Skip to main content

Triacylglycerol Accumulation in Photosynthetic Cells in Plants and Algae

  • Chapter
  • First Online:

Part of the book series: Subcellular Biochemistry ((SCBI,volume 86))

Abstract

Plant and algal oils are some of the most energy-dense renewable compounds provided by nature. Triacylglycerols (TAGs) are the major constituent of plant oils, which can be converted into fatty acid methyl esters commonly known as biodiesel. As one of the most efficient producers of TAGs, photosynthetic microalgae have attracted substantial interest for renewable fuel production. Currently, the big challenge of microalgae based TAGs for biofuels is their high cost compared to fossil fuels. A conundrum is that microalgae accumulate large amounts of TAGs only during stress conditions such as nutrient deprivation and temperature stress, which inevitably will inhibit growth. Thus, a better understanding of why and how microalgae induce TAG biosynthesis under stress conditions would allow the development of engineered microalgae with increased TAG production during conditions optimal for growth. Land plants also synthesize TAGs during stresses and we will compare new findings on environmental stress-induced TAG accumulation in plants and microalgae especially in the well-characterized model alga Chlamydomonas reinhardtii and a biotechnologically relevant genus Nannochloropsis.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Aaronson S (1973) Effect of incubation temperature on the macromolecular and lipid content of the phytoflagellate Ochromonas danica. J Phycol 9:111–113

    Article  CAS  Google Scholar 

  • Abdulla R, Chan ES, Ravindra P (2011) Biodiesel production from Jatropha curcas: a critical review. Crit Rev Biotechnol 31:53–64

    Article  CAS  PubMed  Google Scholar 

  • Abida H, Dolch LJ, Mei C, Villanova V, Conte M, Block MA, Finazzi G, Bastien O, Tirichine L, Bowler C, Rebeille F, Petroutsos D, Jouhet J, Marechal E (2015) Membrane glycerolipid remodeling triggered by nitrogen and phosphorus starvation in Phaeodactylum tricornutum. Plant Physiol 167:118–136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andersen RA, Brett RW, Potter D, Sexton JP (1998) Phylogeny of the Eustigmatophyceae based upon 18S rDNA, with emphasis on Nannochloropsis. Protist 149:61–74

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • ASTM (2002) Standard specification for diesel fuel oils. ASTM D975-02. American Society for Testing and Materials, West Conshohocken

    Google Scholar 

  • Barber J (2009) Photosynthetic energy conversion: natural and artificial. Chem Soc Rev 38:185–196

    Article  CAS  PubMed  Google Scholar 

  • Baroli I, Do AD, Yamane T, Niyogi KK (2003) Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects Chlamydomonas reinhardtii from photooxidative stress. Plant Cell 15:992–1008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bates PD, Stymne S, Ohlrogge J (2013) Biochemical pathways in seed oil synthesis. Curr Opin Plant Biol 16:358–364

    Article  CAS  PubMed  Google Scholar 

  • Baud S, Lepiniec L (2010) Physiological and developmental regulation of seed oil production. Prog Lipid Res 49:235–249

    Article  CAS  PubMed  Google Scholar 

  • Bigogno C, Khozin-Goldberg I, Boussiba S, Vonshak A, Cohen Z (2002) Lipid and fatty acid composition of the green oleaginous alga Parietochloris incisa, the richest plant source of arachidonic acid. Phytochemistry 60:497–503

    Article  CAS  PubMed  Google Scholar 

  • 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 25:4305–4323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boussiba S, Vonshak A, Cohen Z, Avissar Y, Richmond A (1987) Lipid and biomass production by the halotolerant microalga Nanochloropsis salina. Biomass 12:37–47

    Article  CAS  Google Scholar 

  • Bouvier-Nave 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brennan L, Owende P (2010) Biofuels from microalgae-a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sust Energ Rev 14:557–577

    Article  CAS  Google Scholar 

  • Brown MR, Dunstan GA, Norwood SJ, Miller KA (1996) Effects of harvest stage and light on the biochemical composition of the diatom Thalassiosira pseudonana. J Phycol 32:64–73

    Article  CAS  Google Scholar 

  • Bruinsma J (ed) (2003) World agriculture: towards 2015/2030. Earthscan, London

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cernac A, Benning C (2004) WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J 40:575–585

    Article  CAS  PubMed  Google Scholar 

  • Chapman KD, Ohlrogge JB (2012) Compartmentation of triacylglycerol accumulation in plants. J Biol Chem 287:2288–2294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapman KD, Dyer JM, Mullen RT (2013) Commentary: why don’t plant leaves get fat? Plant Sci 207:128–134

    Article  CAS  PubMed  Google Scholar 

  • Cheah WY, Show PL, Chang JS, Ling TC, Juan JC (2014) Biosequestration of atmospheric CO2 and flue gas-containing CO2 by microalgae. Bioresour Technol. doi:10.1016/j.biortech.2014.1011.1026

    PubMed  Google Scholar 

  • Chhetri AB, Tango MS, Budge SM, Watts KC, Islam MR (2008) Non-edible plant oils as new sources for biodiesel production. Int J Mol Sci 9:169–180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25:294–306

    Article  CAS  PubMed  Google Scholar 

  • Chisti Y (2013) Constraints to commercialization of algal fuels. J Biotechnol 167:201–214

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Collins RP, Kalnins K (1969) The fatty acids of Cryptomonas ovata var. palustris. Phyton 26:47–50

    Google Scholar 

  • Commission of the European Communities (2007) Communication from the commission to the council and the European Parliament: biofuels progress report. Commission of the European Communities, Brussels

    Google Scholar 

  • Conover SAM (1975) Partitioning of nitrogen and carbon in cultures of the marine diatom Thalassiosira fluviatillis supplied with nitrate, ammonium, or urea. Mar Biol 32:231–246

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Dismukes GC, Carrieri D, Bennette N, Ananyev GM, Posewitz MC (2008) Aquatic phototrophs: efficient alternatives to land-based crops for biofuels. Curr Opin Biotechnol 19:235–240

    Article  CAS  PubMed  Google Scholar 

  • Durrett TP, Benning C, Ohlrogge J (2008) Plant triacylglycerols as feedstocks for the production of biofuels. Plant J 54:593–607

    Article  CAS  PubMed  Google Scholar 

  • El-Hafid L, Pham AT, Zuily-fodil Y, da Silva JV (1989) Enzymatic breakdown of polar lipids in cotton leaves under water stress: I. Degradation of monogalactosyl-diacylglycerol. Plant Physiol Biochem 27:495–502

    CAS  Google Scholar 

  • Fabregas J, Maseda A, Dominquez A, Otero A (2004) The cell composition of Nannochloropsis sp. changes under different irradiances in semicontinuous culture. World J Microbiol Biotechnol 20:31–35

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Fan J, Yan C, Zhang X, Xu C (2013) Dual role for phospholipid:diacylglycerol acyltransferase: enhancing fatty acid synthesis and diverting fatty acids from membrane lipids to triacylglycerol in Arabidopsis leaves. Plant Cell 25:3506–3518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan J, Yan C, Roston R, Shanklin J, Xu C (2014) Arabidopsis lipins, PDAT1 acyltransferase, and SDP1 triacylglycerol lipase synergistically direct fatty acids toward beta-oxidation, thereby maintaining membrane lipid homeostasis. Plant Cell 26:4119–4134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fourrier N, Bedard J, Lopez-Juez E, Barbrook A, Bowyer J, Jarvis P, Warren G, Thorlby G (2008) A role for SENSITIVE TO FREEZING2 in protecting chloroplasts against freeze-induced damage in Arabidopsis. Plant J 55:734–745

    Article  CAS  PubMed  Google Scholar 

  • Gasulla F, Vom Dorp K, Dombrink I, Zahringer U, Gisch N, Dormann P, Bartels D (2013) The role of lipid metabolism in the acquisition of desiccation tolerance in Craterostigma plantagineum: a comparative approach. Plant J 75:726–741

    Article  CAS  PubMed  Google Scholar 

  • Georgianna DR, Mayfield SP (2012) Exploiting diversity and synthetic biology for the production of algal biofuels. Nature 488:329–335

    Article  CAS  PubMed  Google Scholar 

  • Gorelova O, Baulina O, Solovchenko A, Selyakh I, Chivkunova O, Semenova L, Scherbakov P, Burakova O, Lobakova E (2015) Coordinated rearrangements of assimilatory and storage cell compartments in a nitrogen-starving symbiotic chlorophyte cultivated under high light. Arch Microbiol 197:181–195

    Article  CAS  PubMed  Google Scholar 

  • Harris EH (2001) Chlamydomonas as a model organism. Annu Rev Plant Physiol Plant Mol Biol 52:363–406

    Article  CAS  PubMed  Google Scholar 

  • Hemme D, Veyel D, Muhlhaus T, Sommer F, Juppner J, Unger AK, Sandmann M, Fehrle I, Schonfelder S, Steup M, Geimer S, Kopka J, Giavalisco P, Schroda M (2014) Systems-wide analysis of acclimation responses to long-term heat stress and recovery in the photosynthetic model organism Chlamydomonas reinhardtii. Plant Cell 26:4270–4297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hemschemeier A, Casero D, Liu B, Benning C, Pellegrini M, Happe T, Merchant SS (2013) Copper response regulator1-dependent and -independent responses of the Chlamydomonas reinhardtii transcriptome to dark anoxia. Plant Cell 25:3186–3211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill J, Nelson E, Tilman D, Polasky S, Tiffany D (2006) Environmental, economic, and energetic costs and benefits of biodiesel and ethanol biofuels. Proc Natl Acad Sci U S A 103:11206–11210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • James GO, Hocart CH, Hillier W, Chen H, Kordbacheh F, Price GD, Djordjevic MA (2011) Fatty acid profiling of Chlamydomonas reinhardtii under nitrogen deprivation. Bioresour Technol 102:3343–3351

    Article  CAS  PubMed  Google Scholar 

  • Jia J, Han DX, Gerken HG, Li YT, 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

    Article  Google Scholar 

  • John RP, Anisha GS, Nampoothiri KM, Pandey A (2011) Micro and macroalgal biomass: a renewable source for bioethanol. Bioresour Technol 102:186–193

    Article  CAS  PubMed  Google Scholar 

  • Jones CS, Mayfield SP (2012) Algae biofuels: versatility for the future of bioenergy. Curr Opin Biotechnol 23:346–351

    Article  CAS  PubMed  Google Scholar 

  • Juergens MT, Deshpande RR, Lucker BF, Park JJ, Wang H, Gargouri M, Holguin FO, Disbrow B, Schaub T, Skepper JN, Kramer DM, Gang DR, Hicks LM, Shachar-Hill Y (2015) The regulation of photosynthetic structure and function during nitrogen deprivation in Chlamydomonas reinhardtii. Plant Physiol 167:558–573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaup MT, Froese CD, Thompson JE (2002) A role for diacylglycerol acyltransferase during leaf senescence. Plant Physiol 129:1616–1626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khotimchenko SV, Yakovleva IM (2005) Lipid composition of the red alga Tichocarpus crinitus exposed to different levels of photon irradiance. Phytochemistry 66:73–79

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Khozin-Goldberg I, Cohen Z (2011) Unraveling algal lipid metabolism: recent advances in gene identification. Biochimie 93:91–100

    Article  CAS  PubMed  Google Scholar 

  • Kim S, Kim H, Ko D, Yamaoka Y, Otsuru M, Kawai-Yamada M, Ishikawa T, Oh HM, Nishida I, Li-Beisson Y, Lee Y (2013) Rapid induction of lipid droplets in Chlamydomonas reinhardtii and Chlorella vulgaris by Brefeldin A. PLoS One 8, e81978

    Article  PubMed  PubMed Central  Google Scholar 

  • Klaus D, Ohlrogge JB, Neuhaus HE, Dormann P (2004) Increased fatty acid production in potato by engineering of acetyl-CoA carboxylase. Planta 219:389–396

    Article  CAS  PubMed  Google Scholar 

  • Klug RM, Benning C (2001) Two enzymes of diacylglyceryl-O-4′-(N, N, N,-trimethyl)-homoserine biosynthesis are encoded by btaA and btaB in the purple bacterium Rhodobacter sphaeroides. Proc Natl Acad Sci U S A 98:5910–5915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kropat J, Hong-Hermesdorf A, Casero D, Ent P, Castruita M, Pellegrini M, Merchant SS, Malasarn D (2011) A revised mineral nutrient supplement increases biomass and growth rate in Chlamydomonas reinhardtii. Plant J 66:770–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Han D, Hu G, Dauvillee D, Sommerfeld M, Ball S, Hu Q (2010) Chlamydomonas starchless mutant defective in ADP-glucose pyrophosphorylase hyper-accumulates triacylglycerol. Metab Eng 12:387–391

    Article  PubMed  CAS  Google Scholar 

  • Li X, Moellering ER, Liu B, Johnny C, Fedewa M, Sears BB, Kuo MH, Benning C (2012) A galactoglycerolipid lipase is required for triacylglycerol accumulation and survival following nitrogen deprivation in Chlamydomonas reinhardtii. Plant Cell 24:4670–4686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li F, Gao D, Hu H (2014a) High-efficiency nuclear transformation of the oleaginous marine Nannochloropsis species using PCR product. Biosci Biotechnol Biochem 78:812–817

    Article  CAS  PubMed  Google Scholar 

  • Li J, Han D, Wang D, Ning K, Jia J, Wei L, Jing X, Huang S, Chen J, Li Y, Hu Q, Xu J (2014b) Choreography of transcriptomes and lipidomes of Nannochloropsis reveals the mechanisms of oil synthesis in microalgae. Plant Cell 26:1645–1665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lippold F, vom Dorp K, Abraham M, Holzl G, Wewer V, Yilmaz JL, Lager I, Montandon C, Besagni C, Kessler F, Stymne S, Dormann P (2012) Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis. Plant Cell 24:2001–2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu B, Benning C (2013) Lipid metabolism in microalgae distinguishes itself. Curr Opin Biotechnol 24:300–309

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Vieler A, Li C, Jones AD, Benning C (2013) Triacylglycerol profiling of microalgae Chlamydomonas reinhardtii and Nannochloropsis oceanica. Bioresour Technol 146:310–316

    Article  CAS  PubMed  Google Scholar 

  • Lynch DV, Thompson GA (1982) Low temperature-induced alterations in the chloroplast and microsomal membranes of Dunaliella salina. Plant Physiol 69:1369–1375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mansour MP, Volkman JK, Blackburn SI (2003) The effect of growth phase on the lipid class, fatty acid and sterol composition in the marine dinoflagellate, Gymnodinium sp. in batch culture. Phytochemistry 63:145–153

    Article  CAS  PubMed  Google Scholar 

  • Martin GJ, Hill DR, Olmstead IL, Bergamin A, Shears MJ, Dias DA, Kentish SE, Scales PJ, Botte 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, e103389

    Article  PubMed  PubMed Central  Google Scholar 

  • Martinez-Boti MA, Marino G, Foster GL, Ziveri P, Henehan MJ, Rae JW, Mortyn PG, Vance D (2015) Boron isotope evidence for oceanic carbon dioxide leakage during the last deglaciation. Nature 518:219–222

    Article  CAS  PubMed  Google Scholar 

  • Matthew T, Zhou W, Rupprecht J, Lim L, Thomas-Hall SR, Doebbe A, Kruse O, Hankamer B, Marx UC, Smith SM, Schenk PM (2009) The metabolome of Chlamydomonas reinhardtii following induction of anaerobic H2 production by sulfur depletion. J Biol Chem 284:23415–23425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng Y, Jiang J, Wang H, Cao X, Xue S, Yang Q, Wang W (2015) The characteristics of TAG and EPA accumulation in Nannochloropsis oceanica IMET1 under different nitrogen supply regimes. Bioresour Technol 179:483–489

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Miller R, Wu G, Deshpande RR, Vieler A, Gartner K, Li X, Moellering ER, Zauner S, Cornish AJ, Liu B, Bullard B, Sears BB, Kuo MH, Hegg EL, Shachar-Hill Y, Shiu SH, Benning C (2010) Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol 154:1737–1752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moellering ER, Benning C (2011) Galactoglycerolipid metabolism under stress: a time for remodeling. Trends Plant Sci 16:98–107

    Article  CAS  PubMed  Google Scholar 

  • Moellering ER, Muthan B, Benning C (2010) Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330:226–228

    Article  CAS  PubMed  Google Scholar 

  • Mu J, Tan H, Zheng Q, Fu F, Liang Y, Zhang J, Yang X, Wang T, Chong K, Wang XJ, Zuo J (2008) LEAFY COTYLEDON1 is a key regulator of fatty acid biosynthesis in Arabidopsis. Plant Physiol 148:1042–1054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Napolitano GE (1994) The relationship of lipids with light and chlorophyll measurement in freshwater algae and periphyton. J Phycol 30:943–950

    Article  CAS  Google Scholar 

  • Navari-Izzo F, Rascio N (1999) Plant response to water-deficit conditions. In: Pessarakli M (ed) Handbook of plant and crop stress. Dekker, New York, pp 217–231

    Google Scholar 

  • Nguyen HM, Baudet M, Cuine 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

    Article  CAS  PubMed  Google Scholar 

  • Ogas J, Cheng JC, Sung ZR, Somerville C (1997) Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. Science 277:91–94

    Article  CAS  PubMed  Google Scholar 

  • Ogas J, Kaufmann S, Henderson J, Somerville C (1999) PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc Natl Acad Sci U S A 96:13839–13844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohlrogge JB, Chapman KD (2011) The seeds of green energy: expanding the contribution of plant oils as biofuels. Biochemist 33:34–38

    Google Scholar 

  • Ohlrogge J, Allen D, Berguson B, Dellapenna D, Shachar-Hill Y, Stymne S (2009) Energy. Driving on biomass. Science 324:1019–1020

    Article  CAS  PubMed  Google Scholar 

  • Otsuka H (1961) Changes of lipid and carbohydrate contents of Chlorella cells during the sulfur starvation, as studied by the technique of synchronous culture. J Gen Appl Microbiol 7:72–77

    Article  Google Scholar 

  • Park JJ, Wang H, Gargouri M, Deshpande RR, Skepper JN, Holguin FO, Juergens MT, Shachar-Hill Y, Hicks LM, Gang DR (2015) The response of Chlamydomonas reinhardtii to nitrogen deprivation: a systems biology analysis. Plant J 81:611–624

    Article  CAS  PubMed  Google Scholar 

  • 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, e35214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pugh PR (1971) Changes in the fatty acid composition of Coscinodiscus eccentricus with culture-age and salinity. Mar Biol 11:118–124

    CAS  Google Scholar 

  • Rabbani S, Beyer P, Lintig J, Hugueney P, Kleinig H (1998) Induced β-carotene synthesis driven by triacylglycerol deposition in the unicellular alga Dunaliella bardawil. Plant Physiol 116:1239–1248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Radakovits R, Jinkerson RE, Fuerstenberg SI, Tae H, Settlage RE, Boore JL, Posewitz MC (2012) Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Nat Commun 3:686

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Reitan KI, Rainuzzo JR, Olsen Y (1994) Effect of nutrient limitation on fatty acid and lipid content of marine microalgae. J Phycol 30:972–979

    Article  CAS  Google Scholar 

  • Renaud SM, Thinh LV, Lambrinidis G, Parry DL (2002) Effect of temperature on growth, chemical composition and fatty acid composition of tropical Australian microalgae grown in batch cultures. Aquaculture 211:195–214

    Article  CAS  Google Scholar 

  • Riekhof RW, Benning C (2009) Glycerolipid biosynthesis. In: Stern DB, Harris EH (eds) The Chlamydomonas source book, vol 2, 2nd edn, Organellar and Metabolic Processes. Academic, Elsevier, Boston, pp 41–68

    Chapter  Google Scholar 

  • Rochaix JD (1995) Chlamydomonas reinhardtii as the photosynthetic yeast. Annu Rev Genet 29:209–230

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ross B, Sanchez J, Millan F, Murphy DJ (1993) Differential presence of oleosins in oleogenic seed and mesocarp tissues in olive (Olea europaea) and avocado (Persea americana). Plant Sci 93:203–210

    Article  CAS  Google Scholar 

  • Roston RL, Wang K, Kuhn LA, Benning C (2014) Structural determinants allowing transferase activity in SENSITIVE TO FREEZING 2, classified as a family I glycosyl hydrolase. J Biol Chem 289:26089–26106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakaki T, Ohnishi J, Kondo N, Yamada M (1985) Polar and neutral lipid changes in spinach leaves with ozone fumigation: triacylglycerol synthesis from polar lipids. Plant Cell Physiol 26:253–262

    CAS  Google Scholar 

  • Sakaki T, Kondo N, Yamada M (1990a) Free fatty acids regulate two galactosyltransferases in chloroplast envelope membranes isolated from spinach leaves. Plant Physiol 94:781–787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakaki T, Kondo N, Yamada M (1990b) Pathway for the synthesis of triacylglycerols from monogalactosyldiacylglycerols in ozone-fumigated spinach leaves. Plant Physiol 94:773–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakaki T, Saito K, Kawaguchi A, Kondo N, Yamada M (1990c) Conversion of monogalactosyldiacylglycerols to triacylglycerols in ozone-fumigated spinach leaves. Plant Physiol 94:766–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanjaya, Durrett TP, Weise SE, Benning C (2011) Increasing the energy density of vegetative tissues by diverting carbon from starch to oil biosynthesis in transgenic Arabidopsis. Plant Biotechnol J 9:874–883

    Article  CAS  PubMed  Google Scholar 

  • Sanjaya, Miller R, Durrett TP, Kosma DK, Lydic TA, Muthan B, Koo AJ, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santos-Mendoza M, Dubreucq B, Miquel M, Caboche M, Lepiniec L (2005) LEAFY COTYLEDON 2 activation is sufficient to trigger the accumulation of oil and seed specific mRNAs in Arabidopsis leaves. FEBS Lett 579:4666–4670

    Article  CAS  PubMed  Google Scholar 

  • Santos-Mendoza M, Dubreucq B, Baud S, Parcy F, Caboche M, Lepiniec L (2008) Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J 54:608–620

    Article  CAS  PubMed  Google Scholar 

  • Sato N, Murata N (1980) Temperature shift-induced responses in lipids in the blue-green alga, Anabaena variabilis: the central role of diacylmonogalactosylglycerol in thermo-adaptation. Biochim Biophys Acta 619:353–366

    Article  CAS  PubMed  Google Scholar 

  • Schmollinger S, Muhlhaus 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shiratake T, Sato A, Minoda A, Tsuzuki M, Sato N (2013) Air-drying of cells, the novel conditions for stimulated synthesis of triacylglycerol in a green alga, Chlorella kessleri. PLoS One 8, e79630

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Siaut M, Cuine S, Cagnon C, Fessler B, Nguyen M, Carrier P, Beyly A, Beisson F, Triantaphylides 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simionato D, Block MA, La Rocca N, Jouhet J, Marechal 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Stephenson PG, Moore CM, Terry MJ, Zubkov MV, Bibby TS (2011) Improving photosynthesis for algal biofuels: toward a green revolution. Trends Biotechnol 29:615–623

    Article  CAS  PubMed  Google Scholar 

  • Stoller EW, Weber EJ (1975) Differential cold tolerance, starch, sugar, protein, and lipid of yellow and purple nutsedge tubers. Plant Physiol 55:859–863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stone SL, Braybrook SA, Paula SL, Kwong LW, Meuser J, Pelletier J, Hsieh TF, Fischer RL, Goldberg RB, Harada JJ (2008) Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: implications for somatic embryogenesis. Proc Natl Acad Sci U S A 105:3151–3156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takagi M, Karseno, Yoshida T (2006) Effect of salt concentration on intracellular accumulation of lipids and triacylglyceride in marine microalgae Dunaliella cells. J Biosci Bioeng 101:223–226

    Article  CAS  PubMed  Google Scholar 

  • Taleb A, Pruvost J, Legrand J, Marec H, Le-Gouic B, Mirabella B, Legeret B, Bouvet S, Peltier G, Li-Beisson Y, Taha S, Takache H (2015) Development and validation of a screening procedure of microalgae for biodiesel production: application to the genus of marine microalgae Nannochloropsis. Bioresour Technol 177:224–232

    Article  CAS  PubMed  Google Scholar 

  • Thorlby G, Fourrier N, Warren G (2004) The SENSITIVE TO FREEZING2 gene, required for freezing tolerance in Arabidopsis thaliana, encodes a β-glucosidase. Plant Cell 16:2192–2203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Traller JC, Hildebrand M (2013) High throughput imaging to the diatom Cyclotella cryptica demonstrates substantial cell-to-cell variability in the rate and extent of triacylglycerol accumulation. Algal Res 2:244–252

    Article  Google Scholar 

  • Tranbarger TJ, Dussert S, Joet T, Argout X, Summo M, Champion A, Cros D, Omore A, Nouy B, Morcillo F (2011) Regulatory mechanisms underlying oil palm fruit mesocarp maturation, ripening, and functional specialization in lipid and carotenoid metabolism. Plant Physiol 156:564–584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • US Department of Energy (2007) Annual energy outlook 2007. Report number DOE/EIA-0383. Energy Information Administration, US Department of Energy, Washington, DC

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Vanhercke T, El Tahchy A, Liu Q, Zhou XR, Shrestha P, Divi UK, Ral JP, Mansour MP, Nichols PD, James CN, Horn PJ, Chapman KD, Beaudoin F, Ruiz-Lopez N, Larkin PJ, de Feyter RC, Singh SP, Petrie JR (2014) Metabolic engineering of biomass for high energy density: oilseed-like triacylglycerol yields from plant leaves. Plant Biotechnol J 12:231–239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Venkata Mohan S, Rohit MV, Chiranjeevi P, Chandra R, Navaneeth B (2015) Heterotrophic microalgae cultivation to synergize biodiesel production with waste remediation: progress and perspectives. Bioresour Technol 184:169–178

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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, Zauner 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 oceanica CCMP1779. PLoS Genet 8, e1003064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang G, Lin Q, Xu Y (2007) Tetraena mongolica Maxim can accumulate large amounts of triacylglycerol in phloem cells and xylem parenchyma of stems. Phytochemistry 68:2112–2117

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang D, Ning K, Li J, Hu J, Han D, Wang H, Zeng X, Jing X, Zhou Q, Su X, Chang X, Wang A, Wang W, Jia J, Wei L, Xin Y, Qiao Y, Huang R, Chen J, Han B, Yoon K, Hill RT, Zohar Y, Chen F, Hu Q, Xu J (2014) Nannochloropsis genomes reveal evolution of microalgal oleaginous traits. PLoS Genet 10, e1004094

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Winichayakul S, Scott RW, Roldan M, Hatier JH, Livingston S, Cookson R, Curran AC, Roberts NJ (2013) In vivo packaging of triacylglycerols enhances Arabidopsis leaf biomass and energy density. Plant Physiol 162:626–639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu C, Fan J, Froehlich JE, Awai K, Benning C (2005) Mutation of the TGD1 chloroplast envelope protein affects phosphatidate metabolism in Arabidopsis. Plant Cell 17:3094–3110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Ohlrogge JB (2009) Turnover of fatty acids during natural senescence of Arabidopsis, Brachypodium, and switchgrass and in Arabidopsis β-oxidation mutants. Plant Physiol 150:1981–1989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Yu X, Song L, An C (2011) ABI4 activates DGAT1 expression in Arabidopsis seedlings during nitrogen deficiency. Plant Physiol 156:873–883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 6:67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang HY, Hanna MA, Ali Y, Nan L (1996) Yellow nutsedge (Cyperus esculentus L) tuber oil as a fuel. Ind Crops Prod 5:177–181

    Article  CAS  Google Scholar 

  • Zhang R, Patena W, Armbruster U, Gang SS, Blum SR, Jonikas MC (2014) High-throughput genotyping of green algal mutants reveals random distribution of mutagenic insertion sites and endonucleolytic cleavage of transforming DNA. Plant Cell 26:1398–1409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Work on lipid and TAG metabolism in the Benning lab has been supported by grants from the Center for Advanced Biofuels Systems (CABS), an Energy Frontier Research Center funded by the U.S. Department of Energy, Office of Basic Energy Sciences under award number DE-SC0001295, the U.S. Department of Energy, Office of Basic Energy Sciences Grant DE-FG02-98ER20305, the US National Science Foundation, MCB 0741395 and MCB-1515169, the US Department of Energy-Great Lakes Bioenergy Research Center Cooperative Agreement DE-FC02-07ER64494, the US Air Force Office of Scientific Research, FA9550-11-1-0264, and Michigan State University AgBioResearch.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christoph Benning .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Du, ZY., Benning, C. (2016). Triacylglycerol Accumulation in Photosynthetic Cells in Plants and Algae. In: Nakamura, Y., Li-Beisson, Y. (eds) Lipids in Plant and Algae Development. Subcellular Biochemistry, vol 86. Springer, Cham. https://doi.org/10.1007/978-3-319-25979-6_8

Download citation

Publish with us

Policies and ethics