Stress-induced neutral lipid biosynthesis in microalgae — Molecular, cellular and physiological insights

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1861, Issue 9, 2016, Pages 1269-1281

  Zienkiewicz, Krzysztof ^a,b,c   Du, Zhi Yan ^a,b   Ma, Wei ^a   Vollheyde, Katharina ^c   Benning, Christoph ^a,b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Diacylglycerol:acyltransferase (DGAT); Lipid; Lipid droplet (LD); Microalgae; Phospholipid:diacylglycerol acyltransferase (PDAT); Triacylglycerol (TAG)

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; FATTY ACID SYNTHASE; PYRUVATE DEHYDROGENASE COMPLEX; TRIACYLGLYCEROL; BIOFUEL; FATTY ACID; LIPID;

AMINO ACID SEQUENCE; ARTICLE; CELLULAR DISTRIBUTION; CHLAMYDOMONAS REINHARDTII; CHLORELLA; CHLOROPLAST; CONVERGENT EVOLUTION; ECTOPIC EXPRESSION; ENDOPLASMIC RETICULUM STRESS; ENZYME ANALYSIS; FATTY ACID SYNTHESIS; GENE AMPLIFICATION; GENE SILENCING; GENETIC ANALYSIS; HETEROLOGOUS EXPRESSION; LIPID METABOLISM; LIPID STORAGE; LIPOGENESIS; LIPOLYSIS; MICROALGA; MOLECULAR BIOLOGY; MOLECULAR MECHANICS; NANNOCHLOROPSIS; NANNOCHLOROPSIS GADITANA; NONHUMAN; PHAEODACTYLUM TRICORNUTUM; PHENOTYPE; PHOTOSYNTHESIS; PHYLOGENY; PLANT GENE; PLANT GENOME; PLANT STRESS; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; RNA INTERFERENCE; TRANSIENT EXPRESSION; BIOSYNTHESIS; GENETICS; METABOLISM;

BIOFUELS; FATTY ACIDS; GENOME, PLANT; LIPID METABOLISM; LIPIDS; MICROALGAE; PHOTOSYNTHESIS; TRIGLYCERIDES;

EID: 84975706443     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2016.02.008     Document Type: Article

References (142)

1. [1] Radakovits, R., Jinkerson, R.E., Darzins, A., Posewitz, M.C., Genetic engineering of algae for enhanced biofuel production. Eukaryot. Cell 9 (2010), 486–501.
2. [2] Miller, R., Wu, G., Deshpande, R.R., Vieler, A., Gartner, K., Li, X., Moellering, E.R., Zauner, S., Cornish, A.J., Liu, B., Bullard, B., Sears, B.B., Kuo, M.H., Hegg, E.L., Shachar-Hill, Y., Shiu, S.H., Benning, C., Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol. 154 (2010), 1737–1752.
3. [3] Yang, Z., Ohlrogge, J.B., Turnover of fatty acids during natural senescence of Arabidopsis, Brachypodium, and Switchgrass and in Arabidopsis β-oxidation mutants. Plant Physiol. 150 (2009), 1981–1989.
4. [4] Boyle, N.R., Page, M.D., Liu, B., Blaby, I.K., Casero, D., Kropat, J., Cokus, S.J., Hong-Hermesdorf, A., Shaw, J., Karpowicz, S.J., Gallaher, S.D., Johnson, S., Benning, C., Pellegrini, M., Grossman, A., Merchant, S.S., Three acyltransferases and nitrogen-responsive regulator are implicated in nitrogen starvation-induced triacylglycerol accumulation in Chlamydomonas. J. Biol. Chem. 287 (2012), 15811–15825.
5. [5] Giroud, C., Gerber, A., Eichenberger, W., Lipids of Chlamydomonas reinhardtii. Analysis of molecular species and intracellular site(s) of biosynthesis. Plant Cell Physiol. 29 (1988), 587–595.
6. [6] Hu, Q., Sommerfeld, M., Jarvis, E., Ghirardi, M., Posewitz, M., Seibert, M., Darzins, A., Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J. Cell Mol. Biol. 54 (2008), 621–639.
7. [7] Zienkiewicz, K., Castro, A.J., Alche Jde, D., Zienkiewicz, A., Suarez, C., Rodriguez-Garcia, M.I., Identification and localization of a caleosin in olive (Olea europaea L.) pollen during in vitro germination. J. Exp. Bot. 61 (2010), 1537–1546.
8. [8] Liu, B., Benning, C., Lipid metabolism in microalgae distinguishes itself. Curr. Opin. Biotechnol. 24 (2013), 300–309.
9. [9] Fan, J., Andre, C., Xu, C., A chloroplast pathway for the de novo biosynthesis of triacylglycerol in Chlamydomonas reinhardtii. FEBS Lett. 585 (2011), 1985–1991.
10. [10] Vieler, A., Wu, G., Tsai, C.H., Bullard, B., Cornish, A.J., Harvey, C., Reca, I.B., Thornburg, C., Achawanantakun, R., Buehl, C.J., Campbell, M.S., Cavalier, D., Childs, K.L., Clark, T.J., Deshpande, R., Erickson, E., Ferguson, A. Armenia, Handee, W., Kong, Q., Li, X., Liu, B., Lundback, S., Peng, C., Roston, R.L., Sanjaya, Simpson, J.P., Terbush, A., Warakanont, J., Zauner, S., Farre, E.M., Hegg, E.L., Jiang, N., Kuo, M.H., Lu, Y., Niyogi, K.K., Ohlrogge, J., Osteryoung, K.W., Shachar-Hill, Y., Sears, B.B., Sun, Y., Takahashi, H., Yandell, M., Shiu, S.H., Benning, C., Genome, functional gene annotation, and nuclear transformation of the heterokont oleaginous alga Nannochloropsis oceanica CCMP1779. PLoS Genet., 8, 2012, e1003064.
11. [11] Li, J., Han, D., Wang, D., Ning, K., Jia, J., Wei, L., Jing, X., Huang, S., Chen, J., Li, Y., Hu, Q., Xu, J., Choreography of transcriptomes and lipidomes of nannochloropsis reveals the mechanisms of oil synthesis in microalgae. Plant Cell 26 (2014), 1645–1665.
12. [12] Yang, W., Pollard, M., Li-Beisson, Y., Beisson, F., Feig, M., Ohlrogge, J., A distinct type of glycerol-3-phosphate acyltransferase with sn-2 preference and phosphatase activity producing 2-monoacylglycerol. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 12040–12045.
13. [13] Reddy, V.S., Rao, D.K., Rajasekharan, R., Functional characterization of lysophosphatidic acid phosphatase from Arabidopsis thaliana. Biochim. Biophys. Acta 1801 (2010), 455–461.
14. [14] Petrie, J.R., Vanhercke, T., Shrestha, P., El Tahchy, A., White, A., Zhou, X.R., Liu, Q., Mansour, M.P., Nichols, P.D., Singh, S.P., Recruiting a new substrate for triacylglycerol synthesis in plants: the monoacylglycerol acyltransferase pathway. PLoS ONE, 7, 2012, e35214.
15. [15] Simpson, J.P., Ohlrogge, J.B., A novel pathway for triacylglycerol biosynthesis is responsible for the accumulation of massive quantities of glycerolipids in the surface wax of bayberry (Myrica pensylvanica) fruit. Plant Cell, 2016.
16. [16] Yen, C.L., Stone, S.J., Koliwad, S., Harris, C., Farese, R.V. Jr., Thematic review series: glycerolipids. DGAT enzymes and triacylglycerol biosynthesis. J. Lipid Res. 49 (2008), 2283–2301.
17. [17] Dahlqvist, A., Ståhl, U., Lenman, M., Banas, A., Lee, M., Sandager, L., Ronne, H., Stymne, S., Phospholipid:diacylglycerol acyltransferase: an enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants. Proc. Natl. Acad. Sci. U. S. A. 97 (2000), 6487–6492.
18. [18] Zhang, M., Fan, J., Taylor, D.C., Ohlrogge, J.B., DGAT1 and PDAT1 acyltransferases have overlapping functions in Arabidopsis triacylglycerol biosynthesis and are essential for normal pollen and seed development. Plant Cell 21 (2009), 3885–3901.
19. [19] Yoon, K., Han, D., Li, Y., Sommerfeld, M., Hu, Q., Phospholipid:diacylglycerol acyltransferase is a multifunctional enzyme involved in membrane lipid turnover and degradation while synthesizing triacylglycerol in the unicellular green microalga Chlamydomonas reinhardtii. Plant Cell 24 (2012), 3708–3724.
20. [20] Merchant, S.S., Prochnik, S.E., Vallon, O., Harris, E.H., Karpowicz, S.J., Witman, G.B., Terry, A., Salamov, A., Fritz-Laylin, L.K., Marechal-Drouard, L., Marshall, W.F., Qu, L.H., Nelson, D.R., Sanderfoot, A.A., Spalding, M.H., Kapitonov, V.V., Ren, Q., Ferris, P., Lindquist, E., Shapiro, H., Lucas, S.M., Grimwood, J., Schmutz, J., Cardol, P., Cerutti, H., Chanfreau, G., Chen, C.L., Cognat, V., Croft, M.T., 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, P.A., Lemaire, S.D., Lobanov, A.V., Lohr, M., Manuell, A., Meier, I., Mets, L., Mittag, M., Mittelmeier, T., Moroney, J.V., Moseley, J., Napoli, C., Nedelcu, A.M., Niyogi, K., Novoselov, S.V., Paulsen, I.T., Pazour, G., Purton, S., Ral, J.P., Riano-Pachon, D.M., Riekhof, W., Rymarquis, L., Schroda, M., Stern, D., Umen, J., Willows, R., Wilson, N., Zimmer, S.L., Allmer, J., Balk, J., Bisova, K., Chen, C.J., Elias, M., Gendler, K., Hauser, C., Lamb, M.R., Ledford, H., Long, J.C., Minagawa, J., Page, M.D., Pan, J., Pootakham, W., Roje, S., Rose, A., Stahlberg, E., Terauchi, A.M., Yang, P., Ball, S., Bowler, C., Dieckmann, C.L., Gladyshev, V.N., Green, P., Jorgensen, R., Mayfield, S., Mueller-Roeber, B., Rajamani, S., Sayre, R.T., Brokstein, P., Dubchak, I., Goodstein, D., Hornick, L., Huang, Y.W., Jhaveri, J., Luo, Y., Martinez, D., Ngau, W.C., Otillar, B., Poliakov, A., Porter, A., Szajkowski, L., Werner, G., Zhou, K., Grigoriev, I.V., Rokhsar, D.S., Grossman, A.R., The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318 (2007), 245–250.
21. [21] Blanc, G., Duncan, G., Agarkova, I., Borodovsky, M., Gurnon, J., Kuo, A., Lindquist, E., Lucas, S., Pangilinan, J., Polle, J., Salamov, A., Terry, A., Yamada, T., Dunigan, D.D., Grigoriev, I.V., Claverie, J.M., Van Etten, J.L., The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell 22 (2010), 2943–2955.
22. [22] Palenik, B., Grimwood, J., Aerts, A., Rouze, P., Salamov, A., Putnam, N., Dupont, C., Jorgensen, R., Derelle, E., Rombauts, S., Zhou, K., Otillar, R., Merchant, S.S., Podell, S., Gaasterland, T., Napoli, C., Gendler, K., Manuell, A., Tai, V., Vallon, O., Piganeau, G., Jancek, S., Heijde, M., Jabbari, K., Bowler, C., Lohr, M., Robbens, S., Werner, G., Dubchak, I., Pazour, G.J., Ren, Q., Paulsen, I., Delwiche, C., Schmutz, J., Rokhsar, D., Van de Peer, Y., Moreau, H., Grigoriev, I.V., The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 7705–7710.
23. [23] Radakovits, R., Jinkerson, R.E., Fuerstenberg, S.I., Tae, H., Settlage, R.E., Boore, J.L., Posewitz, M.C., Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropsis gaditana. Nat. Commun., 3, 2012, 686.
24. [24] Wei, L., Xin, Y., Wang, D., Jing, X., Zhou, Q., Su, X., Jia, J., Ning, K., Chen, F., Hu, Q., Xu, J., Nannochloropsis plastid and mitochondrial phylogenomes reveal organelle diversification mechanism and intragenus phylotyping strategy in microalgae. BMC Genomics, 14, 2013, 534.
25. [25] 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, R.T., Zohar, Y., Chen, F., Hu, Q., Xu, J., Nannochloropsis genomes reveal evolution of microalgal oleaginous traits. PLoS Genet., 10, 2014.
26. [26] Bowler, C., Allen, A.E., Badger, J.H., Grimwood, J., Jabbari, K., Kuo, A., Maheswari, U., Martens, C., Maumus, F., Otillar, R.P., Rayko, E., Salamov, A., Vandepoele, K., Beszteri, B., Gruber, A., Heijde, M., Katinka, M., Mock, T., Valentin, K., Verret, F., Berges, J.A., Brownlee, C., Cadoret, J.P., Chiovitti, A., Choi, C.J., Coesel, S., De Martino, A., Detter, J.C., Durkin, C., Falciatore, A., Fournet, J., Haruta, M., Huysman, M.J., Jenkins, B.D., Jiroutova, K., Jorgensen, R.E., Joubert, Y., Kaplan, A., Kroger, N., Kroth, P.G., La Roche, J., Lindquist, E., Lommer, M., Martin-Jezequel, V., Lopez, P.J., Lucas, S., Mangogna, M., McGinnis, K., Medlin, L.K., Montsant, A., Secq, M.P. Oudot-Le, Napoli, C., Obornik, M., Parker, M.S., Petit, J.L., Porcel, B.M., Poulsen, N., Robison, M., Rychlewski, L., Rynearson, T.A., Schmutz, J., Shapiro, H., Siaut, M., Stanley, M., Sussman, M.R., Taylor, A.R., Vardi, A., von Dassow, P., Vyverman, W., Willis, A., Wyrwicz, L.S., Rokhsar, D.S., Weissenbach, J., Armbrust, E.V., Green, B.R., Van de Peer, Y., Grigoriev, I.V., The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456 (2008), 239–244.
27. [27] Molnar, A., Bassett, A., Thuenemann, E., Schwach, F., Karkare, S., Ossowski, S., Weigel, D., Baulcombe, D., Highly specific gene silencing by artificial microRNAs in the unicellular alga Chlamydomonas reinhardtii. Plant J. Cell Mol. Biol. 58 (2009), 165–174.
28. [28] Merchant, S.S., Kropat, J., Liu, B., Shaw, J., Warakanont, J., TAG, you're it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation. Curr. Opin. Biotechnol. 23 (2012), 352–363.
29. [29] Zhang, C., Hu, H., High-efficiency nuclear transformation of the diatom Phaeodactylum tricornutum by electroporation. Mar. Genomics 16 (2014), 63–66.
30. [30] Miyahara, M., Aoi, M., Inoue-Kashino, N., Kashino, Y., Ifuku, K., Highly efficient transformation of the diatom Phaeodactylum tricornutum by multi-pulse electroporation. Biosci. Biotechnol. Biochem. 77 (2013), 874–876.
31. [31] Kilian, O., Benemann, C.S., Niyogi, K.K., Vick, B., High-efficiency homologous recombination in the oil-producing alga Nannochloropsis sp. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 21265–21269.
32. [32] Riekhof, W.R., Sears, B.B., Benning, C., Annotation of genes involved in glycerolipid biosynthesis in Chlamydomonas reinhardtii: discovery of the betaine lipid synthase BTA1Cr. Eukaryot. Cell 4 (2005), 242–252.
33. [33] Moellering, E., Miller, R., Benning, C., Molecular genetics of lipid metabolism in the model green alga Chlamydomonas reinhardtii. Wada, H., Murata, N., (eds.) Lipids in Photosynthesis, 2010, Springer Netherlands, 139–155 (Place Published).
34. [34] Li-Beisson, Y., Beisson, F., Riekhof, W., Metabolism of acyl-lipids in Chlamydomonas reinhardtii. Plant J. Cell Mol. Biol. 82 (2015), 504–522.
35. [35] Shtaida, N., Khozin-Goldberg, I., Solovchenko, A., Chekanov, K., Didi-Cohen, S., Leu, S., Cohen, Z., Boussiba, S., Downregulation of a putative plastid PDC E1alpha subunit impairs photosynthetic activity and triacylglycerol accumulation in nitrogen-starved photoautotrophic Chlamydomonas reinhardtii. J. Exp. Bot. 65 (2014), 6563–6576.
36. [36] Misra, N., Panda, P.K., Parida, B.K., Mishra, B.K., Phylogenomic study of lipid genes involved in microalgal biofuel production-candidate gene mining and metabolic pathway analyses. Evol. Bioinformatics Online 8 (2012), 545–564.
37. [37] Chapman, K.D., Ohlrogge, J.B., Compartmentation of triacylglycerol accumulation in plants. J. Biol. Chem. 287 (2012), 2288–2294.
38. [38] Gidda, S.K., Shockey, J.M., Rothstein, S.J., Dyer, J.M., Mullen, R.T., Arabidopsis thaliana GPAT8 and GPAT9 are localized to the ER and possess distinct ER retrieval signals: functional divergence of the dilysine ER retrieval motif in plant cells. Plant Physiol. Biochem. 47 (2009), 867–879.
39. [39] Deng, X.D., Cai, J.J., Fei, X.W., Involvement of phosphatidate phosphatase in the biosynthesis of triacylglycerols in Chlamydomonas reinhardtii. J. Zhejiang. Univ. Sci. B 14 (2013), 1121–1131.
40. [40] Shockey, J.M., Gidda, S.K., Chapital, D.C., Kuan, J.C., Dhanoa, P.K., Bland, J.M., Rothstein, S.J., Mullen, R.T., Dyer, J.M., Tung tree DGAT1 and DGAT2 have nonredundant functions in triacylglycerol biosynthesis and are localized to different subdomains of the endoplasmic reticulum. Plant Cell 18 (2006), 2294–2313.
41. [41] Turchetto-Zolet, A.C., Maraschin, F.S., de Morais, G.L., Cagliari, A., Andrade, C.M., Margis-Pinheiro, M., Margis, R., Evolutionary view of acyl-CoA diacylglycerol acyltransferase (DGAT), a key enzyme in neutral lipid biosynthesis. BMC Evol. Biol., 11, 2011, 263.
42. [42] Wagner, M., Hoppe, K., Czabany, T., Heilmann, M., Daum, G., Feussner, I., Fulda, M., Identification and characterization of an acyl-CoA:diacylglycerol acyltransferase 2 (DGAT2) gene from the microalga O. tauri. Plant Physiol. Biochem. 48 (2010), 407–416.
43. [43] Guiheneuf, F., Leu, S., Zarka, A., Khozin-Goldberg, I., Khalilov, I., Boussiba, S., Cloning and molecular characterization of a novel acyl-CoA:diacylglycerol acyltransferase 1-like gene (PtDGAT1) from the diatom Phaeodactylum tricornutum. FEBS J. 278 (2011), 3651–3666.
44. [44] Gong, Y., Zhang, J., Guo, X., Wan, X., Liang, Z., Hu, C.J., Jiang, M., Identification and characterization of PtDGAT2B, an acyltransferase of the DGAT2 acyl-coenzyme A: diacylglycerol acyltransferase family in the diatom Phaeodactylum tricornutum. FEBS Lett. 587 (2013), 481–487.
45. [45] Chen, J.E., Smith, A.G., A look at diacylglycerol acyltransferases (DGATs) in algae. J. Biotechnol. 162 (2012), 28–39.
46. [46] Cao, H., Structure–function analysis of diacylglycerol acyltransferase sequences from 70 organisms. BMC Res. Notes, 4, 2011, 249.
47. [47] Moustafa, A., Beszteri, B., Maier, U.G., Bowler, C., Valentin, K., Bhattacharya, D., Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324 (2009), 1724–1726.
48. [48] Cavalier-Smith, T., Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J. Eukaryot. Microbiol. 46 (1999), 347–366.
49. [49] Pan, X., Peng, F.Y., Weselake, R.J., Genome-wide analysis of phospholipid:diacylglycerol acyltransferase (PDAT) genes in plants reveals the eudicot-wide PDAT gene expansion and altered selective pressures acting on the core eudicot PDAT paralogs. Plant Physiol. 167 (2015), 887–904.
50. [50] Iskandarov, U., Sitnik, S., Shtaida, N., Didi-Cohen, S., Leu, S., Khozin-Goldberg, I., Cohen, Z., Boussiba, S., Cloning and characterization of a GPAT-like gene from the microalga Lobosphaera incisa (Trebouxiophyceae): overexpression in Chlamydomonas reinhardtii enhances TAG production. J. Appl. Phycol., 2015, 1–13.
51. [51] Lv, H., Qu, G., Qi, X., Lu, L., Tian, C., Ma, Y., Transcriptome analysis of Chlamydomonas reinhardtii during the process of lipid accumulation. Genomics 101 (2013), 229–237.
52. [52] Tardif, M., Atteia, A., Specht, M., Cogne, G., Rolland, N., Brugiere, S., Hippler, M., Ferro, M., Bruley, C., Peltier, G., Vallon, O., Cournac, L., PredAlgo: a new subcellular localization prediction tool dedicated to green algae. Mol. Biol. Evol. 29 (2012), 3625–3639.
53. [53] La Russa, M., Bogen, C., Uhmeyer, A., Doebbe, A., Filippone, E., Kruse, O., Mussgnug, J.H., Functional analysis of three type-2 DGAT homologue genes for triacylglycerol production in the green microalga Chlamydomonas reinhardtii. J. Biotechnol. 162 (2012), 13–20.
54. [54] Hung, C.H., Ho, M.Y., Kanehara, K., Nakamura, Y., Functional study of diacylglycerol acyltransferase type 2 family in Chlamydomonas reinhardtii. FEBS Lett. 587 (2013), 2364–2370.
55. [55] Sanjaya, Miller, R., Durrett, T.P., Kosma, D.K., Lydic, T.A., Muthan, B., Koo, A.J., Bukhman, Y.V., Reid, G.E., Howe, G.A., Ohlrogge, J., Benning, C., Altered lipid composition and enhanced nutritional value of Arabidopsis leaves following introduction of an algal diacylglycerol acyltransferase 2. Plant Cell 25 (2013), 677–693.
56. [56] Fan, J., Cui, Y., Wan, M., Wang, W., Li, Y., Lipid accumulation and biosynthesis genes response of the oleaginous Chlorella pyrenoidosa under three nutrition stressors. Biotechnol. Biofuels, 7, 2014, 17.
57. [57] Guarnieri, M.T., Nag, A., Yang, S., Pienkos, P.T., Proteomic analysis of Chlorella vulgaris: potential targets for enhanced lipid accumulation. J. Proteome 93 (2013), 245–253.
58. [58] Petschnigg, J., Wolinski, H., Kolb, D., Zellnig, G., Kurat, C.F., Natter, K., Kohlwein, S.D., Good fat, essential cellular requirements for triacylglycerol synthesis to maintain membrane homeostasis in yeast. J. Biol. Chem. 284 (2009), 30981–30993.
59. [59] Siaut, M., Cuine, S., Cagnon, C., Fessler, B., Nguyen, M., Carrier, P., Beyly, A., Beisson, F., Triantaphylides, C., Li-Beisson, Y., Peltier, G., Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnol., 11, 2011, 7.
60. [60] Li, X., Moellering, E.R., Liu, B., Johnny, C., Fedewa, M., Sears, B.B., Kuo, M.H., Benning, C., A galactoglycerolipid lipase is required for triacylglycerol accumulation and survival following nitrogen deprivation in Chlamydomonas reinhardtii. Plant Cell 24 (2012), 4670–4686.
61. [61] Yang, Z.K., Niu, Y.F., Ma, Y.H., Xue, J., Zhang, M.H., Yang, W.D., Liu, J.S., Lu, S.H., Guan, Y., Li, H.Y., Molecular and cellular mechanisms of neutral lipid accumulation in diatom following nitrogen deprivation. Biotechnol. Biofuels, 6, 2013, 67.
62. [62] Chisti, Y., Biodiesel from microalgae. Biotechnol. Adv. 25 (2007), 294–306.
63. [63] Georgianna, D.R., Mayfield, S.P., Exploiting diversity and synthetic biology for the production of algal biofuels. Nature 488 (2012), 329–335.
64. [64] Tsai, C.H., Warakanont, J., Takeuchi, T., Sears, B.B., Moellering, E.R., Benning, C., 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 (2014), 15833–15838.
65. [65] Roessler, P.G., 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 (1988), 521–528.
66. [66] Traller, J.C., Hildebrand, M., 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 (2013), 244–252.
67. [67] Otsuka, H., 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 (1961), 72–77.
68. [68] Matthew, T., Zhou, W., Rupprecht, J., Lim, L., Thomas-Hall, S.R., Doebbe, A., Kruse, O., Hankamer, B., Marx, U.C., Smith, S.M., Schenk, P.M., The metabolome of Chlamydomonas reinhardtii following induction of anaerobic H2 production by sulfur depletion. J. Biol. Chem. 284 (2009), 23415–23425.
69. [69] Reitan, K.I., Rainuzzo, J.R., Olsen, Y., Effect of nutrient limitation on fatty acid and lipid content of marine microalgae. J. Phycol. 30 (1994), 972–979.
70. [70] Abida, H., Dolch, L.J., Mei, C., Villanova, V., Conte, M., Block, M.A., Finazzi, G., Bastien, O., Tirichine, L., Bowler, C., Rebeille, F., Petroutsos, D., Jouhet, J., Marechal, E., Membrane glycerolipid remodeling triggered by nitrogen and phosphorus starvation in Phaeodactylum tricornutum. Plant Physiol., 2014.
71. [71] Khozin-Goldberg, I., Cohen, Z., The effect of phosphate starvation on the lipid and fatty acid composition of the fresh water eustigmatophyte Monodus subterraneus. Phytochemistry 67 (2006), 696–701.
72. [72] Urzica, E.I., Vieler, A., Hong-Hermesdorf, A., Page, M.D., Casero, D., Gallaher, S.D., Kropat, J., Pellegrini, M., Benning, C., Merchant, S.S., Remodeling of membrane lipids in iron-starved Chlamydomonas. J. Biol. Chem. 288 (2013), 30246–30258.
73. [73] Kropat, J., Hong-Hermesdorf, A., Casero, D., Ent, P., Castruita, M., Pellegrini, M., Merchant, S.S., Malasarn, D., A revised mineral nutrient supplement increases biomass and growth rate in Chlamydomonas reinhardtii. Plant J. Cell Mol. Biol. 66 (2011), 770–780.
74. [74] Kim, S., Kim, H., Ko, D., Yamaoka, Y., Otsuru, M., Kawai-Yamada, M., Ishikawa, T., Oh, H.M., Nishida, I., Li-Beisson, Y., Lee, Y., Rapid induction of lipid droplets in Chlamydomonas reinhardtii and Chlorella vulgaris by Brefeldin A. PLoS ONE, 8, 2013, e81978.
75. [75] Napolitano, G.E., The relationship of lipids with light and chlorophyll measurement in freshwater algae and periphyton. J. Phycol. 30 (1994), 943–950.
76. [76] Brown, M.R., Dunstan, G.A., Norwood, S.J., Miller, K.A., Effects of harvest stage and light on the biochemical composition of the diatom Thalassiosira pseudonana. J. Phycol. 32 (1996), 64–73.
77. [77] Khotimchenko, S.V., Yakovleva, I.M., Lipid composition of the red alga Tichocarpus crinitus exposed to different levels of photon irradiance. Phytochemistry 66 (2005), 73–79.
78. [78] Hemschemeier, A., Casero, D., Liu, B., Benning, C., Pellegrini, M., Happe, T., Merchant, S.S., Copper response regulator 1-dependent and -independent responses of the Chlamydomonas reinhardtii transcriptome to dark anoxia. Plant Cell 25 (2013), 3186–3211.
79. [79] Hemme, D., Veyel, D., Muhlhaus, T., Sommer, F., Juppner, J., Unger, A.K., Sandmann, M., Fehrle, I., Schonfelder, S., Steup, M., Geimer, S., Kopka, J., Giavalisco, P., Schroda, M., Systems-wide analysis of acclimation responses to long-term heat stress and recovery in the photosynthetic model organism Chlamydomonas reinhardtii. Plant Cell 26 (2014), 4270–4297.
80. [80] Yao, S., Brandt, A., Egsgaard, H., Gjermansen, C., Neutral lipid accumulation at elevated temperature in conditional mutants of two microalgae species. Plant Physiol. Biochem. 61 (2012), 71–79.
81. [81] Aaronson, S., Effect of incubation temperature on the macromolecular and lipid content of the phytoflagellate Ochromonas danica. J. Phycol. 9 (1973), 111–113.
82. [82] Boussiba, S., Vonshak, A., Cohen, Z., Avissar, Y., Richmond, A., Lipid and biomass production by the halotolerant microalga Nanochloropsis salina. Biomass 12 (1987), 37–47.
83. [83] Takagi, M., Karseno, T., Yoshida, Effect of salt concentration on intracellular accumulation of lipids and triacylglyceride in marine microalgae Dunaliella cells. J. Biosci. Bioeng. 101 (2006), 223–226.
84. [84] Mus, F., Toussaint, J.P., Cooksey, K.E., Fields, M.W., Gerlach, R., Peyton, B.M., Carlson, R.P., Physiological and molecular analysis of carbon source supplementation and pH stress-induced lipid accumulation in the marine diatom Phaeodactylum tricornutum. Appl. Microbiol. Biotechnol. 97 (2013), 3625–3642.
85. [85] Shiratake, T., Sato, A., Minoda, A., Tsuzuki, M., Sato, N., Air-drying of cells, the novel conditions for stimulated synthesis of triacylglycerol in a green alga, Chlorella kessleri. PLoS ONE, 8, 2013, e79630.
86. [86] Ramanan, R., Kim, B.H., Cho, D.H., Ko, S.R., Oh, H.M., Kim, H.S., Lipid droplet synthesis is limited by acetate availability in starchless mutant of Chlamydomonas reinhardtii. FEBS Lett. 587 (2013), 370–377.
87. [87] Wu, S., Huang, A., Zhang, B., Huan, L., Zhao, P., Lin, A., Wang, G., Enzyme activity highlights the importance of the oxidative pentose phosphate pathway in lipid accumulation and growth of Phaeodactylum tricornutum under CO2 concentration. Biotechnol. Biofuels, 8, 2015, 78.
88. [88] Alipanah, L., Rohloff, J., Winge, P., Bones, A.M., Brembu, T., Whole-cell response to nitrogen deprivation in the diatom Phaeodactylum tricornutum. J. Exp. Bot. 66 (2015), 6281–6296.
89. [89] Ge, F., Huang, W., Chen, Z., Zhang, C., Xiong, Q., Bowler, C., Yang, J., Xu, J., Hu, H., Methylcrotonyl-CoA carboxylase regulates triacylglycerol accumulation in the model diatom Phaeodactylum tricornutum. Plant Cell 26 (2014), 1681–1697.
90. [90] Iwai, M., Ikeda, K., Shimojima, M., Ohta, H., Enhancement of extraplastidic oil synthesis in Chlamydomonas reinhardtii using a type-2 diacylglycerol acyltransferase with a phosphorus starvation-inducible promoter. Plant Biotechnol. J. 12 (2014), 808–819.
91. [91] Fan, J., Yan, C., Andre, C., Shanklin, J., Schwender, J., Xu, C., Oil accumulation is controlled by carbon precursor supply for fatty acid synthesis in Chlamydomonas reinhardtii. Plant Cell Physiol. 53 (2012), 1380–1390.
92. [92] Li, Y., Han, D., Hu, G., Dauvillee, D., Sommerfeld, M., Ball, S., Hu, Q., Chlamydomonas starchless mutant defective in ADP-glucose pyrophosphorylase hyper-accumulates triacylglycerol. Metab. Eng. 12 (2010), 387–391.
93. [93] Wang, Z.T., Ullrich, N., Joo, S., Waffenschmidt, S., Goodenough, U., Algal lipid bodies: stress induction, purification, and biochemical characterization in wild-type and starchless Chlamydomonas reinhardtii. Eukaryot. Cell 8 (2009), 1856–1868.
94. [94] Work, V.H., Radakovits, R., Jinkerson, R.E., Meuser, J.E., Elliott, L.G., Vinyard, D.J., Laurens, L.M., Dismukes, G.C., Posewitz, M.C., Increased lipid accumulation in the Chlamydomonas reinhardtii sta7-10 starchless isoamylase mutant and increased carbohydrate synthesis in complemented strains. Eukaryot. Cell 9 (2010), 1251–1261.
95. [95] Rabbani, S., Beyer, P., Lintig, J., Hugueney, P., Kleinig, H., Induced beta-carotene synthesis driven by triacylglycerol deposition in the unicellular alga Dunaliella bardawil. Plant Physiol. 116 (1998), 1239–1248.
96. [96] Zhekisheva, M., Boussiba, S., Khozin-Goldberg, I., Zarka, A., Cohen, Z., Accumulation of oleic acid in Haematococcus pluvialis (Chlorophyceae) under nitrogen starvation or high light is correlated with that of astaxanthin esters. J. Phycol. 38 (2002), 325–331.
97. [97] Monnier, A., Liverani, S., Bouvet, R., Jesson, B., Smith, J.Q., Mosser, J., Corellou, F., Bouget, F.Y., Orchestrated transcription of biological processes in the marine picoeukaryote Ostreococcus exposed to light/dark cycles. BMC Genomics, 11, 2010, 192.
98. [98] Panchy, N., Wu, G., Newton, L., Tsai, C.H., Chen, J., Benning, C., Farre, E.M., Shiu, S.H., Prevalence, Evolution, and cis-regulation of Diel Transcription in Chlamydomonas reinhardtii, G3 (Bethesda). 4, 2014, 2461–2471.
99. [99] Poliner, E., Panchy, N., Newton, L., Wu, G., Lapinsky, A., Bullard, B., Zienkiewicz, A., Benning, C., Shiu, S.H., Farre, E.M., Transcriptional coordination of physiological responses in Nannochloropsis oceanica CCMP1779 under light/dark cycles. Plant J. Cell Mol. Biol. 83 (2015), 1097–1113.
100. [100] Sukenik, A., Carmeli, Y., Lipid synthesis and fatty acid composition in Nannochloropsis sp. (Eustigmatophyceae) grown in a light–dark cycle 1. J. Phycol. 26 (1990), 463–469.
101. [101] Fábregas, J., Maseda, A., Domínguez, A., Ferreira, M., Otero, A., Changes in the cell composition of the marine microalga, Nannochloropsis gaditana, during a light:dark cycle. Biotechnol. Lett. 24 (2002), 1699–1703.
102. [102] Focks, N., Benning, C., wrinkled1: a novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism. Plant Physiol. 118 (1998), 91–101.
103. [103] Cernac, A., Benning, C., WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J. 40 (2004), 575–585.
104. [104] Masaki, T., Mitsui, N., Tsukagoshi, H., Nishii, T., Morikami, A., Nakamura, K., Activator of Spomin::LUC1/WRINKLED1 of Arabidopsis thaliana transactivates sugar-inducible promoters. Plant Cell Physiol. 46 (2005), 547–556.
105. [105] Ruuska, S.A., Girke, T., Benning, C., Ohlrogge, J.B., Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell 14 (2002), 1191–1206.
106. [106] Marchive, C., Nikovics, K., A. To, Lepiniec, L., Baud, S., Transcriptional regulation of fatty acid production in higher plants: molecular bases and biotechnological outcomes. Eur. J. Lipid Sci. Technol. 116 (2014), 1332–1343.
107. [107] Baud, S., Wuilleme, S., A. To, Rochat, C., Lepiniec, L., Role of WRINKLED1 in the transcriptional regulation of glycolytic and fatty acid biosynthetic genes in Arabidopsis. Plant J. 60 (2009), 933–947.
108. [108] Maeo, K., Tokuda, T., Ayame, A., Mitsui, N., Kawai, T., Tsukagoshi, H., Ishiguro, S., Nakamura, K., An AP2-type transcription factor, WRINKLED1, of Arabidopsis thaliana binds to the AW-box sequence conserved among proximal upstream regions of genes involved in fatty acid synthesis. Plant J. 60 (2009), 476–487.
109. [109] Vanhercke, T., El Tahchy, A., Shrestha, P., Zhou, X.R., Singh, S.P., Petrie, J.R., Synergistic effect of WRI1 and DGAT1 coexpression on triacylglycerol biosynthesis in plants. FEBS Lett. 587 (2013), 364–369.
110. [110] Sanjaya, T.P., Durrett, S.E., Weise, C., Benning, Increasing the energy density of vegetative tissues by diverting carbon from starch to oil biosynthesis in transgenic Arabidopsis. Plant Biotechnol. J. 9 (2011), 874–883.
111. [111] Ma, W., Kong, Q., Grix, M., Mantyla, J.J., Yang, Y., Benning, C., Ohlrogge, J.B., Deletion of a C-terminal intrinsically disordered region of WRINKLED1 affects its stability and enhances oil accumulation in Arabidopsis. Plant J. 83 (2015), 864–874.
112. [112] Baud, S., Mendoza, M.S., A. To, Harscoet, E., Lepiniec, L., Dubreucq, B., WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis. Plant J. Cell Mol. Biol. 50 (2007), 825–838.
113. [113] Chapman, K.D., Dyer, J.M., Mullen, R.T., Biogenesis and functions of lipid droplets in plants: thematic review series: lipid droplet synthesis and metabolism: from yeast to man. J. Lipid Res. 53 (2012), 215–226.
114. [114] Crowe, A.J., Abenes, M., Plant, A., Moloney, M.M., The seed-specific transactivator, ABI3, induces oleosin gene expression. Plant Sci. Int. J. Exp. Plant Biol. 151 (2000), 171–181.
115. [115] El-Hafid, L., Pham, A.T., Zuily-fodil, Y., da Silva, J.V., Enzymatic breakdown of polar lipids in cotton leaves under water stress: I. Degradation of monogalactosyl-diacylglycerol. Plant Physiol. Biochem. 27 (1989), 495–502.
116. [116] Navari-Izzo, F., Rascio, N., Plant response to water-deficit conditions. Pessarakli, M., (eds.) Handbook of Plant and Crop Stress, 1999, Dekker, 217–231 (Place Published).
117. [117] Sakaki, T., Ohnishi, J., Kondo, N., Yamada, M., Polar and neutral lipid changes in spinach leaves with ozone fumigation: triacylglycerol synthesis from polar lipids. Plant Cell Physiol. 26 (1985), 253–262.
118. [118] Moellering, E.R., Muthan, B., Benning, C., Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330 (2010), 226–228.
119. [119] Yang, Y., Yu, X., Song, L., An, C., ABI4 activates DGAT1 expression in Arabidopsis seedlings during nitrogen deficiency. Plant Physiol. 156 (2011), 873–883.
120. [120] Moellering, E.R., Benning, C., Galactoglycerolipid metabolism under stress: a time for remodeling. Trends Plant Sci. 16 (2011), 98–107.
121. [121] Roston, R.L., Wang, K., Kuhn, L.A., Benning, C., Structural determinants allowing transferase activity in SENSITIVE TO FREEZING 2, classified as a family I glycosyl hydrolase. J. Biol. Chem. 289 (2014), 26089–26106.
122. [122] Sakaki, T., Saito, K., Kawaguchi, A., Kondo, N., Yamada, M., Conversion of monogalactosyldiacylglycerols to triacylglycerols in ozone-fumigated spinach leaves. Plant Physiol. 94 (1990), 766–772.
123. [123] Gasulla, F., Vom Dorp, K., Dombrink, I., Zahringer, U., Gisch, N., Dormann, P., Bartels, D., The role of lipid metabolism in the acquisition of desiccation tolerance in Craterostigma plantagineum: a comparative approach. Plant J. Cell Mol. Biol. 75 (2013), 726–741.
124. [124] A. To, Joubes, J., Barthole, G., Lecureuil, A., Scagnelli, A., Jasinski, S., Lepiniec, L., Baud, S., WRINKLED transcription factors orchestrate tissue-specific regulation of fatty acid biosynthesis in Arabidopsis. Plant Cell 24 (2012), 5007–5023.
125. [125] Gidda, S.K., Watt, S., Collins-Silva, J., Kilaru, A., Arondel, V., Yurchenko, O., Horn, P.J., James, C.N., Shintani, D., Ohlrogge, J.B., Chapman, K.D., Mullen, R.T., Dyer, J.M., Lipid droplet-associated proteins (LDAPs) are involved in the compartmentalization of lipophilic compounds in plant cells. Plant Signal. Behav., 8, 2013, e27141.
126. [126] Gonzalez-Ballester, D., Pootakham, W., Mus, F., Yang, W., Catalanotti, C., Magneschi, L., de Montaigu, A., Higuera, J.J., Prior, M., Galvan, A., Fernandez, E., Grossman, A.R., Reverse genetics in Chlamydomonas: a platform for isolating insertional mutants. Plant Methods, 7, 2011, 24.
127. [127] Hu, J., Wang, D., Li, J., Jing, G., Ning, K., Xu, J., Genome-wide identification of transcription factors and transcription-factor binding sites in oleaginous microalgae Nannochloropsis. Sci. Rep., 4, 2014, 5454.
128. [128] Murphy, D.J., Structure, function and biogenesis of storage lipid bodies and oleosins in plants. Prog. Lipid Res. 32 (1993), 247–280.
129. [129] Murphy, S., Martin, S., Parton, R.G., Lipid droplet-organelle interactions; sharing the fats. Biochim. Biophys. Acta 1791 (2009), 441–447.
130. [130] Nguyen, H.M., Baudet, M., Cuine, S., Adriano, J.M., Barthe, D., Billon, E., Bruley, C., Beisson, F., Peltier, G., Ferro, M., Li-Beisson, Y., Proteomic profiling of oil bodies isolated from the unicellular green microalga Chlamydomonas reinhardtii: with focus on proteins involved in lipid metabolism. Proteomics 11 (2011), 4266–4273.
131. [131] Vieler, A., Brubaker, S.B., Vick, B., Benning, C., A lipid droplet protein of Nannochloropsis with functions partially analogous to plant oleosins. Plant Physiol. 158 (2012), 1562–1569.
132. [132] Moellering, E.R., Benning, C., RNA interference silencing of a major lipid droplet protein affects lipid droplet size in Chlamydomonas reinhardtii. Eukaryotic Cell 9 (2010), 97–106.
133. [133] Peled, E., Leu, S., Zarka, A., Weiss, M., Pick, U., Khozin-Goldberg, I., Boussiba, S., Isolation of a novel oil globule protein from the green alga Haematococcus pluvialis (Chlorophyceae). Lipids 46 (2011), 851–861.
134. [134] Davidi, L., Katz, A., Pick, U., Characterization of major lipid droplet proteins from Dunaliella. Planta 236 (2012), 19–33.
135. [135] Tsai, C.H., Zienkiewicz, K., Amstutz, C.L., Brink, B.G., Warakanont, J., Roston, R., Benning, C., Dynamics of protein and polar lipid recruitment during lipid droplet assembly in Chlamydomonas reinhardtii. Plant J. Cell Mol. Biol. 83 (2015), 650–660.
136. [136] Davidi, L., Shimoni, E., Khozin-Goldberg, I., Zamir, A., Pick, U., Origin of beta-carotene-rich plastoglobuli in Dunaliella bardawil. Plant Physiol. 164 (2014), 2139–2156.
137. [137] Davidi, L., Levin, Y., Ben-Dor, S., Pick, U., Proteome analysis of cytoplasmatic and plastidic beta-carotene lipid droplets in Dunaliella bardawil. Plant Physiol. 167 (2015), 60–79.
138. [138] Goodson, C., Roth, R., Wang, Z.T., Goodenough, U., Structural correlates of cytoplasmic and chloroplast lipid body synthesis in Chlamydomonas reinhardtii and stimulation of lipid body production with acetate boost. Eukaryotic Cell 10 (2011), 1592–1606.
139. [139] Valcourt, J.R., Lemons, J.M., Haley, E.M., Kojima, M., Demuren, O.O., Coller, H.A., Staying alive: metabolic adaptations to quiescence. Cell cycle (Georgetown, Tex.) 11 (2012), 1680–1696.
140. [140] Barka, F., Angstenberger, M., Ahrendt, T., Lorenzen, W., Bode, H.B., Buchel, C., Identification of a triacylglycerol lipase in the diatom Phaeodactylum tricornutum. Biochim. Biophys. Acta, 2015.
141. [141] Derelle, E., Ferraz, C., Rombauts, S., Rouzé, P., Worden, A.Z., Robbens, S., Partensky, F., Degroeve, S., Echeynié, S., Cooke, R., Saeys, Y., Wuyts, J., Jabbari, K., Bowler, C., Panaud, O., Piégu, B., Ball, S.G., Ral, J.P., Bouget Fç, Y., Piganeau, G., De Baets, B., Picard, A., Delseny, M., Demaille, J., Van de Peer, Y., Moreau, H., Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 11647–11652.
142. [142] Li, X., Benning, C., Kuo, M.H., Rapid triacylglycerol turnover in Chlamydomonas reinhardtii requires a lipase with broad substrate specificity. Eukaryot. Cell 11 (2012), 1451–1462.