Regulation of the cholesterol biosynthetic pathway and its integration with fatty acid biosynthesis in the oleaginous microalga Nannochloropsis oceanica

Biotechnology for Biofuels

Volumn 7, Issue 1, 2014, Pages

  Lu, Yandu ^a   Zhou, Wenxu ^b   Wei, Li ^a   Li, Jing ^b   Jia, Jing ^a   Li, Fei ^a   Smith, Steven M ^b   Xu, Jian ^a  

^a QINGDAO INSTITUTE OF BIOENERGY AND BIOPROCESS TECHNOLOGY   (China)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Cholesterol biosynthetic pathway; Fatty acid biosynthesis; Feedback regulation; Nannochloropsis

Indexed keywords

ALGAE; BIOCHEMISTRY; BIOSYNTHESIS; CELL PROLIFERATION; CHOLESTEROL; FATTY ACIDS; GENETIC ENGINEERING; LIPIDS; MICROORGANISMS;

BIOSYNTHETIC PATHWAY; CHEMICAL BIOLOGY; EUKARYOTIC CELLS; FATTY ACID BIOSYNTHESIS; FEEDBACK REGULATION; NANNOCHLOROPSIS; STEROL BIOSYNTHESIS; TEMPORAL TRACKING;

ALCOHOLS;

FATTY ACID; HOMEOSTASIS; INHIBITOR; MICROALGA; PHOTOSYNTHESIS; STEROL;

EMBRYOPHYTA; EUKARYOTA; MAMMALIA; NANNOCHLOROPSIS; NANNOCHLOROPSIS OCEANICA;

EID: 84902539648     PISSN: 17546834     EISSN: None     Source Type: Journal    
DOI: 10.1186/1754-6834-7-81     Document Type: Article

References (68)

1. Biosynthesis of cholesterol and other sterols. Nes WD, Chem Rev 2011 111 6423 6451 10.1021/cr200021m 21902244
2. Allelic mutant series reveal distinct functions for Arabidopsis cycloartenol synthase 1 in cell viability and plastid biogenesis. Babiychuk E, Bouvier-Navé P, Compagnon V, Suzuki M, Muranaka T, Van Montagu M, Kushnir S, Schaller H, Proc Natl Acad Sci 2008 105 3163 3168 10.1073/pnas.0712190105 18287026
3. Postembryonic seedling lethality in the sterol-deficient Arabidopsis cyp51A2 mutant is partially mediated by the composite action of ethylene and reactive oxygen species. Kim HB, Lee H, Oh CJ, Lee H-Y, Eum HL, Kim H-S, Hong Y-P, Lee Y, Choe S, An CS, Choi S-B, Plant Physiol 2010 152 192 205 10.1104/pp.109.149088 19915013
4. Smagghe G, Ecdysone, Structures and Functions New York: Springer 2009
5. Epigenetic control of vasopressin expression is maintained by steroid hormones in the adult male rat brain. Auger CJ, Coss D, Auger AP, Forbes-Lorman RM, Proc Natl Acad Sci 2011 108 4242 4247 10.1073/pnas.1100314108 21368111
6. Plant hormones are versatile chemical regulators of plant growth. Santner A, Calderon-Villalobos LIA, Estelle M, Nat Chem Biol 2009 5 301 307 10.1038/nchembio.165 19377456
7. Evolutionarily conserved Δ25(27)-olefin ergosterol biosynthesis pathway in the alga Chlamydomonas reinhardtii. Miller MB, Haubrich BA, Wang Q, Snell WJ, Nes WD, J Lipid Res 2012 53 1636 1645 10.1194/jlr.M027482 22591742
8. Deoxyxylulose phosphate pathway to terpenoids. Eisenreich W, Rohdich F, Bacher A, Trends Plant Sci 2001 6 78 84 11173292
9. A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Vickers CE, Gershenzon J, Lerdau MT, Loreto F, Nat Chem Biol 2009 5 283 291 10.1038/nchembio.158 19377454
10. Identification of the Arabidopsis dry2/sqe1-5 mutant reveals a central role for sterols in drought tolerance and regulation of reactive oxygen species. Posé D, Castanedo I, Borsani O, Nieto B, Rosado A, Taconnat L, Ferrer A, Dolan L, Valpuesta V, Botella MA, Plant J 2009 59 63 76 10.1111/j.1365-313X. 2009.03849.x 19309460
11. Arabidopsis mutants reveal multiple roles for sterols in plant development. Clouse SD, Plant Cell 2002 14 1995 2000 10.1105/tpc.140930 12215500
12. Sterols regulate development and gene expression in Arabidopsis. He JX, Fujioka S, Li TC, Kang SG, Seto H, Takatsuto S, Yoshida S, Jang JC, Plant Physiol 2003 131 1258 1269 10.1104/pp.014605 12644676
13. Sterol regulation of fatty acid synthase promoter: coordinate feedback regulation of two major lipid pathways. Bennett MK, Lopez JM, Sanchez HB, Osborne TF, J Biol Chem 1995 270 25578 25583 10.1074/jbc.270.43.25578 7592729
14. SREBP in signal transduction: cholesterol metabolism and beyond. Bengoechea-Alonso MT, Ericsson J, Curr Opin Cell Biol 2007 19 215 222 10.1016/j.ceb.2007.02.004 17303406
15. Cholesterol homeostasis: Clipping out a slippery regulator. Osborne TF, Curr Biol 1997 7 172 R174 10.1016/S0960-9822(97)70081-2 9162482
16. SREBPs: transcriptional mediators of lipid homeostasis. Horton J, Goldstein J, Brown M, Cold Spring Harbor Symposia on Quantitative Biology Woodbury, NY: Cold Spring Harbor Laboratory Press 2002 491 498
17. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. Horton JD, J Clin Invest 2002 109 1125 1131 10.1172/JCI0215593 11994399
18. An outlook on microalgal biofuels. Wijffels RH, Barbosa MJ, Science 2010 329 796 799 10.1126/science.1189003 20705853
19. Exploiting diversity and synthetic biology for the production of algal biofuels. Georgianna DR, Mayfield SP, Nature 2012 488 329 335 10.1038/nature11479 22895338
20. Sterols in microorganisms. Volkman J, Appl Microbiol Biotechnol 2003 60 495 506 10.1007/s00253-002-1172-8 12536248
21. Phylogenomics of sterol synthesis: insights into the origin, evolution, and diversity of a key eukaryotic feature. Desmond E, Gribaldo S, Genome Biol Evol 2009 1 364 381 20333205
22. Sterol composition of Phaeodactylum tricornutum as influenced by growth temperature and light spectral quality. Véron B, Billard C, Dauguet JC, Hartmann MA, Lipids 1996 31 989 994 10.1007/BF02522694 8882980
23. Choreography of transcriptomes and lipidomes of Nannochloropsis reveals the mechanisms of oleaginousness in microalgae. Li J, Han D, Wang D, Ning K, Hu Q, Xu J, Plant Cell 2014 http://dx.doi.org/10.1105/tpc.113.121418
24. Nannochloropsis plastid and mitochondrial phylogenomes reveal organelle diversification mechanism and intragenus phylotyping strategy in microalgae. Wei L, Xin Y, Wang DM, Jing XY, Zhou Q, Su XQ, Jia J, Ning K, Chen F, Hu Q, Xu J, BMC Genomics 2013 14 534 doi:10.1186/1471-2164-14-534 10.1186/1471-2164-14-534 23915326
25. Genome, functional gene annotation, and nuclear transformation of the heterokont oleaginous alga Nannochloropsis oceanica CCMP1779. Vieler A, Wu G, Tsai CH, Bullard B, Cornish AJ, Harvey C, Reca IB, Thornburg C, Achawanantakun R, Buehl CJ, et al. Plos Genet 2012 8 1003064 10.1371/journal.pgen.1003064 23166516
26. Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Radakovits R, Jinkerson RE, Fuerstenberg SI, Tae H, Settlage RE, Boore JL, Posewitz MC, Nat Comm 2012 doi:10.1038/ncomms3356
27. Nannochloropsis genomes reveal evolution of microalgal oleaginous traits. Wang D, Ning K, Li J, Hu Q, Xu J, Plos Genet 2014 doi:10.1371/journal.pgen. 1004094
28. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, et al. Nature 2008 451 783 788 10.1038/nature06617 18273011
29. Chemical genetic approaches to plant biology. Blackwell HE, Zhao Y, Plant Physiol 2003 133 448 455 10.1104/pp.103.031138 14555772
30. ChemMine. A compound mining database for chemical genomics. Girke T, Cheng L-C, Raikhel N, Plant Physiol 2005 138 573 577 10.1104/pp.105.062687 15955920
31. Opportunities and challenges in plant chemical biology. Hicks GR, Raikhel NV, Nat Chem Biol 2009 5 268 272 10.1038/nchembio0509-268 19377447
32. Chemical genetics: ligand-based discovery of gene function. Stockwell BR, Nat Rev Genet 2000 1 116 125 10.1038/35038557 11253651
33. Chemical genetics. Walsh DP, Chang Y-T, Chem Rev 2006 106 2476 2530 10.1021/cr0404141 16771457
34. Inhibition of squalene synthase and squalene epoxidase in tobacco cells triggers an up-regulation of 3-hydroxy-3-methylglutaryl coenzyme A reductase. Wentzinger LF, Bach TJ, Hartmann MA, Plant Physiol 2002 130 334 346 10.1104/pp.004655 12226513
35. Cholesterol import fails to prevent catalyst-based inhibition of ergosterol synthesis and cell proliferation of Trypanosoma brucei. Zhou W, Cross GAM, Nes WD, J Lipid Res 2007 48 665 673 17127773
36. Properties and inhibition of the first two enzymes of the non-mevalonate pathway of isoprenoid biosynthesis. Mueller C, Schwender J, Zeidler J, Lichtenthaler H, Biochem Soc Trans 2000 28 792 793 10.1042/BST0280792 11171210
37. Expression, purification, reconstitution and inhibition of Ustilago maydis sterol 14α-demethylase (CYP51; P45014DM). Lamb DC, Kelly DE, Manning NJ, Hollomon DW, Kelly SL, FEMS Microbiol Lett 1998 169 369 373 9868783
38. Manipulation by Tridemorph, a systemic fungicide, of the sterol composition of maize leaves and roots. Bladocha M, Benveniste P, Plant Physiol 1983 71 756 762 10.1104/pp.71.4.756 16662902
39. New aspects on lanosterol 14α-demethylase and cytochrome P450 evolution: lanosterol/cycloartenol diversification and lateral transfer. Režen T, Debeljak N, Kordiš D, Rozman D, J Mol Evol 2004 59 51 58 10.1007/s00239-004-2603-1 15383907
40. Arabidopsis cyp51 mutant shows postembryonic seedling lethality associated with lack of membrane integrity. Kim HB, Schaller H, Goh CH, Kwon M, Choe S, An CS, Durst F, Feldmann KA, Feyereisen R, Plant Physiol 2005 138 2033 2047 10.1104/pp.105.061598 16040657
41. Responses of Nannochloropsis oceanica IMET1 to long-term nitrogen starvation and recovery. Dong H-P, Williams E, Wang D-Z, Xie Z-X, Hsia R-C, Jenck A, Halden R, Li J, Chen F, Place AR, Plant Physiol 2013 162 1110 1126 10.1104/pp.113.214320 23637339
42. Plasma membrane sterols are essential for sensing osmotic changes in the halotolerant alga Dunaliella. Zelazny AM, Shaish A, Pick U, Plant Physiol 1995 109 1395 1403 12228675
43. Sterol and phospholipid changes during alfalfa seed germination. Huang L-S, Grunwald C, Phytochemistry 1988 27 2049 2053 10.1016/0031-9422(88)80095-5
44. MRL1, a conserved pentatricopeptide repeat protein, is required for stabilization of rbcL mRNA in Chlamydomonas and Arabidopsis. Johnson X, Wostrikoff K, Finazzi G, Kuras R, Schwarz C, Bujaldon S, Nickelsen J, Stern DB, Wollman F-A, Vallon O, Plant Cell 2010 22 234 248 10.1105/tpc.109.066266 20097872
45. Cholesterol feedback: from Schoenheimer's bottle to Scap's MELADL. Brown MS, Goldstein JL, J Lipid Res 2009 50 15 S27 18974038
46. Regulation of HMG-CoA reductase in mammals and yeast. Burg JS, Espenshade PJ, Progr Lipid Res 2011 50 403 410 10.1016/j.plipres.2011.07.002
47. Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Worden AZ, Lee J-H, Mock T, Rouzé P, Simmons MP, Aerts AL, Allen AE, Cuvelier ML, Derelle E, Everett MV, et al. Science 2009 324 268 272 10.1126/science.1167222 19359590
48. The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Palenik B, Grimwood J, Aerts A, Rouzé P, Salamov A, Putnam N, Dupont C, Jorgensen R, Derelle E, Rombauts S, et al. Proc Nat Acad Sci 2007 104 7705 7710 10.1073/pnas.0611046104 17460045
49. Cholesterol as an evolutionary response to living with oxygen. Brown AJ, Galea AM, Evolution 2010 64 2179 2183 20394667
50. Sterol methyltransferase 1 controls the level of cholesterol in plants. Diener AC, Li H, Zhou W, Whoriskey WJ, Nes WD, Fink GR, Plant Cell 2000 12 853 870 10.1105/tpc.12.6.853 10852933
51. The sterol methyltransferases SMT1, SMT2, and SMT3 influence Arabidopsis development through nonbrassinosteroid products. Carland F, Fujioka S, Nelson T, Plant Physiol 2010 153 741 756 10.1104/pp.109.152587 20421456
52. Isolation and identification of sterols from subcellular fractions of bean leaves (Phaseolus vulgaris). Brandt RD, Benveniste P, Biochim Biophys Acta (BBA)-Biomembr 1972 282 85 92
53. Ergosterol biosynthesis: a fungal pathway for life on land? Dupont S, Lemetais G, Ferreira T, Cayot P, Gervais P, Beney L, Evolution 2012 66 2961 2968 10.1111/j.1558-5646.2012.01667.x 22946816
54. The ratio of campesterol to sitosterol that modulates growth in Arabidopsis is controlled by STEROL METHYLTRANSFERASE 2;1. Schaeffer A, Bronner R, Benveniste P, Schaller H, Plant J 2001 25 605 615 11319028
55. 2+/calmodulin is critical for brassinosteroid biosynthesis and plant growth. Du L, Poovaiah BW, Nature 2005 437 741 745 10.1038/nature03973 16193053
56. Complete blockage of the mevalonate pathway results in male gametophyte lethality. Suzuki M, Nakagawa S, Kamide Y, Kobayashi K, Ohyama K, Hashinokuchi H, Kiuchi R, Saito K, Muranaka T, Nagata N, J Exp Bot 2009 60 2055 2064 10.1093/jxb/erp073 19363204
57. Comparative profiling of lipid-soluble antioxidants and transcripts reveals two phases of photo-oxidative stress in a xanthophyll-deficient mutant of Chlamydomonas reinhardtii. Ledford HK, Baroli I, Shin JW, Fischer BB, Eggen RIL, Niyogi KK, Mol Genet Genom 2004 272 470 479 10.1007/s00438-004-1078-5
58. Plant sterols and the membrane environment. Hartmann M-A, Trends Plant Sci 1998 3 170 175 10.1016/S1360-1385(98)01233-3
59. Sterol regulation of human fatty acid synthase promoter I requires nuclear factor-Y- and Sp-1-binding sites. Xiong S, Chirala SS, Wakil SJ, Proc Nat Acad Sci 2000 97 3948 3953 10.1073/pnas.040574197 10759542
60. Isolation and characterization of a stress-dependent plastidial Δ12 fatty acid desaturase from the Antarctic microalga Chlorella vulgaris NJ-7. Lu Y, Chi X, Li Z, Yang Q, Li F, Liu S, Gan Q, Qin S, Lipids 2010 45 179 187 10.1007/s11745-009-3381-8 20087673
61. SMART 7: recent updates to the protein domain annotation resource. Letunic I, Doerks T, Bork P, Nucleic Acids Res 2012 40 302 D305 10.1093/nar/gkr931 22053084
62. Multiple sequence alignment with the Clustal series of programs. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD, Nucleic Acids Res 2003 31 3497 3500 10.1093/nar/gkg500 12824352
63. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Talavera G, Castresana J, Syst Biol 2007 56 564 577 10.1080/10635150701472164 17654362
64. ProtTest 3: fast selection of best-fit models of protein evolution. Darriba D, Taboada GL, Doallo R, Posada D, Bioinformatics 2011 27 1164 1165 10.1093/bioinformatics/btr088 21335321
65. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O, Syst Biol 2010 59 307 321 10.1093/sysbio/syq010 20525638
66. Phospholipid:diacylglycerol acyltransferase is a multifunctional enzyme involved in membrane lipid turnover and degradation while synthesizing triacylglycerol in the unicellular green microalga Chlamydomonas reinhardtii. Yoon K, Han D, Li Y, Sommerfeld M, Hu Q, Plant Cell 2012 24 3708 3724 10.1105/tpc.112.100701 23012436
67. A link between sterol biosynthesis, the cell wall, and cellulose in Arabidopsis. Schrick K, Fujioka S, Takatsuto S, Stierhof Y-D, Stransky H, Yoshida S, Jürgens G, Plant J 2004 38 227 243 10.1111/j.1365-313X.2004. 02039.x 15078327
68. Molecular characterization of the CER1 gene of Arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Aarts MG, Keijzer CJ, Stiekema WJ, Pereira A, Plant Cell 1995 7 2115 2127 10.1105/tpc.7.12.2115 8718622