Triacylglycerol accumulation in photosynthetic cells in plants and algae

Subcellular Biochemistry

Volumn 86, Issue , 2016, Pages 179-205

  Du, Zhi Yan ^a   Benning, Christoph ^a  

^a Michigan State University   (United States)

Author keywords

Lipid droplet; Lipid metabolism; Lipid remodeling; Nutrient deprivation; Photosynthesis

Indexed keywords

TRIACYLGLYCEROL;

BIOSYNTHESIS; CYTOLOGY; METABOLISM; MICROALGA; PHOTOSYNTHESIS; PHYSIOLOGICAL STRESS; PLANT;

MICROALGAE; PHOTOSYNTHESIS; PLANTS; STRESS, PHYSIOLOGICAL; TRIGLYCERIDES;

EID: 84962439134     PISSN: 03060225     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-3-319-25979-6_8     Document Type: Article

References (147)

1. Aaronson S (1973) Effect of incubation temperature on the macromolecular and lipid content of the phytoflagellate Ochromonas danica. J Phycol 9: 111-113.
2. Abdulla R, Chan ES, Ravindra P (2011) Biodiesel production from Jatropha curcas: a critical review. Crit Rev Biotechnol 31: 53-64.
3. 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.
4. 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.
5. 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.
6. ASTM (2002) Standard specification for diesel fuel oils. ASTM D975-02. American Society for Testing and Materials, West Conshohocken.
7. Barber J (2009) Photosynthetic energy conversion: natural and artificial. Chem Soc Rev 38: 185-196.
8. 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.
9. Bates PD, Stymne S, Ohlrogge J (2013) Biochemical pathways in seed oil synthesis. Curr Opin Plant Biol 16: 358-364.
10. Baud S, Lepiniec L (2010) Physiological and developmental regulation of seed oil production. Prog Lipid Res 49: 235-249.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. 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.
17. 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.
18. Bruinsma J (ed) (2003) World agriculture: towards 2015/2030. Earthscan, London.
19. 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.
20. 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.
21. Chapman KD, Ohlrogge JB (2012) Compartmentation of triacylglycerol accumulation in plants. J Biol Chem 287: 2288-2294.
22. Chapman KD, Dyer JM, Mullen RT (2013) Commentary: why don't plant leaves get fat? Plant Sci 207: 128-134.
23. Cheah WY, Show PL, Chang JS, Ling TC, Juan JC (2014) Biosequestration of atmospheric CO 2 and flue gas-containing CO 2 by microalgae. Bioresour Technol. doi: 10. 1016/j. biortech. 2014. 1011. 1026.
24. 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.
25. Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25: 294-306.
26. Chisti Y (2013) Constraints to commercialization of algal fuels. J Biotechnol 167: 201-214.
27. 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.
28. Collins RP, Kalnins K (1969) The fatty acids of Cryptomonas ovata var. palustris. Phyton 26: 47-50.
29. 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.
30. 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.
31. 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.
32. 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.
33. Durrett TP, Benning C, Ohlrogge J (2008) Plant triacylglycerols as feedstocks for the production of biofuels. Plant J 54: 593-607.
34. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. Georgianna DR, Mayfield SP (2012) Exploiting diversity and synthetic biology for the production of algal biofuels. Nature 488: 329-335.
42. 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.
43. Harris EH (2001) Chlamydomonas as a model organism. Annu Rev Plant Physiol Plant Mol Biol 52: 363-406.
44. 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.
45. 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.
46. 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.
47. 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.
48. 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.
49. 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-Dorfmanlike lipid droplet accumulation in plants. Proc Natl Acad Sci U S A 107: 17833-17838.
50. 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.
51. 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.
52. John RP, Anisha GS, Nampoothiri KM, Pandey A (2011) Micro and macroalgal biomass: a renewable source for bioethanol. Bioresour Technol 102: 186-193.
53. Jones CS, Mayfield SP (2012) Algae biofuels: versatility for the future of bioenergy. Curr Opin Biotechnol 23: 346-351.
54. 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.
55. Kaup MT, Froese CD, Thompson JE (2002) A role for diacylglycerol acyltransferase during leaf senescence. Plant Physiol 129: 1616-1626.
56. Kelly AA, van Erp H, Quettier AL, Shaw E, Menard G, Kurup S, Eastmond PJ (2013) The SUGARDEPENDENT1 lipase limits triacylglycerol accumulation in vegetative tissues of Arabidopsis. Plant Physiol 162: 1282-1289.
57. Khotimchenko SV, Yakovleva IM (2005) Lipid composition of the red alga Tichocarpus crinitus exposed to different levels of photon irradiance. Phytochemistry 66: 73-79.
58. 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.
59. Khozin-Goldberg I, Cohen Z (2011) Unraveling algal lipid metabolism: recent advances in gene identification. Biochimie 93: 91-100.
60. 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.
61. 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.
62. 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.
63. 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.
64. 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.
65. 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.
66. 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.
67. 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.
68. 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.
69. 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.
70. 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.
71. Liu B, Benning C (2013) Lipid metabolism in microalgae distinguishes itself. Curr Opin Biotechnol 24: 300-309.
72. 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.
73. Lynch DV, Thompson GA (1982) Low temperature-induced alterations in the chloroplast and microsomal membranes of Dunaliella salina. Plant Physiol 69: 1369-1375.
74. 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.
75. 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.
76. 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.
77. 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 H 2 production by sulfur depletion. J Biol Chem 284: 23415-23425.
78. 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.
79. 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.
80. 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.
81. 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.
82. Moellering ER, Benning C (2011) Galactoglycerolipid metabolism under stress: a time for remodeling. Trends Plant Sci 16: 98-107.
83. Moellering ER, Muthan B, Benning C (2010) Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330: 226-228.
84. 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.
85. Napolitano GE (1994) The relationship of lipids with light and chlorophyll measurement in freshwater algae and periphyton. J Phycol 30: 943-950.
86. 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.
87. 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.
88. Ogas J, Cheng JC, Sung ZR, Somerville C (1997) Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. Science 277: 91-94.
89. 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.
90. Ohlrogge JB, Chapman KD (2011) The seeds of green energy: expanding the contribution of plant oils as biofuels. Biochemist 33: 34-38.
91. Ohlrogge J, Allen D, Berguson B, Dellapenna D, Shachar-Hill Y, Stymne S (2009) Energy. Driving on biomass. Science 324: 1019-1020.
92. 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.
93. 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.
94. 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.
95. Pugh PR (1971) Changes in the fatty acid composition of Coscinodiscus eccentricus with cultureage and salinity. Mar Biol 11: 118-124.
96. 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.
97. 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.
98. 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.
99. 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.
100. 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.
101. Rochaix JD (1995) Chlamydomonas reinhardtii as the photosynthetic yeast. Annu Rev Genet 29: 209-230.
102. 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.
103. 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.
104. 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.
105. 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.
106. 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.
107. 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.
108. 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.
109. 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.
110. 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.
111. 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.
112. 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.
113. 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.
114. 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.
115. 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.
116. 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.
117. 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.
118. 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.
119. 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.
120. Stoller EW, Weber EJ (1975) Differential cold tolerance, starch, sugar, protein, and lipid of yellow and purple nutsedge tubers. Plant Physiol 55: 859-863.
121. 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.
122. 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.
123. 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.
124. 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.
125. 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.
126. 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.
127. 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.
128. 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.
129. US Department of Energy (2007) Annual energy outlook 2007. Report number DOE/EIA-0383. Energy Information Administration, US Department of Energy, Washington, DC.
130. 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.
131. 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: oilseedlike triacylglycerol yields from plant leaves. Plant Biotechnol J 12: 231-239.
132. 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.
133. 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.
134. 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.
135. 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.
136. 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.
137. 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.
138. 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.
139. 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.
140. 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.
141. 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.
142. Yang Y, Yu X, Song L, An C (2011) ABI4 activates DGAT1 expression in Arabidopsis seedlings during nitrogen deficiency. Plant Physiol 156: 873-883.
143. 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.
144. 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.
145. 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.
146. 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.
147. 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.