Lipids in Photosynthesis pp 139-155 | Cite as
Molecular Genetics of Lipid Metabolism in the Model Green Alga Chlamydomonas reinhardtii
Summary
Research focusing on microalgae is currently experiencing a renaissance due to the potential of microalgae for providing biofuels without competing with food crops. Despite this potential, our knowledge of neutral and membrane lipid metabolism in microalgae is very limited, and opportunities to explore lipid metabolism in microalgae and contrast it to plant lipid metabolism abound. The unicellular green alga Chlamydomonas reinhardtii is currently the best genetic and genomic model for microalgal lipid research. This chapter summarizes the current knowledge of lipid metabolism in this alga. Chlamydomonas lipid metabolism differs in some aspects from that of seed plants. For example, Chlamydomonas lacks phosphatidylcholine and has in its place the betaine lipid diacylglyceryl-N,N,N-trimethylhomoserine. This has important implications for lipid trafficking and lipid modification. These distinct aspects of algal lipid metabolism combined with the lower number of genes involved in lipid metabolism in Chlamydomonas provide several opportunities for basic research aimed at a more in-depth understanding of lipid metabolism in eukaryotic photosynthetic organisms in general.
Keywords
Fatty Acid Desaturation Phosphatidic Acid Phosphatase Betaine Lipid Lipid Trafficking Thylakoid LipidAbbreviations
- ACP
Acyl carrier protein
- CDP-DAG
CDP-diacylglycerol
- DAG
Diacylglycerol
- DGTS
Dia-cylglyceryl-N,N,N-trimethylhomoserine
- DGDG
Digalac-tosyl -diacyl-gly cerol
- ER
Endoplasmic reticulum
- FAS
Fatty acid synthase
- MGDG
Monogalactosyldiacylg-lycerol
- PA
Phosphatidic acid
- PC
Phosphatidylcholine
- PE
Phosphatidylethanolamine
- PG
Phosphatidylglycerol
- PI
Phosphatidylinositol
- PS
Phosphatidylserine
- PUFA
Polyunsaturated fatty acid
- RNAi
RNA interference
- SQDG
Sulfoquinovosyldiacylglycerol
- TAG
Triacylglycerol.
Notes
Acknowledgments
Work on lipid biosynthesis in plants and algae in the Benning lab is currently supported, in part, by grants from the US Air Force Office of Scientific Research, the US National Science Foundation, the US Department of Energy, the Great Lakes Bioenergy Research Center, BASF-Plant Sciences, the MSU Center of Excellence for the Structural Biology Membrane Proteins, and the Michigan Agricultural Experiment Station.
References
- Babiychuk E, Müller F, Eubel H, Braun HP, Frentzen M and Kushnir S (2003) Arabidopsis phosphatidylglycerophos-phate synthase 1 is essential for chloroplast differentiation, but is dispensable for mitochondrial function. Plant J 33: 899–909PubMedCrossRefGoogle Scholar
- Beisson F, Koo AJ, Ruuska S, Schwender J, Pollard M, Thelen JJ, Paddock T, Salas JJ, Savage L, Milcamps A, Mhaske VB, Cho Y and Ohlrogge JB (2003) Arabidopsis genes involved in acyl lipid metabolism. A 2003 census of the candidates, a study of the distribution of expressed sequence tags in organs, and a web-based database. Plant Physiol 132: 681–697PubMedCrossRefGoogle Scholar
- Benamotz A and Tornabene TG (1985) Chemical profile of selected species of microalgae with emphasis on lipids. J Phycol 21: 72–81CrossRefGoogle Scholar
- Benamotz A, Shaish A and Avron M (1989) Mode of action of the massively accumulated β-carotene of Dunaliella bardawil in protecting the alga against damage by excess irradiation. Plant Physiol 91: 1040–1043CrossRefGoogle Scholar
- Benning C (2008) A role for lipid trafficking in chloroplast biogenesis. Prog Lipid Res 47: 381–389PubMedCrossRefGoogle Scholar
- Benning C and Ohta H (2005) Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. J Biol Chem 280: 2397–2400PubMedCrossRefGoogle Scholar
- Benning C, Beatty JT, Prince RC and Somerville CR (1993) The sulfolipid sulfoquinovosyldiacylglycerol is not required for photosynthetic electron transport in Rhodo-bacter sphaeroides but enhances growth under phosphate limitation. Proc Natl Acad Sci USA 90: 1561–1565PubMedCrossRefGoogle Scholar
- Benning C, Huang ZH and Gage DA (1995) Accumulation of a novel glycolipid and a betaine lipid in cells of Rho-dobacter sphaeroides grown under phosphate limitation. Arch Biochem Biophys 317: 103–111PubMedCrossRefGoogle Scholar
- Benning C, Garavito RM, Shimojima M (2008) Sulfolipid biosynthesis and function in plants. In: Hell R, Dahl C, Knaff D and Leusteck T (eds) Sulfur Metabolism in Pho-totrophic Organisms. Springer, Dordrecht, pp. 185–200CrossRefGoogle Scholar
- Bigogno C, Khozin-Goldberg I, Boussiba S, Vonshak A and Cohen Z (2002) Lipid and fatty acid composition of the green oleaginous alga Parietochloris incisa, the richest plant source of arachidonic acid. Phytochemistry 60: 497–503PubMedCrossRefGoogle Scholar
- Blouin A, Lavezzi T and Moore TS (2003) Membrane lipid biosynthesis in Chlamydomonas reinhardtii. Partial characterization of CDP-diacylglycerol:myo-inositol 3-phos-phatidyltransferase. Plant Physiol Biochem 41: 11–16CrossRefGoogle Scholar
- Browse J and Somerville C (1991) Glycerolipid biosynthesis: Biochemistry and regulation. Annu Rev Plant Physiol Plant Mol Biol 42: 467–506CrossRefGoogle Scholar
- Browse J, McCourt P and Somerville C (1985) A mutant of Arabidopsis lacking a chloroplast-specific lipid. Science 227: 763–765PubMedCrossRefGoogle Scholar
- Browse J, Warwick N, Somerville CR and Slack CR (1986) Fluxes through the prokaryotic and eukaryotic pathways of lipid synthesis in the “16:3” plant Arabidopsis thaliana. Biochem J 235: 25–31PubMedGoogle Scholar
- Cedergren RA and Hollingsworth RI (1994) Occurrence of sulfoquinovosyl diacylglycerol in some members of the family Rhizobiaceae. J Lipid Res 35: 1452–1461PubMedGoogle Scholar
- Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25: 294–306PubMedCrossRefGoogle Scholar
- Dahlqvist A, Stahl U, Lenman M, Banas A, Lee M, Sandager L, Ronne H and Stymne H (2000) Phospholipid: diacylg-lycerol acyltransferase: An enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants. Proc Natl Acad Sci USA 97: 6487–6492PubMedCrossRefGoogle Scholar
- Davies JP, Yildiz F and Grossman AR (1994) Mutants of Chlamydomonas with aberrant responses to sulfur deprivation. Plant Cell 6: 53–63PubMedGoogle Scholar
- Davies JP, Yildiz FH and Grossman A (1996) Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. EMBO J 15: 2150– 2159PubMedGoogle Scholar
- Davies JP, Yildiz FH and Grossman AR (1999) Sac3, an Snf1-like serine/threonine kinase that positively and negatively regulates the responses of Chlamydomonas to sulfur limitation. Plant Cell 11: 1179–1190PubMedGoogle Scholar
- Dempster TA and Sommerfeld MR (1998) Effects of environmental conditions on growth and lipid accumulation in Nitzschia communis (Bacillariophyceae). J Phycol 34: 712–721CrossRefGoogle Scholar
- De Swaaf ME, de Rijk TC, Eggink G and Sijtsma L (1999) Optimisation of docosahexaenoic acid production in batch cultivations by Crypthecodinium cohnii. J Biotech 70: 185–192CrossRefGoogle Scholar
- Dörmann P and Benning C (2002) Galactolipids rule in seed plants. Trends Plant Sci 7: 112–118PubMedCrossRefGoogle Scholar
- Dubertret G, Mirshahi A, Mirshahi M, Gerard-Hirne C and Tremolieres A (1994) Evidence from in vivo manipulations of lipid composition in mutants that the Δ3-trans-hexadecenoic acid-containing phosphatidylglycerol is involved in the biogenesis of the light-harvesting chlorophyll a/b-protein complex of Chlamydomonas reinhardtii. Eur J Biochem 226: 473–482PubMedCrossRefGoogle Scholar
- Dubertret G, Gerard-Hirne C and Tremolieres A (2002) Importance of trans-Δ3-hexadecenoic acid containing phosphatidylglycerol in the formation of the trimeric light-harvesting complex in Chlamydomonas. Plant Phys-iol Biochem 40: 829–836CrossRefGoogle Scholar
- Eichenberger W (1982) Distribution of diacylglyceryl-O-4′-(N,N,N-trimethyl)homoserine in different algae. Plant Sci Lett 24: 91–95CrossRefGoogle Scholar
- 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: 213–221Google Scholar
- Eichenberger W and Boschetti A (1977) Occurrence of 1(3),2-diacylglyceryl-(3)-O-4′-(N,N,N-trimethyl)homo-serine in Chlamydomonas reinhardtii. FEBS Lett 88: 201–204CrossRefGoogle Scholar
- Essigmann B, Güler S, Narang RA, Linke D and 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 USA 95: 1950–1955PubMedCrossRefGoogle Scholar
- Frentzen M (2004) Phosphatidylglycerol and sulfoquinovo-syldiacylglycerol: anionic membrane lipids and phosphate regulation. Curr Opin Plant Biol 7: 270–276PubMedCrossRefGoogle Scholar
- Fuhrmann M, Stahlberg A, Govorunova E, Rank S and Hegemann P (2001) The abundant retinal protein of the Chlamydomonas eye is not the photoreceptor for photo-taxis and photophobic responses. J Cell Sci 114: 3857– 3863PubMedGoogle Scholar
- Garnier J, Maroc J and Guyon D (1987) Characterization of new strains of photosynthetic mutants of Chlamydomonas reinhardtii. IV. Impaired excitation energy transfer in three low fluorescent mutants. Plant Cell Physiol 28: 1117–1131Google Scholar
- Garnier J, Wu B, Maroc J, Guyon D and Tremolieres A (1990) Restoration of both an oligomeric form of the light-harvesting antenna CP II and a fluorescence state II-state I transition by Δ3-trans-hexadecenoic acid-containing phosphatidylglycerol in cells of a mutant of Chlamydomonas reinhardtii. Biochim Biophys Acta 1020: 153–162CrossRefGoogle Scholar
- Giroud C, Gerber A and Eichenberger W (1988) Lipids of Chlamydomonas reinhardtii. Analysis of molecular species and intracellular site(s) of biosynthesis. Plant Cell Physiol 29: 587–595Google Scholar
- Gombos Z, Wada H and Murata N (1992) Unsaturation of fatty acids in membrane lipids enhances tolerance of the cyanobacterium Synechocystis PCC 6803 to low-temperature photoinhibition. Proc Natl Acad Sci USA 89: 9959–9963PubMedCrossRefGoogle Scholar
- Gounaris K and Barber J (1985) Isolation and characterisation of a photosytem II reaction center lipoprotein complex. FEBS Lett 188: 68–72CrossRefGoogle Scholar
- Grenier G, Guyon D, Roche O, Dubertret G and Tremo-lieres A (1991) Modification of the membrane fatty-acid composition of Chlamydomonas reinhardtii cultured in the presence of liposomes. Plant Physiol Biochem 29: 429–440Google Scholar
- Grossman AR, Croft M, Gladyshev VN, Merchant SS, Posewitz MC, Prochnik S and Spalding MH (2007) Novel metabolism in Chlamydomonas through the lens of genomics. Curr Opin Plant Biol 10: 190–198PubMedCrossRefGoogle Scholar
- Guckert JB and Cooksey KE (1990) Triglyceride accumulation and fatty acid profile changes in Chlorella (Chlo-rophyta) during high pH-induced cell cycle inhibition. J Phycol 26: 72–79CrossRefGoogle Scholar
- Hagio M, Gombos Z, Varkonyi Z, Masamoto K, Sato N, Tsuzuki M and Wada H (2000) Direct evidence for requirement of phosphatidylglycerol in photosystem II of photosynthesis. Plant Physiol 124: 795–804PubMedCrossRefGoogle Scholar
- Hagio M, Sakurai I, Sato S, Kato T, Tabata S and Wada H (2002) Phosphatidylglycerol is essential for the development of thylakoid membranes in Arabidopsis thaliana. Plant Cell Physiol 43: 1456–1464PubMedCrossRefGoogle Scholar
- Härtel H, Dörmann P and Benning C (2000) DGD1-inde-pendent biosynthesis of extraplastidic galactolipids following phosphate deprivation in Arabidopsis. Proc Natl Acad Sci USA 97: 10649–10654PubMedCrossRefGoogle Scholar
- Heinz E and Roughan G (1983) Similarities and differences in lipid metabolism of chloroplasts isolated from 18:3 and 16:3 plants. Plant Physiol 72: 273–279PubMedCrossRefGoogle Scholar
- Hobbs DH, Lu C and Hills MJ (1999) Cloning of a cDNA encoding diacylglycerol acyltransferase from Arabidop-sis thaliana and its functional expression. FEBS Lett 452: 145–149PubMedCrossRefGoogle Scholar
- Hofmann M and Eichenberger W (1996) Biosynthesis of diacylglyceryl-N,N,N-trimethylhomoserine in Rhodo-bacter sphaeroides and evidence for lipid-linked N meth-ylation. J Bacteriol 178: 6140–6144PubMedGoogle Scholar
- Holzl G and Dörmann P (2007) Structure and function of glycoglycerolipids in plants and bacteria. Prog Lipid Res 46: 225–243PubMedCrossRefGoogle Scholar
- Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M and Darzins A (2008) Microalgal triacylglycer-ols as feedstocks for biofuel production: perspectives and advances. Plant J 54: 621–639PubMedCrossRefGoogle Scholar
- Janero DR and Barrnett R (1981a) Cellular and thylakoid-membrane glycolipids of Chlamydomonas reinhardtii 137+. J Lipid Res 22: 1119–1125Google Scholar
- Janero DR and Barrnett R (1981b) Cellular and thylakoid-membrane phospholipids of Chlamydomonas reinhardtii 137+. J Lipid Res 22: 1126–1130Google Scholar
- Janero DR and Barrnett R (1982) Isolation and characterization of an ether-linked homoserine lipid from the thylakoid membrane of Chlamydomonas reinhardtii 137+. J Lipid Res 23: 307–316PubMedGoogle Scholar
- Jouhet J, Marechal E, Baldan B, Bligny R, Joyard J and Block MA (2004) Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria. J Cell Biol 167: 863–874PubMedCrossRefGoogle Scholar
- Jouhet J, Marechal E and Block MA (2007) Glycerolipid transfer for the building of membranes in plant cells. Prog Lipid Res 46: 37–55PubMedCrossRefGoogle Scholar
- Joyard J, Teyssier E, Miege C, Berny-Seigneurin D, Mare-chal E, Block MA, Dorne AJ, Rolland N, Ajlani G and Douce R (1998) The biochemical machinery of plastid envelope membranes. Plant Physiol 118: 715–723PubMedCrossRefGoogle Scholar
- Kajikawa M, Yamato KT, Kohzu Y, Shoji S, Matsui K, Tanaka Y, Sakai Y and Fukuzawa H (2006) A front-end desaturase from Chlamydomonas reinhardtii produces pinolenic and coniferonic acids by ω 13 desaturation in methylotrophic yeast and tobacco. Plant Cell Physiol 47: 64–73PubMedCrossRefGoogle Scholar
- Kathir P, LaVoie M, Brazelton WJ, Haas NA, Lefeb-vre PA and Silflow CD (2003) Molecular map of the Chlamydomonas reinhardtii nuclear genome. Euk Cell 2: 362–379CrossRefGoogle Scholar
- Kelly AA and Dörmann P (2002) DGD2, an Arabidopsis gene encoding a UDP-galactose-dependent digalacto-syldiacylglycerol synthase is expressed during growth under phosphate-limiting conditions. J Biol Chem 277: 1166–1173PubMedCrossRefGoogle Scholar
- Kennedy EP (1961) Biosynthesis of complex lipids. Fed Proc 20: 934–940PubMedGoogle Scholar
- Khotimchenko SV and Yakovleva IM (2004) Effect of solar irradiance on lipids of the green alga Ulva fenestrata Pos-tels et Ruprecht. Bot Mar 47: 395–401CrossRefGoogle Scholar
- Khotimchenko SV and Yakovleva IM (2005) Lipid composition of the red alga Tichocarpus crinitus exposed to different levels of photon irradiance. Phytochemistry 66: 73–79PubMedCrossRefGoogle Scholar
- Khozin-Goldberg I and Cohen Z (2006) The effect of phosphate starvation on the lipid and fatty acid composition of the fresh water eustigmatophyte Monodus subterraneus. Phytochemistry 67: 696–701PubMedCrossRefGoogle Scholar
- Kim HU and Huang AH (2004) Plastid lysophosphatidyl acyltransferase is essential for embryo development in Arabidopsis. Plant Physiol 134: 1206–1216PubMedCrossRefGoogle Scholar
- Kim HU, Li Y and Huang AH (2005) Ubiquitous and endoplasmic reticulum-located lysophosphatidyl acyl-transferase, LPAT2, is essential for female but not male gametophyte development in Arabidopsis. Plant Cell 17: 1073–1089PubMedCrossRefGoogle Scholar
- Klug RM and 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 USA 98: 5910–5915PubMedCrossRefGoogle Scholar
- Kroon JTM, Wei WX, Simon WJ and Slabas AR (2006) Identification and functional expression of a type 2 acyl-CoA: diacylglycerol acyltransferase (DGAT2) in developing castor bean seeds which has high homology to the major triglyceride biosynthetic enzyme of fungi and animals. Phytochemistry 67: 2541–2549PubMedCrossRefGoogle Scholar
- Kunst L, Browse J and Somerville C (1988) Altered regulation of lipid biosynthesis in a mutant of Arabidopsis deficient in chloroplast glycerol-3-phosphate acyltransferase activity. Proc Natl Acad Sci USA 85: 4143–4147PubMedCrossRefGoogle Scholar
- Maanni AE, Dubertret G, Delrieu M, Rochon A and Tremo-lieres A (1998) Mutants of Chlamydomonas reinhardtii affected in phosphatidylglycerol metabolism and thyla-koid biogenesis. Plant Physiol Biochem 36: 609–619CrossRefGoogle Scholar
- Maroc J, Tremolieres A, Garnier J and Guyon D (1987) Oligomeric form of the light-harvesting chlorophyll a + b-protein complex CP-II, phosphatidyldiacylglyc-erol, Δ3-trans-hexadecenoic acid and energy transfer in Chlamydomonas reinhardtii, wild type and mutants. Bio-chim Biophys Acta 893: 91–99CrossRefGoogle Scholar
- McConn M and Browse J (1998) Polyunsaturated membranes are required for photosynthetic competence in a mutant of Arabidopsis. Plant J 15: 521–530PubMedCrossRefGoogle Scholar
- Mendiola-Morgenthaler L, Eichenberger W and Bos-chetti A (1985) Isolation of chloroplast envelopes from Chlamydomonas. Lipid and polypeptide composition. Plant Sci Lett 41: 97–104CrossRefGoogle Scholar
- Menke W, Radunz A, Schmid GH, Koenig F and Hirtz RD (1976) Intermolecular interactions of polypeptides and lipids in the thylakoid membrane. Z Naturforsch [C] 31: 436–444Google Scholar
- Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernandez E, Fukuzawa H, Gonzalez-Ballester D, Gonzalez-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riano-Pachon DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martinez D, Ngau WC, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS and Grossman AR (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245–250PubMedCrossRefGoogle Scholar
- Merzlyak MN, Chivkunova OB, Gorelova OA, Reshetnik-ova IV, Solovchenko AE, Khozin-Goldberg I and 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: 833–843CrossRefGoogle Scholar
- Minoda A, Sato N, Nozaki H, Okada K, Takahashi H, Sonoike K and Tsuzuki M (2002) Role of sulfoquinovosyl diacylglyc-erol for the maintenance of photosystem II in Chlamydomonas reinhardtii. Eur J Biochem 269: 2353–2358PubMedCrossRefGoogle Scholar
- Minoda A, Sonoike K, Okada K, Sato N and Tsuzuki M (2003) Decrease in the efficiency of the electron donation to tyrosine Z of photosystem II in an SQDG-deficient mutant of Chlamydomonas. FEBS Lett 553: 109–112PubMedCrossRefGoogle Scholar
- Mongrand S, Besoule J-J, Cabantous F and Cassagne C (1998) The C16:3/C18:3 fatty acid balance in photosyn-thetic tissues from 468 plant species. Phytochemistry 49: 1049–1064CrossRefGoogle Scholar
- Mongrand S, Badoc A, Patouille B, Lacomblez C, Chavent M, Cassagne C and Bessoule JJ (2001) Taxonomy of gymnospermae: multivariate analyses of leaf fatty acid composition. Phytochemistry 58: 101–115PubMedCrossRefGoogle Scholar
- Moore B (2004) Bifunctional and moonlighting enzymes: lighting the way to regulatory control. Trends Plant Sci 9: 221–228PubMedCrossRefGoogle Scholar
- Moore TS, Du Z and Chen Z (2001) Membrane lipid biosynthesis in Chlamydomonas reinhardtii. In vitro biosynthesis of diacylglyceryltrimethylhomoserine. Plant Physiol 125: 423–429PubMedCrossRefGoogle Scholar
- Murata N and Tasaka Y (1997) Glycerol-3-phosphate acyl-transferase in plants. Biochim Biophys Acta 1348: 10–16PubMedCrossRefGoogle Scholar
- Nakamura Y, Tsuchiya M and Ohta H (2007) Plastidic phos-phatidic acid phosphatases identified in a distinct subfamily of lipid phosphate phosphatases with prokaryotic origin. J Biol Chem 282: 29013–29021PubMedCrossRefGoogle Scholar
- Nerlich A, von Orlow M, Rontein D, Hanson AD and Dörmann P (2007) Deficiency in phosphatidylserine decarboxylase activity in the psd1 psd2 psd3 triple mutant of Arabidop-sis affects phosphatidylethanolamine accumulation in mitochondria. Plant Physiol 144: 904–914PubMedCrossRefGoogle Scholar
- Niyogi KK (1999) Photoprotection revisited: Genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50: 333–359PubMedCrossRefGoogle Scholar
- Ohlrogge J and Browse J (1995) Lipid biosynthesis. Plant Cell 7: 957–970PubMedGoogle Scholar
- Picaud A, Creach A and Tremolieres A (1991) Studies on the stimulation by light of fatty-acid synthesis in Chlamydomonas reinhardtii whole cells. Plant Physiol Biochem 29: 441–448Google Scholar
- Pick U, Gounaris K, Weiss M and Barber J (1985) Tightly bound sulfolipids in chloroplast CF0-CF1. Biochim Bio-phys Acta 808: 415–420CrossRefGoogle Scholar
- Pineau B, Girard-Bascou J, Eberhard S, Choquet Y, Tremo-lieres A, Gerard-Hirne C, Bennardo-Connan A, Decottig-nies P, Gillet S and Wollman FA (2004) A single mutation that causes phosphatidylglycerol deficiency impairs synthesis of photosystem II cores in Chlamydomonas rein-hardtii. Eur J Biochem 271: 329–338PubMedCrossRefGoogle Scholar
- Rabbani S, Beyer P, Von Lintig J, Hugueney P and Kleinig H (1998) Induced β-carotene synthesis driven by tria-cylglycerol deposition in the unicellular alga Dunaliella bardawil. Plant Physiol 116: 1239–1248PubMedCrossRefGoogle Scholar
- Reyes-Prieto A, Weber AP and Bhattacharya D (2007) The origin and establishment of the plastid in algae and plants. Annu Rev Genet 41: 147–168PubMedCrossRefGoogle Scholar
- Richardson K, Beardall J and Raven JA (1983) Adaptation of unicellular algae to irradiance — an analysis of strategies. New Phytol 93: 157–191CrossRefGoogle Scholar
- Riekhof WR and Benning C (2008) Glycerolipid biosynthesis. In: Stern D and Harris EH (eds) The Chlamydomonas Sourcebook: Organellar and Metabolic Processes, 2. Elsevier, Dordrecht, pp. 41–68Google Scholar
- Riekhof WR, Ruckle ME, Lydic TA, Sears BB and Benning C (2003) The sulfolipids 2′-O-acyl-sulfoquinovosyldia-cylglycerol and sulfoquinovosyldiacylglycerol are absent from a Chlamydomonas reinhardtii mutant deleted in SQD1. Plant Physiol 133: 864–874PubMedCrossRefGoogle Scholar
- Riekhof WR, Andre C and Benning C (2005a) Two enzymes, BtaA and BtaB, are sufficient for betaine lipid biosynthesis in bacteria. Arch Biochem Biophys 441: 96–105CrossRefGoogle Scholar
- Riekhof WR, Sears BB and Benning C (2005b) Annotation of genes involved in glycerolipid biosynthesis in Chlamydomonas reinhardtii: discovery of the betaine lipid synthase BTA1Cr. Euk Cell 4: 242–252CrossRefGoogle Scholar
- Roessler PG (1988) Effects of silicon deficiency on lipid composition and metabolism in the diatom Cyclotella cryptica. J Phycol 24: 394–400Google Scholar
- Roughan PG and Slack CR (1982) Cellular organization of glycerolipid metabolism. Ann Rev Plant Physiol 33: 97–132CrossRefGoogle Scholar
- Roughan PG, Holland R and Slack CR (1980) The role of chloroplasts and microsomal fractions in polar-lipid synthesis from [1–14C]acetate by cell-free preparations from spinach (Spinacia oleracea) leaves. Biochem J 188: 17–24PubMedGoogle Scholar
- Routaboul JM, Benning C, Bechtold N, Caboche M and Lep-iniec L (1999) The TAG1 locus of Arabidopsis encodes for a diacylglycerol acyltransferase. Plant Physiol Bio-chem 37: 831–840CrossRefGoogle Scholar
- Sanda S, Leustek T, Theisen M, Garavito M and Benning C (2001) Recombinant Arabidopsis SQD1 converts UDP-glucose and sulfite to the sulfolipid head precursor UDP-sulfoquinovose in vitro. J Biol Chem 276: 3941–3946PubMedCrossRefGoogle Scholar
- Santos-Mendoza M, Dubreucq B, Baud S, Parcy F, Caboche M and Lepiniec L (2008) Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J 54: 608–620PubMedCrossRefGoogle Scholar
- Sato N (1988) Dual role of methionine in the biosynthesis of diacylglyceryltrimethylhomoserine in Chlamydomonas reinhardtii. Plant Physiol 86: 931–934PubMedCrossRefGoogle Scholar
- Sato N (1991) Lipids in Cryptomonas CR-1. II. Biosynthesis of betaine lipids and galactolipids. Plant Cell Physiol 32: 845–851Google Scholar
- Sato N (1992) Betaine lipids. Bot Mag Tokyo 105: 185–197CrossRefGoogle Scholar
- Sato N and Furuya M (1983) Isolation and identification of diacylglyceryl-O-4′-(N,N,N-trimethyl)-homoserine from the fern Adiantum capillus-veneris L. Plant Cell Physiol 24: 1113–1120Google Scholar
- Sato N and Kato K (1988) Analysis and biosynthesis of diacylglyceryl-N,N,N-trimethylhomoserine in cells of Marchantia in suspension culture. Plant Sci 55: 21–25CrossRefGoogle Scholar
- Sato N and Murata N (1991) Transition of lipid phase in aqueous dispersions of diacylglyceryltrimethylhomoser-ine. Biochim Biophys Acta 1082: 108–111PubMedCrossRefGoogle Scholar
- Sato N, Sonoike K, Tsuzuki M and Kawaguchi A (1995a) Impaired photosystem II in a mutant of Chlamydomonas reinhardtii defective in sulfoquinovosyl diacylglycerol. Eur J Biochem 234: 16–23CrossRefGoogle Scholar
- Sato N, Tsuzuki M, Matsuda Y, Ehara T, Osafune T and Kawaguchi A (1995b) Isolation and characterization of mutants affected in lipid metabolism of Chlamydomonas reinhardtii. Eur J Biochem 230: 987–993CrossRefGoogle Scholar
- Sato N, Fujiwara S, Kawaguchi A and Tsuzuki M (1997) Cloning of a gene for chloroplast omega6 desaturase of a green alga, Chlamydomonas reinhardtii. J Biochem 122: 1224–1232PubMedCrossRefGoogle Scholar
- Sato N, Hagio M, Wada H and Tsuzuki M (2000) Requirement of phosphatidylglycerol for photosynthetic function in thylakoid membranes. Proc Natl Acad Sci USA 97: 10655–10660PubMedCrossRefGoogle Scholar
- Shanklin J and Somerville C (1991) Stearoyl-acyl-carrier-protein desaturase from higher plants is structurally unrelated to the animal and fungal homologs. Proc Natl Acad Sci USA 88: 2510–2514PubMedCrossRefGoogle Scholar
- Sheehan J, Dunahay T, Benemann J, and Roessler PA (1998) Look Back at the U.S. Department of Energy's Aquatic Species Program: Biodiesel from Algae. US Department of Energy National Renewable Energy Laboratory, http://www1.eere.energy.gov/biomass/pdfs/biodiesel_from_algae.pdf
- Silflow CD and Lefebvre PA (2001) Assembly and motil-ity of eukaryotic cilia and flagella. Lessons from Chlamydomonas reinhardtii. Plant Physiol 127: 1500– 1507PubMedCrossRefGoogle Scholar
- Sineshchekov OA, Jung KH and Spudich JL (2002) Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 99: 8689–8694PubMedGoogle Scholar
- Sirevag R and Levine RP (1972) Fatty acid synthetase from Chlamydomonas reinhardtii. J Biol Chem 247: 2586– 2591PubMedGoogle Scholar
- Spolaore P, Joannis-Cassan C, Duran E and Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101: 87–96PubMedCrossRefGoogle Scholar
- Stobart AK and Stymne S (1985) The regulation of the fatty acid composition of the triacyglycerols in microsomal preparations from avocado mesocarp and the developing cotyledons of safflower. Planta 163: 119–125CrossRefGoogle Scholar
- Stroebel D, Choquet Y, Popot JL and Picot D (2003) An atypical haem in the cytochrome b 6 f complex. Nature 426: 413–418PubMedCrossRefGoogle Scholar
- Suen Y, Hubbard JS, Holzer G and Tornabene TG (1987) Total lipid production of the green alga Nannochlorop-sis sp. QII under different nitrogen regimes. J Phycol 23: 289–296CrossRefGoogle Scholar
- Sugimoto K, Sato N and 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. FEBS Lett 581: 4519–4522PubMedCrossRefGoogle Scholar
- Sugimoto K, Midorikawa T, Tsuzuki M and Sato N (2008) Upregulation of PG synthesis on sulfur-starvation for PSI in Chlamydomonas. Biochem Biophys Res Commun 369: 660–665PubMedCrossRefGoogle Scholar
- Tam LW and Lefebvre PA (1993) Cloning of flagellar genes in Chlamydomonas reinhardtii by DNA insertional muta-genesis. Genetics 135: 375–384PubMedGoogle Scholar
- The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thal-iana. Nature 408: 796–815CrossRefGoogle Scholar
- Tornabene TG, Holzer G, Lien S and Burris N (1983) Lipid composition of the nitrogen starved green alga Neochloris oleoabundans. Enz Microb Tech 5: 435–440CrossRefGoogle Scholar
- Tsuzuki M, Ohnuma E, Sato N, Takaku T and Kawaguchi A (1990) Effects of CO2 concentration during growth on fatty acid composition in microalgae. Plant Physiol 93: 851–856PubMedCrossRefGoogle Scholar
- Vance JE and Steenbergen R (2005) Metabolism and functions of phosphatidylserine. Prog Lipid Res 44: 207–234PubMedCrossRefGoogle Scholar
- Vijayan P, Routaboul JM and Browse J (1998) A genetic approach to investigating membrane lipid structure and photosynthetic function. In: Siegenthaler P-A and Murata N (eds) Lipids in Photosynthesis: Structure, Function and Genetics. Kluwer, Dordrecht, pp. 263–285Google Scholar
- Vogel G and 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: 427–436Google Scholar
- Wallis JG and Browse J (2002) Mutants of Arabidopsis reveal many roles for membrane lipids. Prog Lipid Res 41: 254–278PubMedCrossRefGoogle Scholar
- Weers P and Gulati R (1997) Growth and reproduction of Daphnia galeata in response to changes in fatty acids, phosphorus, and nitrogen in Chlamydomonas reinhardtii. Limnol Oceanogr 42: 1586–1589CrossRefGoogle Scholar
- Wolff RL and Christie WW (2002) Structures, practical sources (gymnosperm seeds), gas-liquid chromatographic data (equivalent chain lengths), and mass spectrometric characteristics of all-cis 5-olefinic acids. Eur J Lipid Sci Technol 104: 234–244CrossRefGoogle Scholar
- Wu-Scharf D, Jeong BR, Zhang CM and Cerutti H (2000) Transgene and transposon silencing in Chlamydomonas reinhardtii by a DEAH-Box RNA helicase. Science 290: 1159–1162PubMedCrossRefGoogle Scholar
- Xu C, Härtel H, Wada H, Hagio M, Yu B, Eakin C and Ben-ning C (2002) The pgp1 locus of Arabidopsis encodes a phosphatidylglycerol synthase with impaired activity. Plant Physiol 129: 594–604PubMedCrossRefGoogle Scholar
- Xu C, Cornish AJ, Froehlich JE and Benning C (2006) Phos-phatidylglycerol biosynthesis in chloroplasts of Arabidop-sis mutants deficient in acyl-ACP glycerol-3-phosphate acyltransferase. Plant J 47: 296–309PubMedCrossRefGoogle Scholar
- Yang W, Mason CB, Pollock SV, Lavezzi T, Moroney JV and Moore TS (2004) Membrane lipid biosynthesis in Chlamydomonas reinhardtii: expression and characterization of CTP:phosphoethanolamine cytidylyltransferase. Biochem J 382: 51–57PubMedCrossRefGoogle Scholar
- Yu B, Xu C and Benning C (2002) Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proc Natl Acad Sci USA 99: 5732–5737PubMedCrossRefGoogle Scholar
- Zhekisheva M, Boussiba S, Khozin-Goldberg I, Zarka A and Cohen Z (2002) Accumulation of oleic acid in Haema-tococcus pluvialis (Chlorophyceae) under nitrogen starvation or high light is correlated with that of astaxanthin esters. J Phycol 38: 325–331CrossRefGoogle Scholar
- Zheng P, Allen WB, Roesler K, Williams ME, Zhang S, Li J, Glassman K, Ranch J, Nubel D, Solawetz W, Bhattra-makki D, Llaca V, Deschamps S, Zhong GY, Tarczynski MC and Shen B (2008) A phenylalanine in DGAT is a key determinant of oil content and composition in maize. Nat Genet 40: 367–372PubMedCrossRefGoogle Scholar
- Zheng Z, Xia Q, Dauk M, Shen W, Selvaraj G and Zou J (2003) Arabidopsis AtGPAT1, a member of the membrane-bound glycerol-3-phosphate acyltransferase gene family, is essential for tapetum differentiation and male fertility. Plant Cell 15: 1872–1887PubMedCrossRefGoogle Scholar
- Zou J, Wei Y, Jako C, Kumar A, Selvaraj G and Taylor DC (1999) The Arabidopsis thaliana TAG1 mutant has a mutation in a diacylglycerol acyltransferase gene. Plant J 19: 645–653PubMedCrossRefGoogle Scholar