Z (2010) Phosphatidylglycerol depletion affects photosystem II activity in Synechococcus sp. PCC 7942 cells. Photosynth Res 103(1):9–30
Bohne AV, Schwarz C, Schottkowski M, Lidschreiber M, Piotrowski M, Zerges W, Nickelsen J (2013) Reciprocal regulation of protein synthesis and carbon metabolism for thylakoid membrane biogenesis. PLoS Biol 11(2):e1001482
Bonaventure G, Salas JJ, Pollard MR, Ohlrogge JB (2003) Disruption of the FATB gene in Arabidopsis demonstrates an essential role of saturated fatty acids in plant growth. Plant Cell 15:1020–1033
Bonaventure G, Bao X, Ohlrogge J, Pollard M (2004) Metabolic responses to the reduction in palmitate caused by disruption of the FATB gene in Arabidopsis. Plant Physiol 135:1269–1279
Borowitzka MA (1988) Microalgae as sources of pharmaceuticals and other biologically active compounds. J Appl Phycol 4:267–279
Borowitzka MA (2016) Systematics, taxonomy and species names: do they matter? In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae. Springer, Dordrecht, pp 655–681
Botté CY, Yamaryo-Botté Y, Janouskovec J, Rupasinghe T, Keeling PJ, Crellin P, Coppel RL, Maréchal E, McConville MJ, McFadden GI (2011) Identification of plant-like galactolipids in Chromera velia, a photosynthetic relative of malaria parasites. J Biol Chem 286:29893–29903
Boussiba S (2000) Carotenogenesis in the green alga Haematococcus pluvialis. Physiol Plant 108:111–117
Bouvier-Navé P, Benveniste P, Oelkers P, Sturley SL, Schaller H (2000) Expression in yeast and tobacco of plant cDNAs encoding acyl CoA: diacylglycerol acyltransferase. Eur J Biochem 267:85–96
Boyle NR, Page MD, Liu B, Blaby IK, Casero D, Kropat J, Cokus SJ, Hong-Hermesdorf A, Shaw J, Karpowicz SJ, Gallaher SD, Johnson S, Benning C, Pellegrini M, Grossman A, Merchant SS (2012) Three acyltransferases and nitrogen-responsive regulator are implicated in nitrogen starvation-induced triacylglycerol accumulation in Chlamydomonas. J Biol Chem 287:15811–15825
Breuers FKH, Bräutigam A, Weber APM (2011) The plastid outer envelope – a highly dynamic interface between plastid and cytoplasm. Front Plant Sci 2:97. doi:10.3389/fpls.2011.00097
Bromke MA, Giavalisco P, Willmitzer L, Hesse H (2013) Metabolic analysis of adaptation to short-term changes in culture conditions of the marine diatom Thalassiosira pseudonana. PLoS One 8(6):e67340
Burgal J, Shockey J, Lu CF, Dyer J, Larson T, Graham I, Browse J (2008) Metabolic engineering of hydroxy fatty acid production in plants: RcDGAT2 drives dramatic increases in ricinoleate levels in seed oil. Plant Biotechnol J 6:819–831
Cai M, He LH, Yu TY (2013) Molecular clone and expression of a NAD+-dependent glycerol-3-phosphate dehydrogenase isozyme gene from the halotolerant alga Dunaliella salina. PLoS One 8(4):e62287
Cao J, Hawkins E, Brozinick J, Liu X, Zhang H, Burn P, Shi Y (2004) A predominant role of acyl-CoA: monoacylglycerol acyltransferase-2 in dietary fat absorption implicated by tissue distribution, subcellular localization, and up-regulation by high fat diet. J Biol Chem 279:18878–18886
Cao J, Li JL, Li D, Tobin JF, Gimeno RE (2006) Molecular identification of microsomal acyl-CoA: glycerol-3-phosphate acyltransferase, a key enzyme in de novo triacylglycerol synthesis. Proc Natl Acad Sci U S A 103:19695–19700
Carman GM, Han GS (2011) Regulation of phospholipid synthesis in the yeast Saccharomyces cerevisiae. Annu Rev Biochem 80:859–883
Cases S, Smith SJ, Zheng YW, Myers HM, Lear SR, Sande E, Novak S, Collins C, Welch CB, Lusis AJ, Erickson SK, Farese RV Jr (1998) Identification of a gene encoding an acyl CoA: diacylglycerol acyltransferase, a key enzyme in triacylglycerol synthesis. Proc Natl Acad Sci U S A 95:13018–13023
Cases S, Stone SJ, Zhou P, Yen E, Tow B, Lardizabal KD, Voelker T, Farese RV Jr (2001) Cloning of DGAT2, a second mammalian diacylglycerol acyltransferase, and related family members. J Biol Chem 276:38870–38876
Catalanotti C, Dubini A, Subramanian V, Yang W, Magneschi L, Mus F, Seibert M, Posewitz MC, Grossman AR (2012) Altered fermentative metabolism in Chlamydomonas reinhardtii mutants lacking pyruvate formate lyase and both pyruvate formate lyase and alcohol dehydrogenase. Plant Cell 24:692–707
Catalanotti C, Yang W, Posewitz MC, Grossman AR (2013) Fermentation metabolism and its evolution in algae. Front Plant Sci 4:150
Chang CW, Moseley JL, Wykoff D, Grossman AR (2005) The LPB1 gene is important for acclimation of Chlamydomonas reinhardtii to phosphorus and sulfur deprivation. Plant Physiol 138:319–329
Chapman KD, Ohlrogge JB (2012) Compartmentation of triacylglycerol accumulation in plants. J Biol Chem 287:2288–2294
Chapman KD, Dyer JM, Mullen RT (2012) Biogenesis and functions of lipid droplets in plants: thematic review series: lipid droplet synthesis and metabolism: from yeast to man. J Lipid Res 53:215–226
Chapman KD, Dyer JM, Mullen RT (2013) Commentary: why don’t plant leaves get fat? Plant Sci 207:128–134
Chaturvedi R, Uppalapati S, Alamsjah M, Fujita Y (2004) Isolation of quizalofop-resistant mutants of Nannochloropsis oculata (Eustigmatophyceae) with high eicosapentaenoic acid following N-methyl-N-nitrosourea-induced random mutagenesis. J Appl Phycol 16:135–144
Chen JE, Smith AG (2012) A look at diacylglycerol acyltransferases (DGATs) in algae. J Biotechnol 162:28–39
Chen H, Kim HU, Weng H, Browse J (2011) Malonyl-CoA synthetase, encoded by ACYL ACTIVATING ENZYME13, is essential for growth and development of Arabidopsis. Plant Cell 23:2247–2262
Chen Y, Chi HY, Meesapyodsuk D, Qiu X (2013) Phytophthora infestans cholinephosphotransferase with substrate specificity for very-long-chain polyunsaturated fatty acids. Appl Environ Microbiol 79:1573–1579
Cohen Z (1999) Production of polyunsaturated fatty acids by the microalga Porphyridium cruentum. In: Cohen Z (ed) Production of chemicals by microalgae. Taylor and Francis, London, pp 1–24
Cohen Z, Khozin-Goldberg I (2005) Searching for PUFA-rich microalgae. In: Cohen Z, Ratledge C (eds) Single cell oils. Amer Oil Chemistry Society, Champaign, pp 53–72
Cohen Z, Didi S, Heimer YM (1992) Overproduction of γ-linolenic and eicosapentaenoic acids by algae. Plant Physiol 98:569–572
Cohen Z, Margheri MC, Tomaselli L (1995) Chemotaxonomy of cyanobacteria. Phytochemistry 40:1155–1158
Cohen Z, Khozin-Goldberg I, Adlerstein D, Bigogno C (2000) The role of triacylglycerol as a reservoir of polyunsaturated fatty acids for the rapid production of chloroplastic lipids in certain microalgae. Biochem Soc Trans 28:740–743
Corteggiani Carpinelli E, Telatin A, Vitulo N, Forcato C, D’Angelo M, Schiavon R, Vezzi A, Giacometti GM, Morosinotto T, Valle G (2014) Chromosome scale genome assembly and transcriptome profiling of Nannochloropsis gaditana in nitrogen depletion. Mol Plant 7:323–335
Csaki LS, Reue K (2010) Lipins: multifunctional lipid metabolism proteins. Annu Rev Nutr 30:257–272
Cui Y, Zheng G, Li X, Lin H, Jiang P, Qin S (2013) Cloning and characterization of a novel diacylglycerol acyltransferase from the diatom Phaeodactylum tricornutum. J Appl Phycol 25:1509–1512
Daboussi F, Leduc S, Maréchal A, Dubois G, Guyot V, Perez-Michaut C, Amato A, Falciatore A, Juillerat A, Beurdeley M, Voytas DF, Cavarec L, Duchateau P (2014) Genome engineering empowers the diatom Phaeodactylum tricornutum for biotechnology. Nat Commun 5:3831. doi:10.1038/ncomms4831
Dahlqvist A, Stahl U, Lenman M, Banas A, Lee M, Sandager L, Ronne H, Stymne S (2000) Phospholipid: diacylglycerol acyltransferase: an enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants. Proc Natl Acad Sci U S A 97:6487–6492
Dahmen JL, Khadka M, Dodson VJ, Leblond JD (2013) Mono- and digalactosyldiacylglycerol composition of dinoflagellates. VI. Biochemical and genomic comparison of galactolipid biosynthesis between Chromera velia (Chromerida), a photosynthetic alveolate with red algal plastid ancestry, and the dinoflagellate, Lingulodinium polyedrum. Eur J Phycol 48:268–277
Danielewicz MA, Anderson LA, Franz AK (2011) Triacylglycerol profiling of marine microalgae by mass spectrometry. J Lipid Res 52:2101–2108
Daum G, Wagner A, Czabany T, Athenstaedt K (2007) Dynamics of neutral lipid storage and mobilization in yeast. Biochimie 89:243–248
Davidi L, Katz A, Pick U (2012) Characterization of major lipid droplet proteins from Dunaliella. Planta 236:19–33
Davidi L, Shimoni E, Khozin-Goldberg I, Zamir A, Pick U (2014) Origin of β-carotene-rich plastoglobuli in Dunaliella bardawil. Plant Physiol 164:2139–2156
Davidi L, Levin Y, Ben-Dor S, Pick U (2015) Proteome analysis of cytoplasmatic and plastidic β-carotene lipid droplets in Dunaliella bardawil. Plant Physiol 167:60–79
Davies JP, Yildiz F, Grossman AR (1994) Mutants of Chlamydomonas with aberrant responses to sulfur deprivation. Plant Cell 6:53–63
Davies JP, Yildiz FH, Grossman AR (1996) Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. EMBO J 15:2150–2159
de Souza LM, Sassaki GL, Romanos MTV, Barreto-Bergter E (2012) Structural characterization and anti-HSV-1 and HSV-2 activity of glycolipids from the marine algae Osmundaria obtusiloba isolated from southeastern Brazilian coast. Mar Drugs 10:918–931
Dembitsky VM (1996) Betaine ether-linked glycerolipids: chemistry and biology. Prog Lipid Res 35:1–51
Dembitsky VM, Levitsky DO (2004) Arsenolipids. Prog Lipid Res 43:403–448
Dembitsky VM, Srebnik M (2002) Natural halogenated fatty acids: their analogues and derivatives. Prog Lipid Res 41:315–367
Deng XD, Gu B, Li YJ, Hu XW, Guo JC, Fei XW (2012) The roles of acyl-CoA: diacylglycerol acyltransferase 2 genes in the biosynthesis of triacylglycerols by the green algae Chlamydomonas reinhardtii. Mol Plant 5:945–947
Dichlberger A, Kovanen PT, Schneider WJ (2013) Mast cells: from lipid droplets to lipid mediators. Clin Sci (Lond) 125(3):121–30
Ding Y, Yang L, Zhang S, Wang Y, Du Y, Pu J, Peng G, Chen Y, Zhang H, Yu J, Hang H, Wu P, Yang F, Yang H, Steinbüchel A, Liu P (2012) Identification of the major functional proteins of prokaryotic lipid droplets. J Lipid Res 53:399–411
Dodson VJ, Dahmen JL, Mouget JL, Leblond JD (2013) Mono- and digalactosyldiacylglycerol composition of the marennine-producing diatom, Haslea ostrearia: comparison to a selection of pennate and centric diatoms. Phycol Res 61:199–207
Dolch LJ, Maréchal E (2015) Inventory of fatty acid desaturases in the pennate diatom Phaeodactylum tricornutum. Mar Drugs 13:1317–1339
Domergue F, Lerchl J, Zähringer U, Heinz E (2002) Cloning and functional characterization of Phaeodactylum tricornutum front-end desaturases involved in eicosapentaenoic acid biosynthesis. Eur J Biochem 269:4105–4113
Domergue F, Spiekermann P, Lerchl J, Beckmann C, Kilian O, Kroth PG, Boland W, Zähringer U, Heinz E (2003) New insight into Phaeodactylum tricornutum fatty acid metabolism: cloning and functional characterization of plastidial and microsomal ∆12-fatty acid desaturases. Plant Physiol 131:1648–1660
Domergue F, Abbadi A, Zähringer U, Moreau H, Heinz E (2005) In vivo characterization of the first acyl-CoA Δ6-desaturase from a member of the plant kingdom, the microalga Ostreococcus tauri. Biochem J 389:483–490
Dong HP, Williams E, Wang DZ, Xie ZX, Hsia RC, Jenck A, Halden R, Li J, Chen F, Place AR (2013) Responses of Nannochloropsis oceanica IMET1 to long-term nitrogen starvation and recovery. Plant Physiol 162:1110–1126
Dörmann P (2005) Membrane lipids. In: Murphy D (ed) Plant lipids. Biology, utilization and manipulation. CRC Press, Boca Raton, pp 123–160
Dörmann P, Benning C (2002) Galactolipids rule in seed plants. Trends Plant Sci 7:112–118
Dörmann P, Heinz E (2011) 50 years of galactolipid research: the beginnings. Retrieved from http://www.lipidlibrary.aocs.org
Dörmann P, Kridl JC, Ohlrogge JB (1994) Cloning and expression in Escherichia coli of a cDNA coding for the oleoyl-acyl carrier protein thioesterase from coriander (Coriandrum sativum L.). Biochim Biophys Acta 1212:134–136
Dörmann P, Balbo I, Benning C (1999) Arabidopsis galactolipid biosynthesis and lipid trafficking mediated by DGD1. Science 284:2181–2184
Dubertret G, Gerard-Hirne C, Trémolières A (2002) Importance of trans-Δ3-hexadecenoic acid containing phosphatidylglycerol in the formation of the trimeric light-harvesting complex in Chlamydomonas. Plant Physiol Biochem 40:829–836
Dunstan GA, Volkman JK, Jeffrey SW, Barrett SM (1992) Biochemical composition of microalgae from the green algal classes Chlorophyceae and Prasinophyceae 2. Lipid classes and fatty acids. J Exp Mar Biol Ecol 161:115–134
Durrett TP, McClosky DD, Tumaney AW, Elzinga DA, Ohlrogge J, Pollard M (2010) A distinct DGAT with sn-3 acetyltransferase activity that synthesizes unusual, reduced-viscosity oils in Euonymus and transgenic seeds. Proc Natl Acad Sci U S A 107:9464–9469
Dyhrman ST, Jenkins BD, Rynearson TA, Saito MA, Mercier ML et al (2012) The transcriptome and proteome of the diatom Thalassiosira pseudonana reveal a diverse phosphorus stress response. PLoS One 7(3):e33768
Eastmond PJ, Quettier AL, Kroon JT, Craddock C, Adams N, Slabas AR (2010) Phosphatidic acid phosphohydrolase 1 and 2 regulate phospholipid synthesis at the endoplasmic reticulum in Arabidopsis. Plant Cell 22:2796–2811
Eichenberger W (1993) Betaine lipids in lower plants: distribution of DGTS, DGTA and phospholipids, and the intracellular localization and site of biosynthesis of DGTS. Plant Physiol Biochem 31:213–221
Eichenberger W, Gribi C (1997) Lipids of Pavlova lutheri (Haptophyceae): cellular site and metabolic role of DGCC. Phytochemistry 45:1561–1567
Eichenberger W, Gribi C, Gfeller H, Grey P, Henderson RJ (1996) Gas chromatographic-mass spectrometric identification of betaine lipids in Chroomonas salina. Phytochemistry 42:967–972
Eltgroth ML, Watwood RL, Wolfe GV (2005) Production and cellular localization of neutral long-chain lipids in the haptophyte algae Isochrysis galbana and Emiliania huxleyi. J Phycol 41:1000–1009
Essigmann B, Güler S, Narang RA, Linke D, Benning C (1998) Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci U S A 95:1950–1955
Fabris M, Matthijs M, Rombatus S, Vyverman W, Goossens A, Baart GJ (2012) The metabolic blueprint of Phaeodactylum tricornutum reveals a eukaryotic Entner–Doudoroff glycolytic pathway. Plant J 70:1004–1014
Fahy E, Sud M, Cotter D, Subramaniam S (2007) LIPID MAPS online tools for lipid research. Nucleic Acids Res 35:W606–W612
Fan J, Andre C, Xu C (2011) A chloroplast pathway for the de novo biosynthesis of triacylglycerol in Chlamydomonas reinhardtii. FEBS Lett 585:1985–1991
Fan J, Yan C, Andre C, Shanklin J, Schwender J, Xu C (2012) Oil accumulation is controlled by carbon precursor supply for fatty acid synthesis in Chlamydomonas reinhardtii. Plant Cell Physiol 53:1380–1390
Farese RV Jr, Walther TC (2009) Lipid droplets finally get a little R-E-S-P-E-C-T. Cell 139(25):855–860
Ferro M, Salvi D, Brugière S, Miras S, Kowalski S, Louwagie M, Garin J, Joyard J, Rolland N (2003) Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Mol Cell Proteomics 2:325–345
Flügge UI, Häusler RE, Ludewig F, Gierth M (2011) The role of transporters in supplying energy to plant plastids. J Exp Bot 62:2381–2392
Frandsen GI, Mundy J, Tzen JT (2001) Oil bodies and their associated proteins, oleosin and caleosin. Physiol Plant 112:301–307
Fulda M, Shockey J, Werber M, Wolter FP, Heinz E (2002) Two long-chain acyl-CoA synthetases from Arabidopsis thaliana involved in peroxisomal fatty acid beta-oxidation. Plant J 32:93–103
Fulda M, Schnurr J, Abbadi A, Heinz E, Browse J (2004) Peroxisomal Acyl-CoA synthetase activity is essential for seedling development in Arabidopsis thaliana. Plant Cell 16:394–405
Furumoto T, Yamaguchi T, Ohshima-Ichie Y, Nakamura M, Tsuchida-Iwata Y, Shimamura M, Ohnishi J, Hata S, Gowik U, Westhoff P, Bräutigam A, Weber AP, Izui K (2011) A plastidial sodium-dependent pyruvate transporter. Nature 476:472–475
Gao J, Ajjawi I, Manoli A, Sawin A, Xu C, Froehlich JE, Last RL, Benning C (2009) FATTY ACID DESATURASE4 of Arabidopsis encodes a protein distinct from characterized fatty acid desaturases. Plant J 60:832–839
Georgianna DR, Mayfield SP (2012) Exploiting diversity and synthetic biology for the production of algal biofuels. Nature 488:329–335
Gidda SK, Shockey JM, Rothstein SJ, Dyer JM, Mullen RT (2009) 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 47:867–879
Gill I, Valivety R (1997) Polyunsaturated fatty acids, part 1: occurrence, biological activities and applications. Trends Biotechnol 15:401–409
Gimpel JA, Specht EA, Georgianna DR, Mayfield SP (2013) Advances in microalgae engineering and synthetic biology applications for biofuel production. Curr Opin Chem Biol 17:489–495
Giroud C, Eichenberger W (1988) Fattyacids of Chlamydomonas reinhardtii structure, positional distribution and biosynthesis. Biol Chem 369:18–19
Giroud C, Eichenberger W (1989) Lipids of Chlamydomonas reinhardtii – incorporation of 14C-acetate, 14C-palmitate and 14C-oleate into different lipids and evidence for lipid-linked desaturation of fattyacids. Plant Cell Physiol 30:121–128
Giroud C, Gerber A, Eichenberger W (1988) Lipids of Chlamydomonas reinhardtii. Analysis of molecular species and intracellular site(s) of biosynthesis. Plant Cell Physiol 29:587–595
Gong Y, Guo X, Wan X, Liang Z, Jiang M (2011) Characterization of a novel thioesterase (PtTE) from Phaeodactylum tricornutum. J Basic Microbiol 51:666–672
Gong Y, Zhang J, Guo X, Wan X, Liang Z, Hu CJ, Jiang M (2013) Identification and characterization of PtDGAT2B, an acyltransferase of the DGAT2 acyl-coenzyme A: diacylglycerol acyltransferase family in the diatom Phaeodactylum tricornutum. FEBS Lett 587:481–487
Gonzalez-Ballester D, Pollock SV, Pootakham W, Grossman AR (2008) The central role of a RK2 kinase in sulfur deprivation responses. Plant Physiol 147:216–227
González-Ballester D, Casero D, Cokus S, Pellegrini M, Merchant SS, Grossman AR (2010) RNA-Seq analysis of sulfur-deprived Chlamydomonas cells reveals aspects of acclimation critical for cell survival. Plant Cell 22:2058–2084
Goode GH, Dewey RE (1999) Characterisation of aminoalcoholphosphotransferases from Arabidopsis thaliana and soybean. Plant Physiol Biochem 37:445–457
Goodenough U, Blaby I, Casero D, Gallaher SD, Goodson C, Johnson S, Lee JH, Merchant SS, Pellegrini M, Roth R, Rusch J, Singh M, Umen JG, Weiss TL, Wulan T (2014) The path to triacylglyceride obesity in the sta6 strain of Chlamydomonas reinhardtii. Eukaryot Cell 13:591–613
Goodson C, Roth R, Wang ZT, Goodenough U (2011) Structural correlates of cytoplasmic and chloroplast lipid body synthesis in Chlamydomonas reinhardtii and stimulation of lipid body production with acetate boost. Eukaryot Cell 10:1592–1606
Gray CG, Lasiter AD, Li C, Leblond JD (2009a) Mono- and digalactosyldiacylglycerol composition of dinoflagellates. I. Peridinin-containing taxa. Eur J Phycol 44:191–197
Gray CG, Lasiter AD, Leblond JD (2009b) Mono- and digalactosyldiacylglycerol composition of dinoflagellates. III. Four cold-adapted, peridinin-containing taxa and the presence of trigalactosyldiacylglycerol as an additional glycolipid. Eur J Phycol 44:439–445
Grillitsch K, Connerth M, Köfeler H, Arrey TN, Rietschel B, Wagner B, Karas M, Daum G (2011) Lipid particles/droplets of the yeast Saccharomyces cerevisiae revisited: lipidome meets proteome. Biochim Biophys Acta 1811:1165–1176
Guarnieri MT, Nag A, Smolinski SL, Darzins A, Seibert M, Pienkos PT (2011) Examination of triacylglycerol biosynthetic pathways via de novo transcriptomic and proteomic analyses in an unsequenced microalga. PLoS One 6(10):e25851
Guarnieri MT, Nag A, Yang S, Pienkos PT (2013) Proteomic analysis of Chlorella vulgaris: potential targets for enhanced lipid accumulation. J Proteomics 93:245–253
Guerra LT, Levitan O, Frada MJ, Sun JS, Falkowski PG, Dismukes GC (2013) Regulatory branch points affecting protein and lipid biosynthesis in the diatom Phaeodactylum tricornutum. Biomass Bioenergy 59:306–315
Guihéneuf F, Fouqueray M, Mimouni V, Ulmann L, Jacquette B, Tremblin G (2010) Effect of UV stress on the fatty acid and lipid class composition in two marine microalgae Pavlova lutheri (Pavlovophyceae) and Odontella aurita (Bacillariophyceae). J Appl Phycol 22:629–638
Guihéneuf F, Leu S, Zarka A, Khozin-Goldberg I, Khalilov I, Boussiba S (2011) Cloning and molecular characterization of a novel acyl-CoA: diacylglycerol acyltransferase 1-like gene (PtDGAT1) from the diatom Phaeodactylum tricornutum. FEBS J 278:3651–3666
Güler S, Seeliger A, Härtel H, Renger G, Benning C (1996) A null mutant of Synechococcus sp. PCC7942 deficient in the sulfolipid sulfoquinovosyl diacylglycerol. J Biol Chem 271:7501–7507
Guschina IA, Harwood JL (2006) Lipids and lipid metabolism in eukaryotic algae. Prog Lipid Res 45:160–186
Guschina IA, Harwood JL (2009a) Algal lipids and effect of the environment on their biochemistry. In: Kainz M, Brett M, Arts M (eds) Lipids in aquatic ecosystems. Springer, Dordrecht, pp 1–24
Guschina IA, Harwood JL (2009b) The versatility of algae and their lipid metabolism. Biochimie 91:679–684
Guschina IA, Dobson G, Harwood JL (2003) Lipid metabolism in cultured lichen photobionts with different phosphorus status. Phytochemistry 64:209–217
Guskov A, Gabdulkhakov A, Broser M, Glöckner C, Hellmich J, Kern J, Frank J, Müh F, Saenger W, Zouni A (2010) Recent progress in the crystallographic studies of photosystem II. Chemphyschem 11:1160–1171
Hall CAS, Benemann JR (2011) Oil from algae? Bioscience 61:741–742
Hamilton ML, Haslam RP, Napier JA, Sayanova O (2014) Metabolic engineering of Phaeodactylum tricornutum for the enhanced accumulation of omega-3 long chain polyunsaturated fatty acids. Metab Eng 22:3–9
Härtel H, Dörmann P, Benning C (2000) DGD1-independent biosynthesis of extraplastidic galactolipids after phosphate deprivation in Arabidopsis. Proc Natl Acad Sci U S A 97:10649–10654
Harwood JL (1998) Membrane lipids in algae. In: Siegenthaler PA, Murata N (eds) Lipids in photosynthesis: structure, function and genetics. Kluwer, Dordrecht, pp 53–64
Harwood JL (2005) Fatty acid biosynthesis. In: Murphy DJ (ed) Plant lipids: biology, utilization and manipulation. CRC Press, Boca Raton, pp 27–102
Harwood JL (2010) Plant fatty acid synthesis. The AOCS lipid library; retrieved from http://www.lipidlibrary.aocs.org/plantbio/fa_biosynth
Haselier A, Akbari H, Weth A, Baumgartner W, Frentzen M (2010) Two closely related genes of Arabidopsis encode plastidial cytidinediphosphate diacylglycerol synthases essential for photoautotrophic growth. Plant Physiol 153:1372–1384
Haslam RP, Ruiz-Lopez N, Eastmond P, Moloney M, Sayanova O, Napier JA (2013) The modification of plant oil composition via metabolic engineering – better nutrition by design. Plant Biotechnol J 11:157–168
Heilmann I, Mekhedov S, King B, Browse J, Shanklin J (2004) Identification of the Arabidopsis palmitoyl-monogalactosyldiacylglycerol Δ7-desaturase gene FAD5, and effects of plastidial retargeting of Arabidopsis desaturases on the fad5 mutant phenotype. Plant Physiol 136:4237–4245
Heinz E (1993) Biosynthesis of polyunsaturated fatty acids. In: Moore TS (ed) Lipid metabolism in plants. CRC Press, Boca Raton, pp 34–89
Heinz E, Roughan PG (1983) Similarities and differences in lipid metabolism of chloroplasts isolated from 18:3 and 16:3 plants. Plant Physiol 72:273–279
Henderson RJ, Mackinlay EE (1992) Radiolabeling studies of lipids in the marine cryptomonad Chroomonas salina in relation to fatty acid desaturation. Plant Cell Physiol 33:395–406
Henneberry AL, McMaster CR (1999) Cloning and expression of a human choline/ethanolaminephosphotransferase: synthesis of phosphatidylcholine and phosphatidylethanolamine. Biochem J 339:291–298
Hernández ML, Whitehead L, He Z, Gazda V, Gilday A, Kozhevnikova E, Vaistij FE, Larson TR, Graham IA (2012) A cytosolic acyltransferase contributes to triacylglycerol synthesis in sucrose-rescued Arabidopsis seed oil catabolism mutants. Plant Physiol 160:215–225
Hildebrand DF, Yu K, McCracken C, Rao SS (2005) Fatty acid manipulation. In: Murphy DJ (ed) Plant lipids: biology, utilization and manipulation. CRC Press, Boca Raton, pp 67–102
Hildebrand M, Abbriano RM, Polle JE, Traller JC, Trentacoste EM, Smith SR, Davis AK (2013) Metabolic and cellular organization in evolutionarily diverse microalgae as related to biofuels production. Curr Opin Chem Biol 17:506–514
Hjelmstad RH, Bell RM (1987) Mutants of Saccharomyces cerevisiae defective in sn-1,2-diacylglycerol cholinephosphotransferase. Isolation, characterization, and cloning of the CPT1 gene. J Biol Chem 262:3909–3917
Hoffmann M, Wagner M, Abbadi A, Fulda M, Feussner I (2008) Metabolic engineering of omega3-very long chain polyunsaturated fatty acid production by an exclusively acyl-CoA-dependent pathway. J Biol Chem 283:22352–22362
Hoffmeister M, Piotrowski M, Nowitzki U, Martin W (2005) Mitochondrial trans-2-enoyl-CoA reductase of wax ester fermentation from Euglena gracilis defines a new family of enzymes involved in lipid synthesis. J Biol Chem 280:4329–4338
Hölzl G, Witt S, Kelly AA, Zähringer U, Warnecke D, Dörmann P, Heinz E (2006) Functional differences between galactolipids and glucolipids revealed in photosynthesis of higher plants. Proc Natl Acad Sci U S A 103:7512–7517
Hu H, Gao K (2003) Optimization of growth and fatty acid composition of a unicellular marine picoplankton, Nannochloropsis sp., with enriched carbon sources. Biotechnol Lett 25:421–425
Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J 54:621–639
Hu Z, Ren Z, Lu C (2012) The phosphatidylcholine diacylglycerol cholinephosphotransferase is required for efficient hydroxy fatty acid accumulation in transgenic Arabidopsis. Plant Physiol 158:1944–1954
Hu J, Wang D, Li J, Jing G, Ning K, Xu J (2014) Genome-wide identification of transcription factors and transcription-factor binding sites in oleaginous microalgae Nannochloropsis. Sci Rep 4:5454. doi:10.1038/srep05454
Huang AHC (1992) Oil bodies and oleosins in seeds. Annu Rev Plant Physiol Plant Mol Biol 43:177–200
Huang NL, Huang MD, Chen TLL, Huang AHC (2013) Oleosin of subcellular lipid droplets evolved in green algae. Plant Physiol 161:1862–1874
Huerlimann R, Heimann K (2013) Comprehensive guide to acetyl-carboxylases in algae. Crit Rev Biotechnol 33:49–65
Huflejt ME, Tremolieres A, Pineau B, Lang JK, Hatheway J, Packer L (1990) Changes in membrane lipid composition during saline growth of the fresh water cyanobacterium Synechococcus 6311. Plant Physiol 94:1512–1521
Hung CH, Ho MY, Kanehara K, Nakamura Y (2013) Functional study of diacylglycerol acyltransferase type 2 family in Chlamydomonas reinhardtii. FEBS Lett 587:2364–2370
Hurlock AK, Roston RL, Wang K, Benning C (2014) Lipid trafficking in plant cells. Traffic 15:915–932
Iskandarov U, Khozin-Goldberg I, Ofir R, Cohen Z (2009) Cloning and characterization of the ∆6 polyunsaturated fatty acid elongase from the green microalga Parietochloris incisa. Lipids 44:545–554
Iskandarov U, Khozin-Goldberg I, Cohen Z (2010) Cloning and characterization of the ∆12, ∆6 and ∆5 desaturases from the green microalga Parietochloris incisa. Lipids 45:519–530
Iskandarov U, Sitnik S, Shtaida N, Didi-Cohen S, Leu S, Khozin-Goldberg I, Cohen Z, Boussiba S (2015) Cloning and characterization of a GPAT-like gene from the microalga Lobosphaera incisa (Trebouxiophyceae): overexpression in Chlamydomonas reinhardtii enhances TAG production. J Appl Phycol http://dx.doi.org/10.1007/s10811-015-0634-1
Itoh R, Toda K, Takahashi H, Takano H, Kuroiwa T (1998) Delta-9 fatty acid desaturase gene containing a carboxyl-terminal cytochrome b5 domain from the red alga Cyanidioschyzon merolae. Curr Genet 33:165–170
Iwai M, Ikeda K, Shimojima M, Ohta H (2014) Enhancement of extraplastidic oil synthesis in Chlamydomonas reinhardtii using a type‐2 diacylglycerol acyltransferase with a phosphorus starvation–inducible promoter. Plant Biotechnol J 12:808–819
Jacquier N, Choudhary V, Mari M, Toulmay A, Reggiori F, Schneiter R (2011) Lipid droplets are functionally connected to the endoplasmic reticulum in Saccharomyces cerevisiae. J Cell Sci 124:2424–2437
Jako C, Kumar A, Wei Y, Zou J, Barton DL, Giblin EM, Covello PS, Taylor DC (2001) Seed-specific over-expression of an Arabidopsis cDNA encoding a diacylglycerol acyltransferase enhances seed oil content and seed weight. Plant Physiol 126:861–874
James CN, Horn PJ, Case CR, Gidda SK, Zhang D, Mullen RT, Dyer JM, Anderson RG, Chapman KD (2010) Disruption of the Arabidopsis CGI-58 homologue produces Chanarin-Dorfman-like lipid droplet accumulation in plants. Proc Natl Acad Sci U S A 107:17833–17838
Jarvis P, Dörmann P, Peto CA, Lutes J, Benning C, Chory J (2000) Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant. Proc Natl Acad Sci U S A 97:8175–8179
Jia J, Han D, Gerken HG, Li Y, Sommerfeld M, Hu Q, Xu J (2015) Molecular mechanisms for photosynthetic carbon partitioning into storage neutral lipids in Nannochloropsis oceanica under nitrogen-depletion conditions. Algal Res 7:66–77
Jinkerson RE, Radakovits R, Posewitz MC (2013) Genomic insights from the oleaginous model alga Nannochloropsis gaditana. Bioengineered 4:37–43
Joseph SJ, Fernández-Robledo JA, Gardner MJ, El-Sayed NM, Kuo CH, Schott EJ, Wang H, Kissinger JC, Vasta GR (2010) Alveolate Perkinsus marinus: biological insights from EST gene discovery. BMC Genomics 11:228. doi:10.1186/1471-2164-11-228
Jouhet J, Maréchal E, Baldan B, Bligny R, Joyard J, Block MA (2004) Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria. J Cell Biol 167:863–874
Jouhet J, Maréchal E, Block MA (2007) Glycerolipid transfer for the building of membranes in plant cells. Prog Lipid Res 46:37–55
Kachroo A, Shanklin J, Whittle E, Lapchyk L, Hildebrand D, Kachroo P (2007) The Arabidopsis stearoyl-acyl carrier protein-desaturase family and the contribution of leaf isoforms to oleic acid synthesis. Plant Mol Biol 63:257–271
Kaczmarzyk D, Fulda M (2010) Fatty acid activation in cyanobacteria mediated by acyl-acyl carrier protein synthetase enables fatty acid recycling. Plant Physiol 152:1598–1610
Kagan ML, West AL, Zante C, Calder PC (2013) Acute appearance of fatty acids in human plasma – a comparative study between polar-lipid rich oil from the microalgae Nannochloropsis oculata and krill oil in healthy young males. Lipids Health Dis 12:102
Kajikawa M, Yamato KT, Kohzu Y, Shoji S, Matsui K, Tanaka Y, Sakai Y, Fukuzawa H (2006) A front-end desaturase from Chlamydomonas reinhardtii produces pinolenic and coniferonic acids by ω13 desaturation in methylotrophic yeast and tobacco. Plant Cell Physiol 47:64–73
Kalscheuer R, Steinbüchel A (2003) A novel bifunctional wax ester synthase/acyl-CoA: diacylglycerol acyltransferase mediates wax ester and triacylglycerol biosynthesis in Acinetobacter calcoaceticus ADP1. J Biol Chem 278:8075–8082
Karsten U, Friedl T, Schumann R, Hoyer K, Lembke S (2005) Mycosporine-like amino acids and phylogenies in green algae: Prasiola and its relatives from the Trebouxiophyceae (Chlorophyta). J Phycol 41:557–566
Kato M, Hajiro-Nakanishi K, Sano H, Miyachi S (1995) Polyunsaturated fatty acids and betaine lipids from Pavlova lutheri. Plant Cell Physiol 36:1607–1611
Kato M, Sakai S, Adachi K, Ikemoto H, Sano H (1996) Distribution of betaine lipids in marine algae. Phytochemistry 42:1341–1345
Katz A, Jimenez C, Pick U (1995) Isolation and characterization of a protein associated with carotene globules in the alga Dunaliella bardawil. Plant Physiol 108:1657–1664
Kazachkov M, Chen Q, Wang L, Zou J (2008) Substrate preferences of a lysophosphatidylcholine acyltransferase highlight its role in phospholipid remodeling. Lipids 43:895–902
Ke J, Behal RH, Back SL, Nikolau BJ, Wurtele ES, Oliver DJ (2000) The role of pyruvate dehydrogenase and acetyl-coenzyme A synthetase in fatty acid synthesis in developing Arabidopsis seeds. Plant Physiol 123:497–508
Kelly AA, Dörmann P (2004) Green light for galactolipid trafficking. Curr Opin Plant Biol 78:262–269
Kelly AA, Dörmannn P (2002) DGD2, an Arabidopsis gene encoding a UDP-galactose-dependent digalactosyldiacylglycerol synthase is expressed during growth under phosphate-limiting conditions. J Biol Chem 277:1166–1173
Kelly K, Jacobs R (2011) Phospholipid biosynthesis. Retrieved from http://lipidlibrary.aocs.org/animbio/animlip.html
Kelly AA, Froehlich JE, Dörmann P (2003) Disruption of the two digalactosyldiacylglycerol synthase genes DGD1 and DGD2 in Arabidopsis reveals the existence of an additional enzyme of galactolipid synthesis. Plant Cell 15:2694–2706
Kelly AA, van Erp H, Quettier AL, Shaw E, Menard G, Kurup S, Eastmond PJ (2013) The sugar-dependent1 lipase limits triacylglycerol accumulation in vegetative tissues of Arabidopsis. Plant Physiol 162:1282–1289
Kennedy EP (1961) Biosynthesis of complex lipids. Fed Proc 20:934–940
Kent C (1995) Eukaryotic phospholipid biosynthesis. Annu Rev Biochem 64:315–343
Kern J, Guskov A (2011) Lipids in photosystem II: multifunctional cofactors. J Photochem Photobiol B 104:19–34
Khozin I, Adlerstein D, Bigogno C, Heimer YM, Cohen Z (1997) Elucidation of the biosynthesis of EPA in the microalga Porphyridium cruentum II: radiolabeling studies. Plant Physiol 114:223–230
Khozin-Goldberg I, Cohen Z (2006) The effect of phosphate starvation on the lipid and fatty acid composition of the fresh water eustigmatophyte Monodus subterraneus. Phytochemistry 67:696–701
Khozin-Goldberg I, Yu HZ, Adlerstein D, Didi-Cohen S, Heimer YM, Cohen Z (2000) Triacylglycerols of the red microalga Porphyridium cruentum can contribute to the biosynthesis of eukaryotic galactolipids. Lipids 35:881–889
Khozin-Goldberg I, Bigogno C, Shrestha P, Cohen Z (2002a) Nitrogen starvation induces the accumulation of arachidonic acid in the freshwater green alga Parietochloris incisa (Trebouxiophyceae). J Phycol 38:991–994
Khozin-Goldberg I, Didi-Cohen S, Shayakhmetova I, Cohen Z (2002b) Elucidation of the biosynthesis of eicosapentaenoic acid (EPA) in the freshwater eustigmatophyte Monodus subterraneus. J Phycol 38:745–756
Khozin-Goldberg I, Shrestha P, Cohen Z (2005) Mobilization of arachidonyl moieties from triacylglycerols into chloroplastic lipids following recovery from nitrogen starvation of the microalga Parietochloris incisa. Biochim Biophys Acta 1738:63–71
Khozin-Goldberg I, Iskandarov U, Cohen Z (2011) LC-PUFA from photosynthetic microalgae: occurrence, biosynthesis, and prospects in biotechnology. Appl Microbiol Biotechnol 91:905–915
Kim HU, Lee KR, Go YS, Jung JH, Suh MC, Kim JB (2011) Endoplasmic reticulum-located PDAT1-2 from castor bean enhances hydroxy fatty acid accumulation in transgenic plants. Plant Cell Physiol 52:983–993
King A, Nam JW, Han JX, Hilliard J, Jaworski JG (2007) Cuticular wax biosynthesis in petunia petals: cloning and characterization of an alcohol-acyltransferase that synthesizes wax-esters. Planta 226:381–394
Kinney AJ (1993) Phospholipid head groups. In: Moore TS (ed) Lipid metabolism in plants. CRC Press, Boca Raton, pp 259–284
Kleczkowski LA, Decker D, Wilczynska M (2011) UDP-sugar pyrophosphorylase: a new old mechanism for sugar activation. Plant Physiol 156:3–10
Klein U (1986) Compartmentation of glycolysis and of the oxidative pentose-phosphate pathway in Chlamydomonas reinhardtii. Planta 167:81–86
Kobayashi K, Kondo M, Fukuda H, Nishimura M, Ohta H (2007) Galactolipid synthesis in chloroplast inner envelope is essential for proper thylakoid biogenesis, photosynthesis, and embryogenesis. Proc Natl Acad Sci U S A 104:17216–17221
Kobayashi K, Awai K, Nakamura M, Nagatani A, Masuda T, Ohta H (2009a) Type-B monogalactosyldiacylglycerol synthases are involved in phosphate starvation-induced lipid remodeling, and are crucial for low-phosphate adaptation. Plant J 57:322–331
Kobayashi K, Nakamura Y, Ohta H (2009b) Type A and type B monogalactosyldiacylglycerol synthases are spatially and functionally separated in the plastids of higher plants. Plant Physiol Biochem 47:518–525
Kobayashi K, Narise T, Sonoike K, Hashimoto H, Sato N, Kondo M, Nishimura M, Sato M, Toyooka K, Sugimoto K, Wada H, Masuda T, Ohta H (2013) Role of galactolipid biosynthesis in coordinated development of photosynthetic complexes and thylakoid membranes during chloroplast biogenesis in Arabidopsis. Plant J 73:250–261
Konishi T, Shinohara K, Yamada K, Sasaki Y (1996) Acetyl-CoA carboxylase in higher plants: most plants other than Gramineae have both the prokaryotic and the eukaryotic forms of this enzyme. Plant Cell Physiol 37:117–122
Kornberg A, Pricer WE Jr (1953) Enzymatic esterification of alpha-glycerophosphate by long chain fatty acids. J Biol Chem 204:345–357
La Russa M, Bogen C, Uhmeyer A, Doebbe A, Filippone E, Kruse O, Mussgnug JH (2012) Functional analysis of three type-2 DGAT homologue genes for triacylglycerol production in the green microalga Chlamydomonas reinhardtii. J Biotechnol 162:13–20
Lands WE (1958) Metabolism of glycerolipides; a comparison of lecithin and triglyceride synthesis. J Biol Chem 231:883–888
Lang I, Hodac L, Friedl T, Feussner I (2011) Fatty acid profiles and their distribution patterns in microalgae: a comprehensive analysis of more than 2000 strains from the SAG culture collection. BMC Plant Biol 11:124
Lardizabal KD, Mai JT, Wagner NW, Wyrick A, Voelker T, Hawkins DJ (2001) DGAT2 is a new diacylglycerol acyltransferase gene family: purification, cloning, and expression in insect cells of two polypeptides from Mortierella ramanniana with diacylglycerol acyltransferase activity. J Biol Chem 276:38862–38869
Lardizabal K, Effertz R, Levering C, Mai J, Pedroso MC, Jury T, Aasen E, Gruys K, Bennett K (2008) Expression of Umbelopsis ramanniana DGAT2A in seed increases oil in soybean. Plant Physiol 148:89–96
Lavens P, Sorgeloos P (1996) Manual on the production and use of life food for aquaculture. FAO Fish technical paper 361, pp 7–42. http://www.fao.org/docrep/003/w3732e/w3732e00.htm assesed on 06.11.2015
Le HD, Meisel JA, deMeijer VE, Gura KM, Puder M (2009) The essentiality of arachidonic acid and docosahexaenoic acid. Prostaglandins Leukot Essent Fatty Acids 81:165–170.
Leblond JD, Chapman PJ (2000) Lipid class distribution of highly unsaturated long chain fatty acids in marine dinoflagellates. J Phycol 36:1103–1108
Leblond JD, Lasiter AD (2009) Mono- and digalactosyldiacylglycerol composition of dinoflagellates. II. Lepidodinium chlorophorum, Karenia brevis, and Kryptoperidinium foliaceum, three dinoflagellates with aberrant plastids. Eur J Phycol 44:199–205
Leblond JD, Roche SA (2009) Mono- and digalactosyldiacylglycerol composition of chlorarachniophytes (Chlorarachniophyceae): production of a novel lauric acid (12:0)-containing form of monogalactosyldiacylglycerol (MGDG). Phycologia 48:101–104
Leblond JD, Evens TJ, Chapman PJ (2003) The biochemistry of dinoflagellate lipids, with particular reference to the fatty acid and sterol composition of a Karenia brevis bloom. Phycologia 42:324–331
Leblond JD, Dahmen JL, Seipelt RL, Elrod-Erickson MJ, Kincaid R, Howard JC, Evens TJ (2005) Lipid composition of chlorarachniophytes from the genera Bigelowiella, Gymnochlora, and Lotharella. J Phycol 41:311–321
Leblond JD, Dahmen JL, Evens TJ (2010a) Mono- and digalactosyldiacylglycerol composition of dinoflagellates. IV. Temperature-induced modulation of fatty acid regiochemistry as observed by electrospray ionization/mass spectrometry. Eur J Phycol 45:13–18
Leblond JD, Timofte HI, Roche SA, Porter NM (2010b) Mono- and digalactosyldiacylglycerol composition of glaucocystophytes (Glaucophyta): a modern interpretation using positive-ion electrospray ionization/mass spectrometry/mass spectrometry. Phycol Res 58:222–229
Lee AG (2000) Membrane lipids: it’s only a phase. Curr Biol 10:R377–R380
Lewin TM, Wang P, Coleman RA (1999) Analysis of amino acid motifs diagnostic for the sn-glycerol-3-phosphate acyltransferase reaction. Biochemistry 38:5764–5771
Leu S, Boussiba S (2014) Advances in the production of high-value products by microalgae. Ind Biotechnol 10:169–183
Li M, Welti R, Wang X (2006) Quantitative profiling of Arabidopsis polar glycerolipids in response to phosphorus starvation. Roles of phospholipases Dζ1 and Dζ2 in phosphatidylcholine hydrolysis and digalactosyldiacylglycerol accumulation in phosphorus-starved plants. Plant Physiol 142:750–761
Li R, Yu K, Hatanaka T, Hildebrand DF (2010a) Vernonia DGATs increase accumulation of epoxy fatty acids in oil. Plant Biotechnol J 8:184–195
Li R, Yu K, Hildebrand DF (2010b) DGAT1, DGAT2 and PDAT expression in seeds and other tissues of epoxy and hydroxy fatty acid accumulating plants. Lipids 45:145–157
Li Y, Han D, Hu G, Dauvillee D, Sommerfeld M, Ball S, Hu Q (2010c) Chlamydomonas starchless mutant defective in ADP-glucose pyrophosphorylase hyper-accumulates triacylglycerol. Metab Eng 12:387–391
Li YT, Han D, Sommerfeld M, Hu Q (2011) Photosynthetic carbon partitioning and lipid production in the oleaginous microalga Pseudochlorococcum sp. (Chlorophyceae) under nitrogen-limited conditions. Bioresour Technol 102:123–129
Li X, Benning C, Kuo MH (2012a) Rapid triacylglycerol turnover in Chlamydomonas reinhardtii requires a lipase with broad substrate specificity. Eukaryot Cell 11:1451–1462
Li X, Moellering ER, Liu B, Johnny C, Fedewa M, Sears BB, Kuo MH, Benning CA (2012b) Galactoglycerolipid lipase is required for triacylglycerol accumulation and survival following nitrogen deprivation in Chlamydomonas reinhardtii. Plant Cell 24:4670–4686
Li Y, Fei X, Deng X (2012c) Novel molecular insights into nitrogen starvation-induced triacylglycerols accumulation revealed by differential gene expression analysis in green algae Micractinium pusillum. Biomass Bioenergy 42:199–211
Li M, Bahn SC, Fan C, Li J, Phan T, Ortiz M, Roth MR, Welti R, Jaworski J, Wang X (2013) Patatin-related phospholipase pPLAIIIδ increases seed oil content with long-chain fatty acids in Arabidopsis. Plant Physiol 162:39–51
Li J, Han D, Wang D, Ning K, Jia J, Wei L, Jing X, Huang S, Chen J, Li Y, Hu Q, Xu J (2014) Choreography of transcriptomes and lipidomes of Nannochloropsis reveals the mechanisms of oil synthesis in microalgae. Plant Cell 26:1645–1665
Liang Y, Maeda Y, Yoshino T, Matsumoto M, Tanaka T (2014) Profiling of polar lipids in marine oleaginous diatom Fistulifera solaris JPCC DA0580: prediction of the potential mechanism for eicosapentaenoic acid-incorporation into triacylglycerol. Mar Drugs 12:3218–3230
Li-Beisson Y, Shorrosh B, Beisson F, Andersson M, Arondel V, Bates P, Baud S, Bird D, DeBono A, Durrett T, Franke R, Graham I, Katayama K, Kelly A, Larson T, Markham J, Miquel M, Molina I, Nishida I, Rowland O, Samuels L, Schmid K, Wada H, Welti R, Xu C, Zallot R, Ohlrogge J (2010) Acyl lipid metabolism. In: Last R (ed) The Arabidopsis book. American Society of Plant Biologists, Rockville, pp 1–65
Li-Beisson Y, Shorrosh B, Beisson F, Andersson MX, Arondel V, Bates PD, Baud S, Bird D, Debono A, Durrett TP, Franke RB, Graham IA, Katayama K, Kelly AA, Larson T, Markham JE, Miquel M, Molina I, Nishida I, Rowland O, Samuels L, Schmid KM, Wada H, Welti R, Xu C, Zallot R, Ohlrogge J. (2013) The Arabidopsis Book. 11:e0161. doi:10.1199/tab.0161
Lin M, Oliver DJ (2008) The role of acetyl-CoA synthetase in Arabidopsis. Plant Physiol 147:1822–1829
Lin M, Behal RH, Oliver DJ (2003) Disruption of plE2, the gene for the E2 subunit of the plastid pyruvate dehydrogenase complex, in Arabidopsis causes an early embryo lethal phenotype. Plant Mol Biol 52:865–872
Lippmeier JC, Crawford KS, Owen CB, Rivas AA, Metz JG, Apt KE (2009) Characterization of both polyunsaturated fatty acid biosynthetic pathways in Schizochytrium sp. Lipids 44:621–630
Liu B, Benning C (2013) Lipid metabolism in microalgae distinguishes itself. Curr Opin Biotechnol 24:300–309
Liu Q, Siloto RM, Lehner R, Stone SJ, Weselake RJ (2012a) Acyl-CoA:diacylglycerol acyltransferase: molecular biology, biochemistry and biotechnology. Prog Lipid Res 51:350–377
Liu J, Sun Z, Zhong Y, Huang J, Hu Q, Chen F (2012b) Stearoyl-acyl carrier protein desaturase gene from the oleaginous microalga Chlorella zofingiensis: cloning, characterization and transcriptional analysis. Planta 236:1665–1676
Liu B, Vieler A, Li C, Daniel Jones A, Benning C (2013) Triacylglycerol profiling of microalgae Chlamydomonas reinhardtii and Nannochloropsis oceanica. Bioresour Technol 146:310–316
Lu C, Xin Z, Ren Z, Miquel M, Browse J (2009) An enzyme regulating triacylglycerol composition is encoded by the ROD1 gene of Arabidopsis. Proc Natl Acad Sci U S A 106:18837–18842
Lundquist TJ, Woertz IC, Quinn NWT, Benemann JR (2010) A realistic technology and engineering assessment of algae biofuel production. Energy Biosciences Institute University of California, California
Lung SC, Weselake RJ (2006) Diacylglycerol acyltransferase: a key mediator of plant triacylglycerol synthesis. Lipids 41:1073–1088
Lv H, Qu G, Qi X, Lu L, Tian C, Ma Y (2013) Transcriptome analysis of Chlamydomonas reinhardtii during the process of lipid accumulation. Genomics 101:229–237
Ma W, Kong Q, Arondel V, Kilaru A, Bates PD, Thrower NA, Benning C, Ohlrogge JB (2013) WRINKLED1, a ubiquitous regulator in oil accumulating tissues from Arabidopsis embryos to oil palm mesocarp. PLoS One 8(7):e68887
MacDougall KM, McNichol J, McGinn PJ, O’Leary SJ, Melanson JE (2011) Triacylglycerol profiling of microalgae strains for biofuel feedstock by liquid chromatography-high-resolution mass spectrometry. Anal Bioanal Chem 401:2609–2616
Maisonneuve S, Bessoule JJ, Lessire R, Delseny M, Roscoe TJ (2010) Expression of rapeseed microsomal lysophosphatidic acid acyltransferase isozymes enhances seed oil content in Arabidopsis. Plant Physiol 152:670–684
Makewicz A, Gribi C, Eichenberger W (1997) Lipids of Ectocarpus fasciculatus (Phaeophyceae). Incorporation of [l-14C]oleate and the role of TAG and MGDG in lipid metabolism. Plant Cell Physiol 38:952–960
Mancini A, Del Rosso F, Roberti R, Orvietani P, Coletti L, Binaglia L (1999) Purification of ethanolaminephosphotransferase from bovine liver microsomes. Biochim Biophys Acta 1437:80–92
Martin P, Van Mooy BAS, Heithoff A, Dyhrman ST (2011) Phosphorus supply drives rapid turnover of membrane phospholipids in the diatom Thalassiosira pseudonana. ISME J 5:1057–1060
Martin GJ, Hill DR, Olmstead IL, Bergamin A, Shears MJ, Dias DA, Kentish SE, Scales PJ, Botté CY, Callahan DL (2014) Lipid profile remodeling in response to nitrogen deprivation in the microalgae Chlorella sp. (Trebouxiophyceae) and Nannochloropsis sp. (Eustigmatophyceae). PLoS One 9(8):e103389
McCourt P, Browse J, Watson J, Arntzen CJ, Somerville CR (1985) Analysis of photosynthetic antenna function in a mutant of Arabidopsis thaliana (L.) lacking trans-hexadecenoic acid. Plant Physiol 78:853–858
McFie PJ, Stone SL, Banman SL, Stone SJ (2010) Topological orientation of acyl-CoA: diacylglycerol acyltransferase-1 (DGAT1) and identification of a putative active site histidine and the role of the n terminus in dimer/tetramer formation. J Biol Chem 285:37377–37387
Manaf AM, Harwood JL (2000) Purification and characterisation of acyl-CoA: glycerol 3-phosphate acyltransferase from oil palm (Elaeis guineensis) tissues. Planta 210:318–328
Mendiola-Morgenthaler L, Eichenberger W, Boschetti A (1985) Isolation of chloroplast envelopes from Chlamydomonas. Lipid and polypeptide composition. Plant Sci 41:97–104
Mentzen WI, Peng J, Ransom N, Nikolau BJ, Wurtele ES (2008) Articulation of three core metabolic processes in Arabidopsis: fatty acid biosynthesis, leucine catabolism and starch metabolism. BMC Plant Biol 11:8–76
Merchant SS, Kropat J, Liu B, Shaw J, Warakanont J (2012) TAG, you’re it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation. Curr Opin Biotechnol 23:352–363
Merzlyak M, Chivkunova O, Reshetnikova I, Solovchenko A, Khozin-Goldberg I, Cohen Z (2007) Effect of nitrogen starvation on optical properties, pigments, and arachidonic acid content of the unicellular green alga Parietochloris incisa (Trebouxiophyceae, Chlorophyta). J Phycol 43:833–843
Metz JG, Roessler P, Facciotti D, Levering C, Dittrich F, Lassner M, Valentine R, Lardizabal K, Domergue F, Yamada A, Yazawa K, Knauf V, Browse J (2001) Production of polyunsaturated fatty acids by polyketide synthetases in both prokaryotes and eukaryotes. Science 293:290–293
Metzger P, Largeau C (2005) Botryococcus braunii: a rich source for hydrocarbons and related ether lipids. Appl Microbiol Biotechnol 66:486–496
Meyer A, Cirpus P, Ott C, Schlecker R, Zähringer U, Heinz E (2003) Biosynthesis of docosahexaenoic acid in Euglena gracilis: biochemical and molecular evidence for the involvement of a D4-fatty acyl group desaturation. Biochemistry 42:9779–9788
Meyer A, Kirsch H, Domergue F, Abbadi A, Sperling P, Bauer J, Cirpus P, Zank TK, Moreau H, Roscoe TJ, Zähringer U, Heinz E (2004) Novel fatty acid elongases and their use for the reconstitution of docosahexaenoic acid biosynthesis. J Lipid Res 45:1899–1909
Mietkiewska E, Siloto RM, Dewald J, Shah S, Brindley DN, Weselake RJ (2011) Lipins from plants are phosphatidate phosphatases that restore lipid synthesis in a pah1Δ mutant strain of Saccharomyces cerevisiae. FEBS J 278:764–775
Miller R, Wu G, Deshpande R, Vieler A, Gartner K, Li X, Moellering E, Zauner S, Cornish A, Liu B (2010) Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol 154:1737–1752
Minoda A, Sato N, Nozaki H, Okada K, Takahashi H, Sonoike K, Tsuzuki M (2002) Role of sulfoquinovosyl diacylglycerol for the maintenance of photosystem II in Chlamydomonas reinhardtii. Eur J Biochem 269:2353–2358
Mitchell AG, Martin CE (1995) A novel cytochrome b5-like domain is linked to the carboxyl terminus of the Saccharomyces cerevisiae delta-9 fatty acid desaturase. J Biol Chem 270:29766–29772
Mitchell BF, Pedersen LB, Feely M, Rosenbaum JL, Mitchell DR (2005) ATP production in Chlamydomonas reinhardtii flagella by glycolytic enzymes. Mol Biol Cell 16:4509–4518
Mizoi J, Nakamura M, Nishida I (2006) Defects in CTP:PHOSPHORYLETHANOLAMINE CYTIDYLYLTRANSFERASE affect embryonic and postembryonic development in Arabidopsis. Plant Cell 18:3370–3385
Mock T, Kroon BM (2002) Photosynthetic energy conversion under extreme conditions – II: the significance of lipids under light limited growth in Antarctic sea ice diatoms. Phytochemistry 61:53–60
Moellering ER, Benning C (2010) RNA interference silencing of a major lipid droplet protein affects lipid droplet size in Chlamydomonas reinhardtii. Eukaryot Cell 9:97–106
Moellering ER, Miller R, Benning C (2009) Molecular genetics of lipid metabolism in the model green alga Chlamydomonas reinhardtii. In: Wada H, Murata N (eds) Lipids in photosynthesis: essential and regulatory functions. Springer, Dordrecht, pp 139–155
Moellering ER, Muthan B, Benning C (2010) Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330:226–228
Molina Grima E, Sánchez Pérez JA, García Sánchez JL, García Camacho F, López Alonso D (1992) EPA from Isochrysis galbana. Growth conditions and productivity. Process Biochem 27:299–306
Molina-Grima E, Garcia Camacho F, Acien Fernandez FG (1999) Production of EPA from Phaeodactylum tricornutum. In: Cohen Z (ed) Chemicals from microalgae. Taylor and Francis, London, pp 57–92
Molnár I, Lopez D, Wisecaver JH, Devarenne TP, Weiss TL, Pellegrini M, Hackett JD (2012) Bio-crude transcriptomics: gene discovery and metabolic network reconstruction for the biosynthesis of the terpenome of the hydrocarbon oil-producing green alga, Botryococcus braunii race B (Showa). BMC Genomics 13:576
Mongrand S, Cassagne C, Bessoule JJ (2000) Import of lyso-phosphatidylcholine into chloroplasts likely at the origin of eukaryotic plastidial lipids. Plant Physiol 122:845–852
Moore TS, Du Z, Chen Z (2001) Membrane lipid biosynthesis in Chlamydomonas reinhardtii. In vitro biosynthesis of diacylglyceryltrimethylhomoserine. Plant Physiol 125:423–429
Moreno-Pérez AJ, Venegas-Calerón M, Vaistij FE, Salas JJ, Larson TR, Garcés R, Graham IA, Martínez-Force E (2012) Reduced expression of FatA thioesterases in Arabidopsis affects the oil content and fatty acid composition of the seeds. Planta 235:629–639
Msanne J, Xu D, Konda AR, Casas-Mollano JA, Awada T, Cahoon EB, Cerutti H (2012) Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonas reinhardtii and Coccomyxa sp. C-169. Phytochemistry 75:50–59
Munnik T (2001) Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci 6:227–233
Murata N, Tasaka Y (1997) Glycerol-3-phosphate acyltransferase in plants. Biochim Biophys Acta 1348:10–16
Murata N, Wada H (1995) Acyl-lipid desaturases and their importance in the tolerance and acclimatization to cold of cyanobacteria. Biochem J 308:1–8
Murphy DJ (2001) The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Prog Lipid Res 40:325–438
Murphy DJ (2012) The dynamic roles of intracellular lipid droplets: from archaea to mammals. Protoplasma 249:541–585
Muto M, Kubota C, Tanaka M, Satoh A, Matsumoto M, Yoshino T, Tanaka T (2013) Identification and functional analysis of delta-9 desaturase, a key enzyme in PUFA synthesis, isolated from the oleaginous diatom Fistulifera. PLoS One 8(9):e73507
Muto M, Tanaka M, Liang Y, Yoshino T, Matsumoto M, Tanaka T (2015) Enhancement of glycerol metabolism in the oleaginous marine diatom Fistulifera solaris JPCC DA0580 to improve triacylglycerol productivity. Biotechnol Biofuels 8(1):4. doi:10.1186/s13068-014-0184-9
Nakamura Y, Tsuchiya M, Ohta H (2007) Plastidic phosphatidic acid phosphatases identified in a distinct subfamily of lipid phosphate phosphatases with prokaryotic origin. J Biol Chem 282:29013–29021
Nakamura Y, Koizumi R, Shui G, Shimojima M, Wenk MR, Ito T, Ohta H (2009) Arabidopsis lipins mediate eukaryotic pathway of lipid metabolism and cope critically with phosphate starvation. Proc Natl Acad Sci U S A 106:20978–20983
Napier JA (2007) The production of unusual fatty acids in transgenic plants. Annu Rev Plant Biol 58:295–319
Napier JA, Graham IA (2010) Tailoring plant lipid composition: designer oilseeds come of age. Curr Opin Plant Biol 13:330–337
Napier JA, Michaelson LV, Stobart AK (1999) Plant desaturases: harvesting the fat of the land. Curr Opin Plant Biol 2:123–127
Naumann I, Klein BC, Bartel SJ, Darsow KH, Buchholz R, Lange HA (2011) Identification of sulfoquinovosyldiacyglycerides from Phaeodactylum tricornutum by matrix-assisted laser desorption/ionization QTrap time-of-flight hybrid mass spectrometry. Rapid Commun Mass Spectrom 25:2517–2523
Nerlich A, von Orlow M, Rontein D, Hanson AD, Dörmann P (2007) Deficiency in phosphatidylserine decarboxylase activity in the psd1 psd2 psd3 triple mutant of Arabidopsis affects phosphatidylethanolamine accumulation in mitochondria. Plant Physiol 144:904–914
Neupert J, Karcher D, Bock R (2009) Generation of Chlamydomonas strains that efficiently express nuclear transgenes. Plant J 57:1140–1150
Nguyen HM, Baudet M, Cuiné S, Adriano JM, Barthe D, Billon E, Bruley C, Beisson F, Peltier G, Ferro M, Li-Beisson Y (2011) Proteomic profiling of oil bodies isolated from the unicellular green microalga Chlamydomonas reinhardtii: with focus on proteins involved in lipid metabolism. Proteomics 11:4266–4273
Nguyen HM, Cuiné S, Beyly-Adriano A, Légeret B, Billon E, Auroy P, Beisson F, Peltier G, Li-Beisson Y (2013) The green microalga Chlamydomonas reinhardtii has a single ω-3 fatty acid desaturase which localizes to the chloroplast and impacts both plastidic and extraplastidic membrane lipids. Plant Physiol 163:914–928
Niehaus TD, Okada S, Devarenne TP, Watt DS, Sviripa V, Chappell J (2011) Identification of unique mechanisms for triterpene biosynthesis in Botryococcus braunii. Proc Natl Acad Sci U S A 108:12260–12265
Nikolau BJ, Ohlrogge JB, Wurtele ES (2003) Plant biotin-containing carboxylases. Arch Biochem Biophys 414:211–222
Oakes J, Brackenridge D, Colletti R, Daley M, Hawkins DJ, Xiong H, Mai J, Screen SE, Val D, Lardizabal K, Gruys K, Deikman J (2011) Expression of fungal diacylglycerol acyltransferase 2 genes to increase kernel oil in maize. Plant Physiol 155:1146–1157
Oelkers P, Tinkelenberg A, Erdeniz N, Cromley D, Billheimer JT, Sturley SL (2000) A lecithin cholesterol acyltransferase-like gene mediates diacylglycerol esterification in yeast. J Biol Chem 275:15609–15612
Oelkers P, Cromley D, Padamsee M, Billheimer JT, Sturley SL (2002) The DGA1 gene determines a second triglyceride synthetic pathway in yeast. J Biol Chem 277:8877–8881
Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970
Okazaki Y, Shimojima M, Sawada Y, Toyooka K, Narisawa T, Mochida K, Tanaka H, Matsuda F, Hirai A, Hirai MY, Ohta H, Saito K (2009) A chloroplastic UDP-glucose pyrophosphorylase from Arabidopsis is the committed enzyme for the first step of sulfolipid biosynthesis. Plant Cell 21:892–909
Oliver DJ, Nikolau BJ, Wurtele ES (2009) Acetyl-CoA – life at the metabolic nexus. Plant Sci 176:597–601
Pagac M, de la Mora HV, Duperrex C, Roubaty C, Vionnet C, Conzelmann A (2011) Topology of 1-acyl-sn-glycerol-3-phosphate acyltransferases SLC1 and ALE1 and related membrane-bound O-acyltransferases (MBOATs) of Saccharomyces cerevisiae. J Biol Chem 286:36438–36447
Pagac M, Vazquez HM, Bochud A, Roubaty C, Knöpfli C, Vionnet C, Conzelmann A (2012) Topology of the microsomal glycerol-3-phosphate acyltransferase Gpt2p/Gat1p of Saccharomyces cerevisiae. Mol Microbiol 86:1156–1166
Page RA, Okada S, Harwood JL (1994) Acetyl-CoA carboxylase exerts strong flux control over lipid synthesis in plants. Biochim Biophys Acta 1210:369–372
Pal D, Khozin-Goldberg I, Cohen Z, Boussiba S (2011) The effect of light, salinity and nitrogen availability on lipid production by Nannochloropsis sp. Appl Microbiol Biotechnol 90:1429–1441
Pal D, Khozin-Goldberg I, Didi-Cohen S, Solovchenko A, Batushansky A, Kaye Y, Sikron N, Samani T, Fait A, Boussiba S (2013) Growth, lipid production and metabolic adjustments in the euryhaline eustigmatophyte Nannochloropsis oceanica CCALA 804 in response to osmotic downshift. Appl Microbiol Biotechnol 97:8291–8306
Pan X, Siloto RM, Wickramarathna AD, Mietkiewska E, Weselake RJ (2013) Identification of a pair of phospholipid: diacylglycerol acyltransferases from developing flax (Linum usitatissimum L.) seed catalyzing the selective production of trilinolenin. J Biol Chem 288:24173–24188
Parthibane V, Rajakumari S, Venkateshwari V, Iyappan R, Rajasekharan R (2012) Oleosin is bifunctional enzyme that has both monoacylglycerolacyltransferase and phospholipase activities. J Biol Chem 287:1946–1954
Pascual F, Carman GM (2013) Phosphatidate phosphatase, a key regulator of lipid homeostasis. Biochim Biophys Acta 1831:514–522
Paul S, Gable K, Beaudoin F, Cahoon E, Jaworski J, Napier JA, Dunn TM (2006) Members of the Arabidopsis FAE1-like 3-Ketoacyl-CoA synthase gene family substitute for the Elop proteins of Saccharomyces cerevisiae. J Biol Chem 281:9018–9029
Peeler TC, Stephenson MB, Einspahr KJ, Thompson GA (1989) Lipid characterization of an enriched plasma membrane fraction of Dunaliella salina grown in media of varying salinity. Plant Physiol 89:970–976
Peled E, Leu S, Zarka A, Weiss M, Pick U, Khozin-Goldberg I, Boussiba S (2011) Isolation of a novel oil globule protein from the green alga Haematococcus pluvialis (Chlorophyceae). Lipids 46:851–861
Pereira SL, Huang YS, Bobik EG, Kinney AJ, Stecca KL, Packer JCL, Mukerji P (2004a) A novel omega3-fatty acid desaturase involved in the biosynthesis of eicosapentaenoic acid. Biochem J 378:665–671
Pereira SL, Leonard AE, Huang YS, Chuang L-T, Mukerji P (2004b) Identification of two novel microalgal enzymes involved in the conversion of the ω-3-fatty acid, eicosapentaenoic acid, into docosahexaenoic acid. Biochem J 384:357–366
Perrine Z, Negi S, Sayre RT (2012) Optimization of photosynthetic light energy utilization by microalgae. Algal Res 1:134–142
Peschke M, Moog D, Klingl A, Maier UG, Hempel F (2013) Evidence for glycoprotein transport into complex plastids. Proc Natl Acad Sci U S A 110:10860–10865
Péterfy M, Phan J, Xu P, Reue K (2001) Lipodystrophy in the fld mouse results from mutation of a new gene encoding a nuclear protein, lipin. Nat Genet 27:121–124
Petrie JR, Liu Q, Mackenzie AM, Shrestha P, Mansour MP, Robert SS, Frampton DF, Blackburn SI, Nichols PD, Singh SP (2010a) Isolation and characterisation of a high-efficiency desaturase and elongases from microalgae for transgenic LC-PUFA production. Mar Biotechnol 12:430–438
Petrie JR, Shrestha P, Mansour MP, Nichols PD, Liu Q, Singh SP (2010b) Metabolic engineering of omega-3 long-chain polyunsaturated fatty acids in plants using an acyl-CoA Δ6-desaturase with ω-3-preference from the marine microalga Micromonas pusilla. Metab Eng 12:233–240
Petrie JR, Vanhercke T, Shrestha P, El Tahchy A, White A, Zhou XR, Liu Q, Mansour MP, Nichols PD, Singh SP (2012) Recruiting a new substrate for triacylglycerol synthesis in plants: the monoacylglycerol acyltransferase pathway. PLoS One 7(4):e35214
Phan J, Reue K (2005) Lipin, a lipodystrophy and obesity gene. Cell Metab 1:73–83
Pineau B, Girard-Bascou J, Eberhard S, Choquet Y, Trémolières A, Gérard-Hirne C, Bennardo-Connan A, Decottignies P, Gillet S, Wollman FA (2004) A single mutation that causes phosphatidylglycerol deficiency impairs synthesis of photosystem II cores in Chlamydomonas reinhardtii. Eur J Biochem 271:329–338
Poppelreuther M, Rudolph B, Du C, Großmann R, Becker M, Thiele C, Ehehalt R, Füllekrug J (2012) The N-terminal region of acyl-CoA synthetase 3 is essential for both the localization on lipid droplets and the function in fatty acid uptake. J Lipid Res 53:888–900
Přibyl P, Cepák V, Zachleder V (2012) Production of lipids and formation and mobilization of lipid bodies in Chlorella vulgaris. J Appl Phycol 25:545–553
Prinz WA (2013) A bridge to understanding lipid droplet growth. Dev Cell 24:335–336
Qi B, Beaudoin F, Fraser T, Stobart AK, Napier JA, Lazarus CM (2002) Identification of a cDNA encoding a novel C18-D9 polyunsaturated fatty acid-specific elongating activity from the docosahexaenoic acid (DHA)-producing microalga, Isochrysis galbana. FEBS Lett 510:159–165
Qi B, Fraser T, Mugford S, Dobson G, Sayanova O, Butler J, Napier J, Stobart A, Lazarus C (2004) Production of very long chain polyunsaturated omega-3 and omega-6 fatty acids in plants. Nat Biotechnol 22:739–745
Raab A, Newcombe C, Pitton D, Ebel R, Feldmann J (2013) Comprehensive analysis of lipophilic arsenic species in a brown alga (Saccharina latissima). Anal Chem 85:2817–2824
Rabbani S, Beyer P, Lintig J, Hugueney P, Kleinig H (1998) Induced beta-carotene synthesis driven by triacylglycerol deposition in the unicellular alga Dunaliella bardawil. Plant Physiol 116:1239–1248
Radakovits R, Jinkerson RE, Darzins A, Posewitz MC (2010) Biofuels from eukaryotic microalgae. Eukaryot Cell 9:486–501
Radakovits R, Eduafo PM, Posewitz MC (2011) Genetic engineering of fatty acid chain length in Phaeodactylum tricornutum. Metab Eng 13:89–95
Rajakumari S, Daum G (2010a) Multiple functions as lipase, steryl ester hydrolase, phospholipase, and acyltransferase of Tgl4p from the yeast Saccharomyces cerevisiae. J Biol Chem 285:15769–15776
Rajakumari S, Daum G (2010b) Janus-faced enzymes yeast Tgl3p and Tgl5p catalyze lipase and acyltransferase reactions. Mol Biol Cell 21:501–510
Ratledge C, Cohen Z (2008) Microbial and algal lipids: do they have a future for biodiesel or as commodity oils? Lipid Technol 20:155–160
Ravina CG, Chang CI, Tsakraklides GP, McDermott JP, Vega JM, Leustek T, Gotor C, Davies JP (2002) The sac mutants of Chlamydomonas reinhardtii reveal transcriptional and posttranscriptional control of cysteine biosynthesis. Plant Physiol 130:2076–2084
Read BA, Kegel J, Klute MJ, Kuo A, Lefebvre SC, Maumus F, Mayer C, Miller J, Monier A, Salamov A, Young J, Aguilar M, Claverie JM, Frickenhaus S, Gonzalez K, Herman EK, Lin YC, Napier J, Ogata H, Sarno AF, Shmutz J, Schroeder D, de Vargas C, Verret F, von Dassow P, Valentin K, Van de Peer Y, Wheeler G, Dacks JB, Delwiche CF, Dyhrman ST, Glöckner G, John U, Richards T, Worden AZ, Zhang X, Grigoriev IV (2013) Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature 499:209–213
Recht L, Zarka A, Boussiba S (2012) Patterns of carbohydrate and fatty acid changes under nitrogen starvation in the microalgae Haematococcus pluvialis and Nannochloropsis sp. Appl Microbiol Biotechnol 94:1495–1503
Recht L, Töpfer N, Batushansky A, Sikron N, Gibon Y, Fait A, Nikoloski Z, Boussiba S, Zarka A (2014) Metabolite profiling and integrative modeling reveal metabolic constraints for carbon partitioning under nitrogen starvation in the green algae Haematococcus pluvialis. J Biol Chem 289:30387–30403
Reitan KI, Rainuzzo JR, Øie G, Olsen Y (1997) A review of the nutritional effects of algae in marine fish larvae. Aquaculture 155:207–221
Řezanka T, Lukavský J, Nedbalová L, Kolouchová I, Sigler K (2012) Effect of starvation on the distribution of positional isomers and enantiomers of triacylglycerol in the diatom Phaeodactylum tricornutum. Phytochemistry 80:17–27
Riekhof WR, Ruckle ME, Lydic TA, Sears BB, Benning C (2003) The sulfolipids sulfolipids 2′-O-acyl-sulfoquinovosyldiacylglycerol and sulfoquinovosyldiacylglycerol are absent from a Chlamydomonas reinhardtii mutant deleted in SQD1. Plant Physiol 133:864–874
Riekhof WR, Andre C, Benning C (2005a) Two enzymes, BtaA and BtaB, are sufficient for betaine lipid biosynthesis in bacteria. Arch Biochem Biophys 441:96–105
Riekhof WR, Sears BB, Benning C (2005b) Annotation of genes involved in glycerolipid biosynthesis in Chlamydomonas reinhardtii: discovery of the betaine lipid synthase BTA1(Cr). Eukaryot Cell 4:242–252
Riekhof WR, Wu J, Jones JL, Voelker DR (2007) Identification and characterization of the major lysophosphatidylethanolamine acyltransferase in Saccharomyces cerevisiae. J Biol Chem 282:28344–28352
Rismani-Yazdi H, Haznedaroglu B, Bibby K, Peccia J (2011) Transcriptome sequencing and annotation of the microalgae Dunaliella tertiolecta: pathway description and gene discovery for production of next-generation biofuels. BMC Genomics 12:148
Rismani-Yazdi H, Haznedaroglu BZ, Hsin C, Peccia J (2012) Transcriptomic analysis of the oleaginous microalga Neochloris oleoabundans reveals metabolic insights into triacylglyceride accumulation. Biotechnol Biofuels 5:74. doi:10.1186/1754-6834-5-74
Robert S, Petrie J, Zhou X-R, Mansour M, Blackburn S, Green A, Singh SP, Nichols PD (2009) Isolation and characterisation of a Δ5-fatty acid elongase from the marine microalga Pavlova salina. Mar Biotechnol 11:410–418
Robichaud PP, Boulay K, Munganyiki JÉ, Surette ME (2013) Fatty acid remodeling in cellular glycerophospholipids following the activation of human T cells. J Lipid Res 54:2665–2677
Roche SA, Leblond JD (2010) Betaine lipids in chlorarachniophytes. Phycol Res 58:298–305
Rodolfi L, Chini Zittelli G, Bassi N, Padovani G, Biondi N, Bonini G, Tredici MR (2009) Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 102:100–112
Roessler PG (1988) Changes in the activities of various lipid and carbohydrate biosynthetic enzymes in the diatom Cyclotella cryptica in response to silicon deficiency. Arch Biochem Biophys 267:521–528
Roessler PG (1990) Environmental control of glycerolipid metabolism in microalgae: commercial implications and future research directions. J Phycol 26:393–399
Roessler PG, Ohlrogge JB (1993) Cloning and characterization of the gene that encodes acetyl-coenzyme A carboxylase in the alga Cyclotella cryptica. J Biol Chem 268:19254–19259
Roessler PG, Bleibaum JL, Thompson GA, Ohlrogge JB (1994) Characteristics of the gene that encodes acetyl- CoA carboxylase in the diatom Cyclotella cryptica. Ann N Y Acad Sci 721:250–256
Rosenberg JN, Oyler GA, Wilkinson L, Betenbaugh MJ (2008) A green light for engineered algae: redirecting metabolism to fuel a biotechnology revolution. Curr Opin Biotechnol 19:430–436
Routaboul JM, Benning C, Bechtold N, Caboche M, Lepiniec L (1999) The TAG1 locus of Arabidopsis encodes for a diacylglycerol acyltransferase. Plant Physiol Biochem 37:831–840
Ruiz-López N, Garcés R, Harwood JL, Martínez-Force E (2010) Characterization and partial purification of acyl-CoA:glycerol 3-phosphate acyltransferase from sunflower (Helianthus annuus L.) developing seeds. Plant Physiol Biochem 48:73–80
Ruiz-López NR, Haslam RP, Usher SL, Napier JA, Sayanova O (2013) Reconstitution of EPA and DHA Biosynthesis in Arabidopsis: iterative metabolic engineering for the synthesis of n-3 LC-PUFAs in transgenic plants. Metab Eng 17:3
Saha S, Enugutti B, Rajakumari S, Rajasekharan R (2006) Cytosolic triacylglycerol biosynthetic pathway in oilseeds. Molecular cloning and expression of peanut cytosolic diacylglycerol acyltransferase. Plant Physiol 141:1533–1543
Sakaki T, Saito K, Kawaguchi A, Kondo N, Yamada M (1990) Conversion of monogalactosyldiacylglycerols to triacylglycerols in ozone-fumigated spinach leaves. Plant Physiol 94:766–772
Sakurai I, Mizusawa N, Wada H, Sato N (2007) Digalactosyldiacylglycerol is required for stabilization of the oxygen-evolving complex in photosystem II. Plant Physiol 145:1361–1370
Salas JJ, Ohlrogge JB (2002) Characterization of substrate specificity of plant FatA and FatB acyl-ACP thioesterases. Arch Biochem Biophys 403:25–34
Sanda S, Leustek T, Theisen MJ, Garavito RM, Benning C (2001) Recombinant Arabidopsis SQD1 converts UDP-glucose and sulfite to the sulfolipid head group precursor UDP-sulfoquinovose in vitro. J Biol Chem 276:3941–3946
Sandager L, Gustavsson MH, Ståhl U, Dahlqvist A, Wiberg E, Banas A, Lenman M, Ronne H, Stymne S (2002) Storage lipid synthesis is non-essential in yeast. J Biol Chem 277:6478–6482
Sanjaya, Miller R, Durrett TP, Kosma DK, Lydic TA, Muthan B, Koo AJK, Bukhman YV, Reid GE, Howe GA, Ohlrogge J, Benning C (2013) Altered lipid composition and enhanced nutritional value of Arabidopsis leaves following introduction of an algal diacylglycerol acyltransferase 2. Plant Cell 25:677–693
Sasaki Y, Nagano Y (2004) Plant acetyl-CoA carboxylase: structure, biosynthesis, regulation, and gene manipulation for plant breeding. Biosci Biotechnol Biochem 68:1175–1184
Sasaki Y, Kozaki A, Hatano M (1997) Link between light and fatty acid synthesis: thioredoxin-linked reductive activation of plastidic acetyl-CoA carboxylase. Proc Natl Acad Sci U S A 94:11096–11101
Sato N (1988) Dual role of methionine in the biosynthesis of diacylglyceryltrimethylhomoserine in Chlamydomonas reinhardtii. Plant Physiol 86:931–934
Sato N (1991) Lipids in Cryptomonas CR-1. II. Biosynthesis of betaine lipids and galactolipids. Plant Cell Physiol 32:845–851
Sato N (2004) Roles of the acidic lipids sulfoquinovosyl diacylglycerol and phosphatidylglycerol in photosynthesis: their specificity and evolution. J Plant Res 117:495–505
Sato N, Moriyama T (2007) Genomic and biochemical analysis of lipid biosynthesis in the unicellular rhodophyte Cyanidioschyzon merolae: lack of a plastidic desaturation pathway results in the coupled pathway of galactolipidsynthesis. Eukaryot Cell 6:1006–1017
Sato N, Sonoike K, Tsuzuki M, Kawaguchi A (1995a) Impaired photosystem II in a mutant of Chlamydomonas reinhardtii defective in sulfoquinovosyl diacylglycerol. Eur J Biochem 234:16–23
Sato N, Tsuzuki M, Matsuda M, Ehara T, Osafune T, Kawaguchi A (1995b) Isolation and characterization of mutants affected in lipid metabolism of Chlamydomonas reinhardtii. Eur J Biochem 230:987–993
Sato N, Aoki M, Maru H, Sonoike K, Minoda A, Tsuzuki M (2003a) Involvement of sulfoquinovosyl diacylglycerol in the structural integrity and heat-tolerance of photosystem II. Planta 217:245–251
Sato N, Sugimoto K, Meguro A, Tsuzuki M (2003b) Identification of a gene for UDP-sulfoquinovose synthase of a green alga, Chlamydomonas reinhardtii, and its phylogeny. DNA Res 10:229–237
Sato N, Tsuzuki M, Kawaguchi A (2003c) Glycerolipid synthesis in Chlorella kessleri 11h. I. Existence of a eukaryotic pathway. Biochim Biophys Acta 1633:27–34
Sato A, Matsumura R, Hoshino N, Tsuzuki M, Sato N (2014) Responsibility of regulatory gene expression and repressed protein synthesis for triacylglycerol accumulation on sulfur-starvation in Chlamydomonas reinhardtii. Front Plant Sci 5:444. doi:10.3389/fpls.2014.00444
Sayanova OV, Napier JA (2004) Eicosapentaenoic acid: biosynthetic routes and the potential for synthesis in transgenic plants. Phytochemistry 65:147–158
Sayanova O, Napier JA (2011) Transgenic oilseed crops as an alternative to fish oils. Prostaglandins Leukot Essent Fat Acids 85:253–260
Sayanova O, Haslam RP, Calerón MV, López NR, Worthy C, Rooks P, Allen MJ, Napier JA (2011) Identification and functional characterisation of genes encoding the omega-3 polyunsaturated fatty acid biosynthetic pathway from the coccolithophore Emiliania huxleyi. Phytochemistry 72:594–600
Schaller S, Latowski D, Jemioła-Rzemińska M, Wilhelm C, Strzałka K, Goss R (2010) The main thylakoid membrane lipid monogalactosyldiacylglycerol (MGDG) promotes the de-epoxidation of violaxanthin associated with the light-harvesting complex of photosystem II (LHCII). Biochim Biophys Acta 1797:414–424
Schlapfer P, Eichenberger W (1983) Evidence for the involvement of diacylglyceryl(N, N, N-trimethyl)-homoserine in the desaturation of oleic and linoleic acids in Chlamydomonas reinhardtii (Chlorophyceae). Plant Sci 32:243–252
Schmollinger S, Mühlhaus T, Boyle NR, Blaby IK, Casero D, Mettler T, Moseley JL, Kropat J, Sommer F, Strenkert D, Hemme D, Pellegrini M, Grossman AR, Stitt M, Schroda M, Merchant SS (2014) Nitrogen-sparing mechanisms in Chlamydomonas affect the transcriptome, the proteome, and photosynthetic metabolism. Plant Cell 26:1410–1435
Schneider JC, Roessler P (1994) Radiolabeling studies of lipids and fatty acids in Nannochloropsis (Eustigmatophyceae), an oleaginous marine alga. J Phycol 30:594–598
Schneider JC, Livne A, Sukenik A, Roessler P (1995) A mutant of Nannochloropsis deficient in eicosapentaenoic acid production. Phytochemistry 40:807–814
Schnurr JA, Shockey JM, de Boer GJ, Browse JA (2002) Fatty acid export from the chloroplast. Molecular characterization of a major plastidial acyl-coenzyme A synthetase from Arabidopsis. Plant Physiol 129:1700–1709
Schwender J, Ohlrogge JB, Shachar-Hill Y (2003) A flux model of glycolysis and the oxidative pentose phosphate pathway in developing Brassica napus embryos. J Biol Chem 278:29442–29453
Scott SA, Davey MP, Dennis JS, Horst I, Howe CJ, Lea-Smith DJ, Smith AG (2010) Biodiesel from algae: challenges and prospects. Curr Opin Biotechnol 21:1–10
Shanklin J, Cahoon EB (1998) Desaturation and related modifications of fatty acids. Annu Rev Plant Physiol Plant Mol Biol 49:611–641
Shanklin J, Whittle E, Fox BG (1994) Eight histidine residues are catalytically essential in a membrane-associated iron enzyme, stearoyl-CoA desaturase, and are conserved in alkane hydroxylase and xylene monooxygenase. Biochemistry 33:12787–12794
Shanklin J, Guy JE, Mishra G, Lindqvist Y (2009) Desaturases: emerging models for understanding functional diversification of diiron-containing enzymes. J Biol Chem 284:18559–18563
Sheehan J, Dunahay T, Benemann J, Roessler P (1998) A look back at the U.S. Department of Energy’s aquatic species program: biodiesel from algae, Close-out report TP-580-24190. National Renewable Energy Laboratory, Golden
Sheffer M, Fried A, Gottlieb HE, Tietz A, Avron M (1986) Lipidcomposition of the plasma-membrane ofthe holotolerant alga, Dunaliella salina. Biochim Biophys Acta 857:165–172
Shimojima M (2011) Biosynthesis and functions of the plant sulfolipid. Prog Lipid Res 50:234–239
Shockey J, Browse J (2011) Genome-level and biochemical diversity of the acyl-activating enzyme superfamily in plants. Plant J 66:143–160
Shockey JM, Gidda SK, Chapital DC, Kuan JC, Dhanoa PK, Bland JM, Rothstein SJ, Mullen RT, Dyer JM (2006) Tung tree DGAT1 and DGAT2 have nonredundant functions in triacylglycerol biosynthesis and are localized to different subdomains of the endoplasmic reticulum. Plant Cell 18:2294–2313
Shrestha P, Cohen D, Khalilov I, Khozin-Goldberg I, Cohen Z (2004) Triacylglycerol biosynthesis in microsomes and oil bodies of the oleaginous green alga Parietochloris incisa. In: Proceedings of 16th international plant lipid symposium, 1–4 June, 2004, Budapest, Hungary. Retrieved from http://www.mete.mtesz.hu/pls/proceedings
Shtaida N, Khozin-Goldberg I, Solovchenko A, Chekanov K, Didi-Cohen S, Leu S, Cohen Z, Boussiba S (2014) Downregulation of a putative plastid PDC E1α subunit impairs photosynthetic activity and triacylglycerol accumulation in nitrogen-starved photoautotrophic Chlamydomonas reinhardtii. J Exp Bot 65:6563–6576
Shtaida N, Khozin-Goldberg I, Boussiba S (2015) The role of pyruvate hub enzymes in supplying carbon precursors for fatty acid synthesis in photosynthetic microalgae. Photosynth Res 125:407–422
Siaut M, Cuiné S, Cagnon C, Fessler B, Nguyen M, Carrier P, Beyly A, Beisson F, Triantaphylidès C, Li-Beisson Y, Peltier G (2011) Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnol 11:7
Siegenthaler PA, Trémolières A (1998) Role of acyl lipids in the function of photosynthetic membranes in higher plants. In: Siegenthaler PA, Murata N (eds) Lipids in photosynthesis: structure, function and genetics. Kluwer, Dordrecht, pp 145–173
Siloto RM, Findlay K, Lopez-Villalobos A, Yeung EC, Nykiforuk C, Moloney MM (2006) The accumulation of oleosins determines the size of seed oil bodies in Arabidopsis. Plant Cell 18:1961–1974
Siloto RM, Truksa M, He X, McKeon T, Weselake RJ (2009) Simple methods to detect triacylglycerol biosynthesis in a yeast-based recombinant system. Lipids 44:963–973
Simionato D, Block MA, La Rocca N, Jouhet J, Maréchal E, Finazzi G, Morosinotto T (2013) The response of Nannochloropsis gaditana to nitrogen starvation includes de novo biosynthesis of triacylglycerols, a decrease of chloroplast galactolipids, and reorganization of the photosynthetic apparatus. Eukaryot Cell 12:665–676
Simopoulos AP (2002) Omega-3 fatty acids in inflammation and autoimmune diseases. J Am Coll Nutr 21:495–505
Simopoulos AP (2008) The importance of the ω-6/ω-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp Biol Med 233:674–688
Slack CR, Campbell LC, Browse JA, Roughan PG (1983) Some evidence for the reversibility of the cholinephosphotransferasecatalysed reaction in developing linseed cotyledons in vivo. Biochim Biophys Acta 754:10–20
Slack CR, Roughan PG, Browse JA, Gardiner SE (1985) Some properties of cholinephosphotransferase from developing safflower cotyledons. Biochim Biophys Acta 833:438–448
Slocombe SP, Cornah J, Pinfield-Wells H, Soady K, Zhang Q, Gilday A, Dyer JM, Graham IA (2009) Oil accumulation in leaves directed by modification of fatty acid breakdown and lipid synthesis pathways. Plant Biotechnol J 7:694–703
Smith S, Tsai SC (2007) The type I fatty acid and polyketide synthases: a tale of two megasynthases. Nat Prod Rep 24:1041–1072
Smith SR, Abbriano RM, Hildebrand M (2012) Comparative analysis of diatom genomes reveals substantial differences in the organization of carbon partitioning pathways. Algal Res 1:2–16
Snyder CL, Yurchenko OP, Siloto RM, Chen X, Liu Q, Mietkiewska E, Weselake RJ (2009) Acyltransferase action in modification of seed oil biosynthesis. Nat Biotechnol 26:11–16
Solovchenko A (2012) Physiological role of neutral lipid accumulation in eukaryotic microalgae under stresses. Russ J Plant Physiol 59:167–176
Solovchenko A, Khozin-Goldberg I (2013) High-CO2 tolerance in microalgae: possible mechanisms and implications for biotechnology and bioremediation. Biotechnol Lett 35:1745–1752
Solovchenko AE, Khozin-Goldberg I, Didi-Cohen S, Cohen Z, Merzlyak MN (2008) Effects of light and nitrogen starvation on the content and composition of carotenoids of the green microalga Parietochloris incisa. Russ J Plant Physiol 55:455–462
Solovchenko A, Merzlyak M, Khozin-Goldberg I, Cohen Z, Boussiba S (2010) Coordinated carotenoid and lipid syntheses induced in Parietochloris incisa (Chlorophyta, Trebouxiophyceae) mutant deficient in Δ5 desaturase by nitrogen starvation and high light. J Phycol 46:763–772
Solovchenko A, Chivkunova O, Semenova L, Selyakh I, Scherbakov P, Karpova E, Lobakova E (2013a) Stress-induced changes in pigment and fatty acid content in the microalga Desmodesmus sp. isolated from a white seahydroid. Russ J Plant Physiol 60:313–321
Solovchenko A, Solovchenko O, Didi-Cohen S, Pal D, Cohen Z, Boussiba S (2013b) Probing the effects of high-light stress on pigment and lipid metabolism in nitrogen-starving microalgae by measuring chlorophyll fluorescence transients: studies with a ∆5 desaturase mutant of Parietochloris incisa (Chlorophyta, Trebouxiophyceae). Algal Res 2:175–182
Somerville C, Browse J (1991) Plant lipids: metabolism, mutants, and membranes. Science 252:80–87
Somerville CR, Browse JA (1996) Dissecting desaturation; plants prove advantageous. Trends Cell Biol 6:148–153
Sprecher H (2000) Metabolism of highly unsaturated n-3 and n-6 fatty acids. Biochim Biophys Acta 1486:219–231
Ståhl U, Carlsson AS, Lenman M, Dahlqvist A, Huang B, Banas W, Banas A, Stymne S (2004) Cloning and functional characterization of a phospholipid: diacylglycerol acyltransferase from Arabidopsis. Plant Physiol 135:1324–1335
Stefanov K, Seizova K, Elenkov I, Kuleva L, Popov S, Dimitrova-Konaklieva S (1994) Lipid composition of the red alga Chondria tenuissima (Good et Wood.) Ag., inhabiting waters with different salinities. Bot Mar 37:445–448
Stephens E, Ross IL, Mussgnug JH, Wagner LD, Borowitzka MA, Posten C, Kruse O, Hankamer B (2010) Future prospects of microalgal biofuel production systems. Trends Plant Sci 15:554–564
Stobart K, Mancha M, Lenman M, Dahlqvist A, Stymne S (1997) Triacylglycerols are synthesised and utilized by transacylation reactions in microsomal preparations of developing safflower (Carthamus tinctorius L.) seeds. Planta 203:58–66
Stone SJ, Levin MC, Zhou P, Han J, Walther TC, Farese RV Jr (2009) The endoplasmic reticulum enzyme DGAT2 is found in mitochondria associated membranes and has a mitochondrial targeting signal that promotes its association with mitochondria. J Biol Chem 284:5352–5361
Sugimoto K, Sato N, Tsuzuki M (2007) Utilization of a chloroplast membrane sulfolipid as a major internal sulfur source for protein synthesis in the early phase of sulfur starvation in Chlamydomonas reinhardtii. FEBS Lett 581:4519–4522
Sugimoto K, Midorikawa T, Tsuzuki M, Sato N (2008) Upregulation of PG synthesis on sulfur-starvation for PS I in Chlamydomonas. Biochem Biophys Res Commun 369:660–665
Sugimoto K, Tsuzuki M, Sato N (2010) Regulation of synthesis and degradation of a sulfolipid under sulfur-starved conditions and its physiological significance in Chlamydomonas reinhardtii. New Phytol 185:676–686
Sukenik A (1999) Production of eicosapentaenoic acid by the marine eustigmatophyte Nannochloropsis. In: Cohen Z (ed) Chemicals from microalgae. Taylor and Francis, London, pp 41–56
Sukenik A, Carmeli Y (1990) Lipid synthesis and fatty acid composition in Nannochloropsis sp. (Eustigmatophyceae) grown in a light-dark cycle. J Phycol 26:463–469
Sukenik A, Yamaguchi Y, Livne A (1993) Alterations in lipid molecular species of the marine eustigmatophyte Nannochlorosis sp. J Phycol 29:620–626
Sukenik A, Beardall J, Kromkamp JC, Kopeck J, Masojídek J, van Bergeijk S, Gabai S, Shaham E, Yamshon A (2009) Photosynthetic performance of outdoor Nannochloropsis mass cultures under a wide range of environmental conditions. Aquat Microb Ecol 56:297–308
Tai M, Stephanopoulos G (2013) Engineering the push and pull of lipid biosynthesis in oleaginous yeast Yarrowia lipolytica for biofuel production. Metab Eng 15:1–9
Tanaka T, Maeda Y, Veluchamy A, Tanaka M, Abida H, Maréchal E, Bowler C, Muto M, Sunaga Y, Tanaka M, Yoshino T, Taniguchi T, Fukuda Y, Nemoto M, Matsumoto M, Wong PS, Aburatani S, Fujibuchi W (2015) Oil accumulation by the oleaginous diatom Fistulifera solaris as revealed by the genome and transcriptome. Plant Cell 27:162–176
Tardif M, Atteia A, Specht M, Cogne G, Rolland N, Brugière S, Hippler M, Ferro M, Bruley C, Peltier G, Vallon O, Cournac L (2012) PredAlgo: a new subcellular localization prediction tool dedicated to green algae. Mol Biol Evol 29:3625–3639
Terashima M, Specht M, Hippler M (2011) The chloroplast proteome: a survey from the Chlamydomonas reinhardtii perspective with a focus on distinctive features. Curr Genet 57:151–168
Thompson GA (1996) Lipids and membrane function in green algae. Biochim Biophys Acta 1302:17–45
Tonon T, Harvey D, Larson TR, Graham IA (2002a) Identification of a very long chain polyunsaturated fatty acid Δ 4-desaturase from the microalga Pavlova lutheri. FEBS Lett 553:440–444
Tonon T, Harvey D, Larson TR, Graham IA (2002b) Long chain polyunsaturated fatty acid production and partitioning to triacylglycerols in four microalgae. Phytochemistry 61:15–24
Tonon T, Harvey D, Qing R, Li Y, Larson TR, Graham IA (2004) Identification of a fatty acid Δ11-desaturase from the microalga Thalassiosira pseudonana. FEBS Lett 563:28–34
Tonon T, Qing R, Harvey D, Li Y, Larson TR, Graham IA (2005a) Identification of a long-chain polyunsaturated fatty acid acyl-coenzyme A synthetase from the diatom Thalassiosira pseudonana. Plant Physiol 138:402–408
Tonon T, Sayanova O, Michaelson LV, Qing R, Harvey D, Larson TR, Li Y, Napier JA, Graham IA (2005b) Fatty acid desaturases from the microalga Thalassiosira pseudonana. FEBS J 272:3401–3412
Tredici M (2010) Photobiology of microalgae mass cultures: understanding the tools for the next green revolution. Biofuels 1:143–162
Trentacoste EM, Shrestha RP, Smith SR, Glé C, Hartmann AC, Hildebrand M, Gerwick WH (2013) Metabolic engineering of lipid catabolism increases microalgal lipid accumulation without compromising growth. Proc Natl Acad Sci U S A 110:19748–19753
Troncoso-Ponce MA, Cao X, Yang Z, Ohlrogge JB (2013) Lipid turnover during senescence. Plant Sci 205–206:13–19
Tsai CH, Warakanont J, Takeuchi T, Sears BB, Moellering ER, Benning C (2014) The protein compromised hydrolysis of triacylglycerols 7 (CHT7) acts as a repressor of cellular quiescence in Chlamydomonas. Proc Natl Acad Sci U S A 111:15833–15838
Tsai CH, Zienkiewicz K, Amstutz CL, Brink BG, Warakanont J, Roston R, Benning C (2015) Dynamics of protein and polar lipid recruitment during lipid droplet assembly in Chlamydomonas reinhardtii. Plant J 83:650–660
Tumaney AW, Shekar S, Rajasekharan R (2001) Identification, purification, and characterization of monoacylglycerol acyltransferase from developing peanut cotyledons. J Biol Chem 276:10847–10852
Urzica EI, Vieler A, Hong-Hermesdorf A, Page MD, Casero D, Gallaher SD, Kropat J, Pellegrini M, Benning C, Merchant SS (2013) Remodeling of membrane lipids in iron starved Chlamydomonas. J Biol Chem 288:30246–30258
Valenzuela J, Mazurie A, Carlson R, Gerlach R, Cooksey K, Peyton B, Fields M (2012) Potential role of multiple carbon fixation pathways during lipid accumulation in Phaeodactylum tricornutum. Biotechnol Biofuels 5:1–17
van Erp H, Bates PD, Burgal J, Shockey J, Browse J (2011) Castor phospholipid: diacylglycerol acyltransferase facilitates efficient metabolism of hydroxy fatty acids in transgenic Arabidopsis. Plant Physiol 155:683–693
van Lis R, Baffert C, Couté Y, Nitschke W, Atteia A (2013) Chlamydomonas reinhardtii chloroplasts contain a homodimeric pyruvate: ferredoxin oxidoreductase that functions with FDX1. Plant Physiol 161:57–71
Van Mooy BAS, Fredricks HF, Pedler BE, Dyhrman ST, Karl DM, Koblízek M, Lomas MW, Mincer TJ, Moore LR, Moutin T, Rappé MS, Webb EA (2009) Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature 458:69–72
Vanhercke T, El Tahchy A, Shrestha P, Zhou XR, Singh SP, Petrie JR (2013) Synergistic effect of WRI1 and DGAT1 coexpression on triacylglycerol biosynthesis in plants. FEBS Lett 587:364–369
Vieler A, Wilhelm C, Goss R, Süss R, Schiller J (2007) The lipid composition of the unicellular green alga Chlamydomonas reinhardtii and the diatom Cyclotella meneghiniana investigated by MALDI-TOF MS and TLC. Chem Phys Lipids 150:143–155
Vieler A, Brubaker SB, Vick B, Benning C (2012a) A lipid droplet protein of Nannochloropsis with functions partially analogous to plant oleosins. Plant Physiol 158:1562–1569
Vieler A, Wu G, Tsai CH, Bullard B, Cornish AJ, Harvey C, Reca IB, Thornburg C, Achawanantakun R, Buehl CJ, Campbell MS, Cavalier D, Childs KL, Clark TJ, Deshpande R, Erickson E, Armenia Ferguson A, Handee W, Kong Q, Li X, Liu B, Lundback S, Peng C, Roston RL, Sanjaya, Simpson JP, Terbush A, Warakanont J, Zäuner S, Farre EM, Hegg EL, Jiang N, Kuo MH, Lu Y, Niyogi KK, Ohlrogge J, Osteryoung KW, Shachar-Hill Y, Sears BB, Sun Y, Takahashi H, Yandell M, Shiu SH, Benning C (2012b) Genome, functional gene annotation, and nuclear transformation of the heterokont oleaginous alga Nannochloropsis sp. CCMP1779. PLoS Genet 8:e1003064
Voelker T, Kinney AJ (2001) Variations in the biosynthesis of seed-storage lipids. Annu Rev Plant Physiol Plant Mol Biol 52:335–361
Voelker TA, Worrell AC, Anderson L, Bleibaum J, Fan C, Hawkins DJ, Radke SE, Davies HM (1992) Fatty acid biosynthesis redirected to medium chains in transgenic oilseed plants. Science 257:72–74
Vogel G, Browse J (1996) Cholinephosphotransferase and diacylglycerol acyltransferase (substrate specificities at a key branch point in seed lipid metabolism. Plant Physiol 110:923–931
Vogel G, Eichenberger W (1992) Betaine lipids in lower plants. Biosynthesis of DGTS and DGTA in Ochromonas danica (Chrysophyceae) and the possible role of DGTS in lipid metabolism. Plant Cell Physiol 33:427–436
Volkman JK, Dunstan GA, Jefrey SW, Kearney PS (1991) Fatty acids from microalgae of the genus Pavlova. Phytochemistry 30:1855–1859
Volkman JK, Brown MR, Dunstan GA, Jeffrey SW (1993) Biochemical composition of marine microalgae from the class Eustigmatophyceae. J Phycol 29:69–78
Wagner A, Daum G (2005) Formation and mobilization of neutral lipids in the yeast Saccharomyces cerevisiae. Biochem Soc Trans 33:1174–1177
Wagner M, Hoppe K, Czabany T, Heilmann M, Daum G, Feussner I, Fulda M (2010) Identification and characterization of an acyl-CoA: diacylglycerol acyltransferase 2 (DGAT2) gene from the microalga O. tauri. Plant Physiol Biochem 48:407–416
Wallis JG, Browse J (1999) The Δ8-desaturase of Euglena gracilis: an alternate pathway for synthesis of 20-carbon polyunsaturated fatty acids. Arch Biochem Biophys 365:307–316
Wallis JG, Watts JL, Browse J (2002) Polyunsaturated fatty acid synthesis: what will they think of next? Trends Biochem Sci 27:467–473
Wältermann M, Stöveken T, Steinbüchel A (2007) Key enzymes for biosynthesis of neutral lipid storage compounds in prokaryotes: properties, function and occurrence of wax ester synthases/acyl-CoA: diacylglycerol acyltransferases. Biochimie 89:230–242
Walther TC, Farese RV Jr (2009) The life of lipid droplets. Biochim Biophys Acta 1791:459–466
Wan M, Liu P, Xia J, Rosenberg JN, Oyler GA, Betenbaugh MJ, Nie Z, Qiu G (2011) The effect of mixotrophy on microalgal growth, lipid content, and expression levels of three pathway genes in Chlorella sorokiniana. Appl Microbiol Biotechnol 91:835–844
Wang Z, Benning C (2012) Chloroplast lipid synthesis and lipid trafficking through ER-plastid membrane contact sites. Biochem Soc Trans 40:457–463
Wang ZT, Ullrich N, Joo S, Waffenschmidt S, Goodenough U (2009) Algal lipid bodies: stress induction, purification, and biochemical characterization in wild-type and starchless Chlamydomonas reinhardtii. Eukaryot Cell 8:1856–1868
Wang H, Alvarez S, Hicks LM (2012a) Comprehensive comparison of iTRAQ and label-free LC-based quantitative proteomics approaches using two Chlamydomonas reinhardtii strains of interest for biofuels engineering. J Proteome Res 11:487–501
Wang L, Shen W, Kazachkov M, Chen G, Chen Q, Carlsson AS, Stymne S, Weselake RJ, Zou J (2012b) Metabolic interactions between the Lands cycle and the Kennedy pathway of glycerolipid synthesis in Arabidopsis developing seeds. Plant Cell 24:4652–4669
Wang Z, Anderson NS, Benning C (2013) The phosphatidic acid binding site of the Arabidopsis trigalactosyldiacylglycerol 4 (TGD4) protein required for lipid import into chloroplasts. J Biol Chem 288:4763–4771
Wang D, Ning K, Li J, Hu J, Han D, Wang H, Zeng X, Jing X, Zhou Q, Su X et al (2014) Nannochloropsis genomes reveal evolution of microalgal oleaginous traits. PLoS Genet 10(1):e1004094
Weber AP, Linka N (2011) Connecting the plastid: transporters of the plastid envelope and their role in linking plastidial with cytosolic metabolism. Annu Rev Plant Biol 62:53–77
Wendel AA, Lewin TM, Coleman RA (2009) Glycerol-3-phosphate acyltransferases: rate limiting enzymes of triacylglycerol biosynthesis. Biochim Biophys Acta 1791:501–506
Weselake RJ, Shah S, Tang M, Quant PA, Snyder CL, Furukawa-Stoffer TL, Zhu W, Taylor DC, Zou J, Kumar A, Hall L, Laroche A, Rakow G, Raney P, Moloney MM, Harwood JL (2008) Metabolic control analysis is helpful for informed genetic manipulation of oilseed rape (Brassica napus) to increase seed oil content. J Exp Bot 59:3543–3549
Weselake RJ, Taylor DC, Rahman MH, Shah S, Laroche A, McVetty PB, Harwood JL (2009) Increasing the flow of carbon into seed oil. Biotechnol Adv 27:866–878
Wijffels RH, Barbosa MJ (2010) An outlook on microalgal biofuels. Science 329:796–799
Wilfling F, Wang H, Haas JT, Krahmer N, Gould TJ, Uchida A, Cheng JX, Graham M, Christiano R, Fröhlich F, Liu X, Buhman KK, Coleman RA, Bewersdorf J, Farese RV Jr, Walther TC (2013) Triacylglycerol synthesis enzymes mediate lipid droplet growth by relocalizing from the ER to lipid droplets. Dev Cell 24:384–399
Work VH, Radakovits R, Jinkerson RE, Meuser JE, Elliott LG, Vinyard DJ, Laurens LM, Dismukes GC, Posewitz MC (2010) Increased lipid accumulation in the Chlamydomonas reinhardtii sta7-10 starchless isoamylase mutant and increased carbohydrate synthesis in complemented strains. Eukaryot Cell 9:1251–1261
Wu W, Ping W, Wu H, Li M, Gu D, Xu Y (2013) Monogalactosyldiacylglycerol deficiency in tobacco inhibits the cytochrome b6f-mediated intersystem electron transport process and affects the photostability of the photosystem II apparatus. Biochim Biophys Acta 1827:709–722
Xu C, Härtel H, Wada H, Hagio M, Yu B, Eakin C, Benning C (2002) The pgp1 mutant locus of Arabidopsis encodes a phosphatidylglycerolphosphate synthase with impaired activity. Plant Physiol 129:594–604
Xu C, Fan J, Riekhof W, Froehlich JE, Benning C (2003) A permease-like protein involved in ER to thylakoid lipid transfer in Arabidopsis. EMBO J 22:2370–2379
Xu C, Yu B, Cornish AJ, Froehlich JE, Benning C (2006) Phosphatidylglycerol biosynthesis in chloroplasts of Arabidopsis mutants deficient in acyl-ACP glycerol-3- phosphate acyltransferase. Plant J 47:296–309
Xu J, Zheng Z, Zou J (2009) A membrane-bound glycerol-3-phosphate acyltransferase from Thalassiosira pseudonana regulates acyl composition of glycerolipids. Botany 87:544–551
Xu J, Chen D, Yan X, Chen J, Zhou C (2010) Global characterization of the photosynthetic glycerolipids from a marine diatom Stephanodiscus sp. by ultra performance liquid chromatography coupled with electrospray ionization-quadrupole-time of flight mass spectrometry. Anal Chim Acta 663:60–68
Yamaoka Y, Yu Y, Mizoi J, Fujiki Y, Saito K, Nishijima M, Lee Y, Nishida I (2011) PHOSPHATIDYLSERINE SYNTHASE1 is required for microspore development in Arabidopsis thaliana. Plant J 67:648–661
Yang W, Mason CB, Pollock SV, Lavezzi T, Moroney JV, Moore TS (2004a) Membrane lipid biosynthesis in Chlamydomonas reinhardtii: expression and characterization of CTP: phosphoethanolamine cytidylyltransferase. Biochem J 382:51–57
Yang W, Moroney JV, Moore TS (2004b) Membrane lipid biosynthesis in Chlamydomonas reinhardtii: ethanolaminephosphotransferase is capable of synthesizing both phosphatidylcholine and phosphatidylethanolamine. Arch Biochem Biophys 430:198–209
Yang L, Ding Y, Chen Y, Zhang S, Huo C, Wang Y, Yu J, Zhang P, Na H, Zhang H, Ma Y, Liu P (2012a) The proteomics of lipid droplets: structure, dynamics, and functions of the organelle conserved from bacteria to humans. J Lipid Res 53:1245–1253
Yang W, Simpson JP, Li-Beisson Y, Beisson F, Pollard M, Ohlrogge JB (2012b) A land-plant-specific glycerol-3-phosphate acyltransferase family in Arabidopsis: substrate specificity, sn-2 preference, and evolution. Plant Physiol 160:638–652
Yang ZK, Niu YF, Ma YH, Xue J, Zhang MH, Yang WD, Liu JS, Lu SH, Guan Y, Li HY (2013) Molecular and cellular mechanisms of neutral lipid accumulation in diatom following nitrogen deprivation. Biotechnol Biofuels 6(1):67
Yen CL, Farese RV Jr (2003) MGAT2, a monoacylglycerol acyltransferase expressed in the small intestine. J Biol Chem 278:18532–18537
Yen CL, Stone SJ, Cases S, Zhou P, Farese RV Jr (2002) Identification of a gene encoding MGAT1, a monoacylglycerol acyltransferase. Proc Natl Acad Sci U S A 99:8512–8517
Yen CL, Stone SJ, Koliwad S, Harris C, Farese RV Jr (2008) Thematic review series: glycerolipids. DGAT enzymes and triacylglycerol biosynthesis. J Lipid Res 49:2283–2301
Yongmanitchai W, Ward OP (1993) Positional distribution of fatty acids, and molecular species of polar lipids, in the diatom Phaeodactylum tricornutum. J Gen Microbiol 139:465–472
Yoon K, Han D, Li Y, Sommerfeld M, Hu Q (2012) 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 24:3708–3724
Yu B, Benning C (2003) Anionic lipids are required for chloroplast structure and function in Arabidopsis. Plant J 36:762–770
Yu B, Xu C, Benning C (2002) Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proc Natl Acad Sci U S A 99:5732–5737
Yu B, Wakao S, Fan J, Benning C (2004) Loss of plastidic lysophosphatidic acid acyltransferase causes embryo-lethality in Arabidopsis. Plant Cell Physiol 45:503–510
Yu ET, Zendejas FJ, Lane PD, Gaucher S, Simmons BA, Lane TW (2009) Triacylglycerol accumulation and profiling in the model diatoms Thalassiosira pseudonana and Phaeodactylum tricornutum (Baccilariophyceae) during starvation. J Appl Phycol 21:669–681
Yuzawa Y, Nishihara H, Haraguchi T, Masuda S, Shimojima M, Shimoyama A, Yuasa H, Okada N, Ohta H (2012) Phylogeny of galactolipid synthase homologs together with their enzymatic analyses revealed a possible origin and divergence time for photosynthetic membrane biogenesis. DNA Res 19:91–102
Zabawinski C, Van Den Koornhuyse N, D’Hulst C, Schlichting R, Giersch C, Delrue B, Lacroix JM, Preiss J, Ball S (2001) Starchless mutants of Chlamydomonas reinhardtii lack the small subunit of a heterotetrameric ADP-glucose pyrophosphorylase. J Bacteriol 183:1069–1077
Zäuner S, Jochum W, Bigorowski T, Benning C (2012) A cytochrome b5-containing plastid-located fatty acid desaturase from Chlamydomonas reinhardtii. Eukaryot Cell 11:856–863
Zehmer JK, Huang Y, Peng G, Pu J, Anderson RG, Liu P (2009) A role for lipid droplets in inter-membrane lipid traffic. Proteomics 9:914–921
Zhang Z, Shrager J, Jain M, Chang CW, Vallon O, Grossman AR (2004) Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot Cell 3:1331–1348
Zhang M, Fan J, Taylor DC, Ohlrogge JB (2009) DGAT1 and PDAT1 acyltransferases have overlapping functions in Arabidopsis triacylglycerol biosynthesis and are essential for normal pollen and seed development. Plant Cell 21:3885–3901
Zhang H, Damude HG, Yadav NS (2012a) Three diacylglycerol acyltransferases contribute to oil biosynthesis and normal growth in Yarrowia lipolytica. Yeast 29:25–38
Zhang L, Ma XL, Pan KH, Yang GP, Yu WG, Zhu BH (2012b) Isolation and characterization of a long-chain acyl-coenzyme A synthetase encoding gene from the marine microalga Nannochloropsis oculata. J Appl Phycol 24:873–880
Zhang C, Iskandarov U, Klotz ET, Stevens RL, Cahoon RE, Nazarenus TJ, Pereira SL, Cahoon EB (2013) A thraustochytrid diacylglycerol acyltransferase 2 with broad substrate specificity strongly increases oleic acid content in engineered Arabidopsis thaliana seeds. J Exp Bot 64:3189–3200
Zhao L, Katavic V, Li F, Haughn GW, Kunst L (2010) 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 64:1048–1058
Zhekisheva M, Boussiba S, Khozin-Goldberg I, Zarka A, Cohen Z (2002) Accumulation of oleic acid in Haematococcus pluvialis (Chlorophyceae) under nitrogen starvation or high light is correlated with that of astaxanthin esters. J Phycol 38:325–331
Zhou XR, Robert SS, Petrie JR, Frampton DM, Mansour MP, Blackburn SI, Nichols PD, Green AG, Singh SP (2007) Isolation and characterization of genes from the marine microalga Pavlova salina encoding three front-end desaturases involved in docosahexaenoic acid biosynthesis. Phytochemistry 68:785–796
Zhou XR, Shrestha P, Yin F, Petrie JR, Singh SP (2013) AtDGAT2 is a functional acyl-CoA: diacylglycerol acyltransferase and displays different acyl-CoA substrate preferences than AtDGAT1. FEBS Lett 587:2371–2376
Zou J, Wei Y, Jako C, Kumar A, Selvaraj G, Taylor DC (1999) The Arabidopsis thaliana TAG1 mutant has a mutation in a diacylglycerol acyltransferase gene. Plant J 19:645–653
Acknowledgments
I would like to thank Zvi Cohen (Ben-Gurion University of the Negev) and late Mark Merzlyak (Moscow State University) for introducing me to the fascinating world of plant and microalgal lipids. Alexei Solovchenko (Moscow State University) for his valuable suggestions and reading the manuscript; Irina Guschina (Cardiff University) and Nastassia Shtaida for their assistance with preparation of illustrative material. I would like to thank all members of the Microalgal Biotechnology Laboratory (Ben-Gurion University of the Negev) for their continuous support of my research and Camille Vainstein for professional English language editing. The Lipidomics Gateway at http://www.lipidmaps.org/tools/index.html for kind permission to reproduce the chemical structures of fatty acids and lipids (Fahy et al. 2007). The financial support of European Commission’s Seventh Framework Program for Research and Technology Development (FP7) is kingly appreciated (project GIAVAP, Grant No. 266401).
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Khozin-Goldberg, I. (2016). Lipid Metabolism in Microalgae. In: Borowitzka, M., Beardall, J., Raven, J. (eds) The Physiology of Microalgae. Developments in Applied Phycology, vol 6. Springer, Cham. https://doi.org/10.1007/978-3-319-24945-2_18
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