Proteomic analysis of Chlorella vulgaris: Potential targets for enhanced lipid accumulation

Journal of Proteomics

Volumn 93, Issue , 2013, Pages 245-253

  Guarnieri, Michael T ^a   Nag, Ambarish ^a   Yang, Shihui ^a   Pienkos, Philip T ^a  

^a NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

Author keywords

Biofuels; Cell cycle; Lipid; Metabolic engineering; Microalgae; Proteomics

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; BIOFUEL; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; NITROGEN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TRANSCRIPTION FACTOR;

ARTICLE; CELL CYCLE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CHLORELLA VULGARIS; GENE PRODUCT; GENE TARGETING; GENETIC ENGINEERING; INTRACELLULAR SIGNALING; LIPID STORAGE; LIPOGENESIS; METABOLIC ENGINEERING; MICROALGA; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEOMICS; RNA TRANSLATION; TRANSCRIPTION REGULATION;

ALGAE; CHLORELLA VULGARIS;

BIOFUELS; CELL CYCLE; LIPID; METABOLIC ENGINEERING; MICROALGAE; PROTEOMICS;

ALGAL PROTEINS; CELL CYCLE PROTEINS; CHLORELLA VULGARIS; FATTY ACIDS; GENE EXPRESSION REGULATION, PLANT; LIPIDS; METABOLIC ENGINEERING; MICROALGAE; NADP; NITROGEN; PROTEOME; PROTEOMICS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTOME; TRIGLYCERIDES;

EID: 84888064893     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.05.025     Document Type: Article

References (43)

1. Pienkos P.T., Darzins A. The promise and challenges of microalgal-derived biofuels. Biofuels Bioprod Bioref 2009, 3:431-440.
2. Miller R., Wu G., Deshpande R.R., Vieler A., Gärtner K., Li X., et al. Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol 2010, 154(4):1737-1752.
3. Rismani-Yazdi H., Haznedaroglu B.Z., Bibby K., Peccia J. Transcriptome sequencing and annotation of the microalgae Dunaliella tertiolecta: pathway description and gene discovery for production of next-generation biofuels. BMC Genomics 2011, 12:148.
4. Hockin N.L., Mock T., Mulholland F., Kopriva S., Malin G. The response of diatom central carbon metabolism to nitrogen starvation is different from that of green algae and higher plants. Plant Physiol 2012, 158(1):299-312.
5. Boyle N.R., Page M.D., Liu B., Blaby I.K., Casero D., Kropat J., et al. Three acyltransferases and nitrogen-responsive regulator are implicated in nitrogen starvation-induced triacylglycerol accumulation in Chlamydomonas. J Biol Chem 2012, 287(19):15811-15825.
6. Recht L., Zarka A., Boussiba S. Patterns of carbohydrate and fatty acid changes under nitrogen starvation in the microalgae Haematococcus pluvialis and Nannochloropsis sp. Appl Microbiol Biotechnol 2012, 94(6):1495-1503.
7. Cakmak T., Angun P., Ozkan A.D., Cakmak Z., Olmez T.T., Tekinay T. Nitrogen and sulfur deprivation differentiate lipid accumulation targets of Chlamydomonas reinhardtii. Bioengineered 2012, 3(6):343-346.
8. Msanne J., Xu D., Konda A.R., Casas-Mollano J.A., Awada T., Cahoon E.B., et al. Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonas reinhardtii and Coccomyxa sp C-169. Phytochemistry 2012, 75:50-59.
9. Li Y.J., Fei X.W., Deng X.D. Novel molecular insights into nitrogen starvation-induced triacylglycerols accumulation revealed by differential gene expression analysis in green algae Micractinium pusillum. Biomass Bioenergy 2012, 42:199-211.
10. Guarnieri M.T., Nag A., Smolinski S.L., Darzins A., Seibert M., Pienkos P.T. Examination of triacylglycerol biosynthetic pathways via de novo transcriptomic and proteomic analyses in an unsequenced microalga. PLoS One 2011, 6(10):e25851.
11. Stephenson A.L.D.J., Howe C.J., Scott S.A., Smith A.G. Influence of nitrogen-limitation regime on the production by Chlorella vulgaris of lipids for biodiesel feedstocks. Biofuels 2010, 1:47-58.
12. Radakovits R., Jinkerson R.E., Fuerstenberg S.I., Tae H., Settlage R.E., Boore J.L., et al. Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Nat Commun 2012, 3:686.
13. Kirk M.M., Kirk D.L. Translational regulation of protein synthesis, in response to light, at a critical stage of Volvox development. Cell 1985, 41(2):419-428.
14. Gillham N.W., Boynton J.E., Hauser C.R. Translational regulation of gene expression in chloroplasts and mitochondria. Annu Rev Genet 1994, 28:71-93.
15. Mayfield S.P., Yohn C.B., Cohen A., Danon A. Regulation of chloroplast gene-expression. Annu Rev Plant Physiol 1995, 46:147-166.
16. Le Bihan T., Martin S.F., Chirnside E.S., van Ooijen G., Barrios-Llerena M.E., O'Neill J.S., et al. Shotgun proteomic analysis of the unicellular alga Ostreococcus tauri. J Proteomics 2011, 74(10):2060-2070.
17. Laurens L.M., Quinn M., Van Wychen S., Templeton D.W., Wolfrum E.J. Accurate and reliable quantification of total microalgal fuel potential as fatty acid methyl esters by in situ transesterification. Anal Bioanal Chem 2012, 403(1):167-178.
18. Perkins D.N., Pappin D.J., Creasy D.M., Cottrell J.S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20(18):3551-3567.
19. Zybailov B., Mosley A.L., Sardiu M.E., Coleman M.K., Florens L., Washburn M.P. Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J Proteome Res 2006, 5(9):2339-2347.
20. Tong W., Cao X., Harris S., Sun H., Fang H., Fuscoe J., et al. ArrayTrack-supporting toxicogenomic research at the U.S. Food and Drug Administration National Center for Toxicological Research. Environ Health Perspect 2003, 11(15):1819-1826.
21. Oliveros J.C. VENNY. An interactive tool for comparing Venn Diagrams http://bioinfogp.cnb.csic.es/tools/venny/index.html.
22. Guckert J.B., Cooksey K.E. Triglyceride accumulation and fatty-acid profile changes in Chlorella (Chlorophyta) during high pH-induced cell-cycle inhibition. J Phycol 1990, 26(1):72-79.
23. LaRonde-LeBlanc N., Wlodawer A. A family portrait of the RIO kinases. J Biol Chem 2005, 280(45):37297-37300.
24. LaRonde-LeBlanc N., Wlodawer A. The RIO kinases: an atypical protein kinase family required for ribosome biogenesis and cell cycle progression. Biochim Biophys Acta 2005, 1754(1-2):14-24.
25. Yamashita Y.M., Nakaseko Y., Samejima I., Kumada K., Yamada H., Michaelson D., et al. 20S cyclosome complex formation and proteolytic activity inhibited by the cAMP/PKA pathway. Nature 1996, 384(6606):276-279.
26. Goto K., Johnson C.H. Is the cell division cycle gated by a circadian clock? The case of Chlamydomonas reinhardtii. J Cell Biol 1995, 129(4):1061-1069.
27. Moulager M., Monnier A., Jesson B., Bouvet R., Mosser J., Schwartz C., et al. Light-dependent regulation of cell division in Ostreococcus: evidence for a major transcriptional input. Plant Physiol 2007, 144(3):1360-1369.
28. Chen Y.F., Etheridge N., Schaller G.E. Ethylene signal transduction. Ann Bot 2005, 95(6):901-915.
29. Ohlrogge J., Browse J. Lipid biosynthesis. Plant Cell 1995, 7(7):957-970.
30. Hardie D.G., Pan D.A. Regulation of fatty acid synthesis and oxidation by the AMP-activated protein kinase. Biochem Soc Trans 2002, 30(Pt 6):1064-1070.
31. Courchesne N.M., Parisien A., Wang B., Lan C.Q. Enhancement of lipid production using biochemical, genetic and transcription factor engineering approaches. J Biotechnol 2009, 141(1-2):31-41.
32. Dunahay T.G., Jarvis E.E., Dais S.S., Roessler P.G. Manipulation of microalgal lipid production using genetic engineering. Appl Biochem Biotechnol 1996, 57-8:223-231.
33. Sheehan J., Dunahay T., Bennemann J., Roessler P. DOE Aquatic Species Program Closeout Report http://www.nrel.gov/docs/legosti/fy98/24190.pdf.
34. Jako C., Kumar A., Wei Y., Zou J., Barton D.L., Giblin E.M., et al. Seed-specific over-expression of an Arabidopsis cDNA encoding a diacylglycerol acyltransferase enhances seed oil content and seed weight. Plant Physiol 2001, 126(2):861-874.
35. Bouvier-Nave P., Benveniste P., Oelkers P., Sturley S.L., Schaller H. Expression in yeast and tobacco of plant cDNAs encoding acyl CoA:diacylglycerol acyltransferase. Eur J Biochem 2000, 267(1):85-96.
36. Zhang Y., Adams I.P., Ratledge C. Malic enzyme: the controlling activity for lipid production? Overexpression of malic enzyme in Mucor circinelloides leads to a 2.5-fold increase in lipid accumulation. Microbiology 2007, 153(Pt 7):2013-2025.
37. Yohn C, Mendez M, Behnke C, Brand A. Stress-induced lipid trigger. Patent No. WO/2011 97261(11); 2011.
38. Kerk D., Bulgrien J., Smith D.W., Gribskov M. Arabidopsis proteins containing similarity to the universal stress protein domain of bacteria. Plant Physiol 2003, 131(3):1209-1219.
39. Gao Z.P., Yu Q.B., Zhao T.T., Ma Q., Chen G.X., Yang Z.N. A functional component of the transcriptionally active chromosome complex, Arabidopsis pTAC14, interacts with pTAC12/HEMERA and regulates plastid gene expression. Plant Physiol 2011, 157(4):1733-1745.
40. Kamisaka Y., Tomita N., Kimura K., Kainou K., Uemura H. DGA1 (diacylglycerol acyltransferase gene) overexpression and leucine biosynthesis significantly increase lipid accumulation in the Deltasnf2 disruptant of Saccharomyces cerevisiae. Biochem J 2007, 408(1):61-68.
41. Allen SM, Aukerman M, Loussaert D, Luck S, Sakai H, Simmons CR, et al. Plants having altered agronomic characteristics under nitrogen limiting conditions and related constructs and methods involving gene encoding SNF2 domain-containing polypeptides. US Patent: 2012/0023617 A1; 2010.
42. González-Ballester D., Casero D., Cokus S., Pellegrini M., Merchant S.S., Grossman A.R. RNA-seq analysis of sulfur-deprived Chlamydomonas cells reveals aspects of acclimation critical for cell survival. Plant Cell Online 2010, 22(6):2058-2084.
43. Lee D.Y., Park J.J., Barupal D.K., Fiehn O. System response of metabolic networks in Chlamydomonas reinhardtii to total available ammonium. Mol Cell Proteomics 2012, 11(10):973-988.