Changes in Transcript Abundance in Chlamydomonas reinhardtii following Nitrogen Deprivation Predict Diversion of Metabolism
Open accessAbstract
Like many microalgae, Chlamydomonas reinhardtii forms lipid droplets rich in triacylglycerols when nutrient deprived. To begin studying the mechanisms underlying this process, nitrogen (N) deprivation was used to induce triacylglycerol accumulation and changes in developmental programs such as gametogenesis. Comparative global analysis of transcripts under induced and noninduced conditions was applied as a first approach to studying molecular changes that promote or accompany triacylglycerol accumulation in cells encountering a new nutrient environment. Towards this goal, high-throughput sequencing technology was employed to generate large numbers of expressed sequence tags of eight biologically independent libraries, four for each condition, N replete and N deprived, allowing a statistically sound comparison of expression levels under the two tested conditions. As expected, N deprivation activated a subset of control genes involved in gametogenesis while down-regulating protein biosynthesis. Genes for components of photosynthesis were also down-regulated, with the exception of the PSBS gene. N deprivation led to a marked redirection of metabolism: the primary carbon source, acetate, was no longer converted to cell building blocks by the glyoxylate cycle and gluconeogenesis but funneled directly into fatty acid biosynthesis. Additional fatty acids may be produced by membrane remodeling, a process that is suggested by the changes observed in transcript abundance of putative lipase genes. Inferences on metabolism based on transcriptional analysis are indirect, but biochemical experiments supported some of these deductions. The data provided here represent a rich source for the exploration of the mechanism of oil accumulation in microalgae.
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Different responses of the TCA cycle in C. reinhardtii and T. pseudonana to nitrogen starvation have been observed, showing that the flux of the TCA cycle may be adaptable.
“Different responses of the TCA cycle in C. reinhardtii and T. pseudonana to nitrogen starvation have been observed (Miller et al., 2010;Hockin et al., 2012), showing that the flux of the TCA cycle may be adaptable.”
From Responses of<i>Nannochloropsis oceanica</i>IMET1 to Long-Term Nitrogen Starvation and Recovery (2013) · cites this paper as Miller et al., 2010
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Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364 · see citing works
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849 · see citing works
Trapnell, C., Williams, B. A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M. J., Salzberg, S. L., Wold, B. J., & Pachter, L. (2010) · Nature Biotechnology · doi:10.1038/nbt.1621 · Cited by 15,556 · see citing works
TopHat: discovering splice junctions with RNA-Seq
Trapnell, C., Pachter, L. S., & Salzberg, S. L. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp120 · Cited by 11,477 · see citing works
DEGseq: an R package for identifying differentially expressed genes from RNA-seq data
Wang, L., Feng, Z., Wang, X., Wang, X., & Zhang, X. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp612 · Cited by 4,553 · see citing works
Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances
Hu, Q., Sommerfeld, M., Jarvis, E., Ghirardi, M., Posewitz, M., Seibert, M., & Darzins, A. (2008) · The Plant Journal · doi:10.1111/j.1365-313x.2008.03492.x · Cited by 3,745 · see citing works
RNA-seq: An assessment of technical reproducibility and comparison with gene expression arrays
Marioni, J. C., Mason, C. E., Mane, S. M., Stephens, M., & Gilad, Y. (2008) · Genome Research · doi:10.1101/gr.079558.108 · Cited by 2,771 · see citing works
The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions
Merchant, S., Prochnik, S., Vallon, O., Harris, E. H., Karpowicz, S. J., Witman, G., Terry, A., Salamov, A., Fritz-Laylin, L., Maréchal-Drouard, L., et al. (2007) · Science · doi:10.1126/science.1143609 · Cited by 2,765 · see citing works
GMAP: A genomic mapping and alignment program for mRNA and EST sequences
Wu, T. D., & Watanabe, C. K. (2005) · Bioinformatics · doi:10.1093/bioinformatics/bti310 · Cited by 2,354 · see citing works
The positive false discovery rate: a Bayesian interpretation and the q-value
Storey, J. D. (2003) · The Annals of Statistics · doi:10.1214/aos/1074290335 · Cited by 2,204 · see citing works
Fat Mobilization in Adipose Tissue Is Promoted by Adipose Triglyceride Lipase
Zimmermann, R., Bogner‐Strauß, J. G., Haemmerle, G., Schoiswohl, G., Birner‐Gruenberger, R., Riederer, M., Lass, A., Neuberger, G., Eisenhaber, F., Hermetter, A., et al. (2004) · Science · doi:10.1126/science.1100747 · Cited by 2,121 · see citing works
An outlook on microalgal biofuels
Wijffels, R. H., & Barbosa, M. J. (2010) · Science · doi:10.1126/science.1189003 · Cited by 1,886 · see citing works
Emanuelsson, O., Nielsen, H., & von HEIJNE, G. (1999) · Protein Science · doi:10.1110/ps.8.5.978 · Cited by 1,790 · see citing works
Bullard, J. H., Purdom, E., Hansen, K. D., & Dudoit, S. (2010) · BMC Bioinformatics · doi:10.1186/1471-2105-11-94 · Cited by 1,680 · see citing works
A pigment-binding protein essential for regulation of photosynthetic light harvesting
Li, X., Björkman, O., Shih, C., Grossman, A. R., Rosenquist, M., Jansson, S., & Niyogi, K. (2000) · Nature · doi:10.1038/35000131 · Cited by 1,540 · see citing works
Self-citationStructure of human pancreatic lipase
Winkler, F. K., D'Arcy, A., & Hunziker, W. H. (1990) · Nature · doi:10.1038/343771a0 · Cited by 1,227 · see citing works
A serine protease triad forms the catalytic centre of a triacylglycerol lipase
Brady, L., Brzozowski, A. M., Derewenda, Z. S., Dodson, E. J., Dodson, G. G., Tolley, S. P., Turkenburg, J. P., Christiansen, L., Huge‐Jensen, B., Nørskov, L., et al. (1990) · Nature · doi:10.1038/343767a0 · Cited by 1,219 · see citing works
PlnTFDB: updated content and new features of the plant transcription factor database
Pérez‐Rodríguez, P., Riaño‐Pachón, D. M., Corrêa, L. G. G., et al. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp805 · Cited by 734 · see citing works
Molecular Mechanisms Regulating Hormone-Sensitive Lipase and Lipolysis
Holm, C., Østerlund, T., Laurell, H., & Contreras, J. A. (2000) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.20.1.365 · Cited by 565 · see citing works
Wang, Z. T., Ullrich, N., Joo, S., Waffenschmidt, S., & Goodenough, U. W. (2009) · Eukaryotic Cell · doi:10.1128/ec.00272-09 · Cited by 542 · see citing works
Transcript length bias in RNA-seq data confounds systems biology
Oshlack, A., & Wakefield, M. J. (2009) · Biology Direct · doi:10.1186/1745-6150-4-14 · Cited by 497 · see citing works
Eastmond, P. J. (2006) · The Plant Cell · doi:10.1105/tpc.105.040543 · Cited by 484 · see citing works
Moellering, E. R., & Christoph Benning, A. (2009) · Eukaryotic Cell · doi:10.1128/ec.00203-09 · Cited by 401 · see citing works
Self-citationMustroph, A., Lee, S. C., Oosumi, T., Zanetti, M. E., Yang, H., Ma, K., Yaghoubi-Masihi, A., Fukao, T., & Bailey-Serres, J. N. (2010) · PLANT PHYSIOLOGY · doi:10.1104/pp.109.151845 · Cited by 374 · see citing works
Sampling the Arabidopsis Transcriptome with Massively Parallel Pyrosequencing
Weber, A. P. M., Weber, K. L., Carr, K. M., Wilkerson, C. G., & Ohlrogge, J. B. (2007) · PLANT PHYSIOLOGY · doi:10.1104/pp.107.096677 · Cited by 366 · see citing works
Shockey, J. M., Fulda, M. S., & Browse, J. (2002) · PLANT PHYSIOLOGY · doi:10.1104/pp.003269 · Cited by 326 · see citing works
Obese Yeast: Triglyceride Lipolysis Is Functionally Conserved from Mammals to Yeast
Kurat, C. F., Natter, K., Petschnigg, J., Wolinski, H., Scheuringer, K., Scholz, H., Zimmermann, R., Leber, R., Zechner, R., & Kohlwein, S. D. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m508414200 · Cited by 323 · see citing works
Anaerobic Acclimation in Chlamydomonas reinhardtii
Mus, F., Dubini, A., Seibert, M., Posewitz, M. C., & Grossman, A. R. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m701415200 · Cited by 316 · see citing works
Collier, J. L., & Grossman, A. R. (1992) · Journal of Bacteriology · doi:10.1128/jb.174.14.4718-4726.1992 · Cited by 310 · see citing works
Roles of phosphatidate phosphatase enzymes in lipid metabolism
Carman, G. M., & Han, G. (2006) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2006.10.003 · Cited by 301 · see citing works
Winder, C. L., Dunn, W. B., Schuler, S., et al. (2008) · Analytical Chemistry · doi:10.1021/ac7023409 · Cited by 296 · see citing works
González-Ballester, D., Casero, D., Cokus, S. J., Pellegrini, M. A., Merchant, S., & Grossman, A. R. (2010) · The Plant Cell · doi:10.1105/tpc.109.071167 · Cited by 268 · see citing works
Mawhinney, T. P., Robinett, R. S. R., Atalay, A., & Madson, M. A. (1986) · Journal of Chromatography A · doi:10.1016/s0021-9673(01)90333-4 · Cited by 235 · see citing works
Riekhof, W. R., Sears, B. B., & Benning, C. (2005) · Eukaryotic Cell · doi:10.1128/ec.4.2.242-252.2005 · Cited by 229 · see citing works
Self-citationAthenstaedt, K., & Daum, G. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m507261200 · Cited by 212 · see citing works
Martin, N. C., & Goodenough, U. W. (1975) · The Journal of Cell Biology · doi:10.1083/jcb.67.3.587 · Cited by 183 · see citing works
Bloom, J. S., Khan, Z., Kruglyak, L., Singh, M., & Caudy, A. A. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-221 · Cited by 178 · see citing works
Isolation of the Chlamydomonas regulatory gene NIT2 by transposon tagging.
Schnell, R. A., & Lefebvre, P. A. (1993) · Genetics · doi:10.1093/genetics/134.3.737 · Cited by 177 · see citing works
Chlamydomonas reinhardtii Genome Project. A Guide to the Generation and Use of the cDNA Information
Shrager, J., Hauser, C. R., Chang, C.-W., Harris, E. H., Davies, J. P., McDermott, J., Kuehn, R., Zhang, Z., & Grossman, A. R. (2003) · PLANT PHYSIOLOGY · doi:10.1104/pp.016899 · Cited by 173 · see citing works
Acclimation to Singlet Oxygen Stress in Chlamydomonas reinhardtii
Ledford, H. K., Chin, B. L., & Niyogi, K. (2007) · Eukaryotic Cell · doi:10.1128/ec.00207-06 · Cited by 171 · see citing works
Chlororespiration: an adaptation to nitrogen deficiency in Chlamydomonas reinhardtii.
Peltier, G., & Schmidt, G. W. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.11.4791 · Cited by 159 · see citing works
Evidence for a Role of ClpP in the Degradation of the Chloroplast Cytochrome b6f Complex
Majeran, W., Wollman, F., & Vallon, O. (2000) · The Plant Cell · doi:10.1105/tpc.12.1.137 · Cited by 159 · see citing works
Taylor, L. E., Nunes‐Nesi, A., Parsley, K., Leiss, A., Leach, G., Coates, S. A., Wingler, A., Fernie, A. R., & Hibberd, J. M. (2010) · The Plant Journal · doi:10.1111/j.1365-313x.2010.04179.x · Cited by 150 · see citing works
Mussgnug, J. H., Wobbe, L., Ingolf, E., Claus, C., Hamilton, M., Fink, A., Kahmann, U., Kapazoglou, A., Mullineaux, C. W., Hippler, M., et al. (2005) · The Plant Cell · doi:10.1105/tpc.105.035774 · Cited by 145 · see citing works
Nguyen, A. V., Thomas‐Hall, S. R., Malnoë, A., Timmins, M., Mussgnug, J. H., Rupprecht, J., Kruse, O., Hankamer, B. D., & Schenk, P. M. (2008) · Eukaryotic Cell · doi:10.1128/ec.00418-07 · Cited by 141 · see citing works
Nitrate Signaling by the Regulatory Gene NIT2 in Chlamydomonas
Camargo, A., Llamas, Á., Schnell, R. A., et al. (2007) · The Plant Cell · doi:10.1105/tpc.106.045922 · Cited by 137 · see citing works
Yamano, T., Miura, K., & Fukuzawa, H. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.107.114652 · Cited by 117 · see citing works
Li, X., Gilmore, A. M., & Niyogi, K. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m204797200 · Cited by 107 · see citing works
Self-citationNitrogen-dependent regulation of photosynthetic gene expression
Plumley, F. G., & Schmidt, G. W. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.8.2678 · Cited by 106 · see citing works
A New Subunit of Cytochromeb 6 f Complex Undergoes Reversible Phosphorylation upon State Transition
Hamel, P. P., Olive, J., Pierre, Y., et al. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m001468200 · Cited by 104 · see citing works
Bonente, G., Passarini, F., Cazzaniga, S., Mancone, C., Buia, M. C., Tripodi, M., Bassi, R., & Caffarri, S. (2008) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.2008.00456.x · Cited by 101 · see citing works
Jamers, A., van der Ven, K., Moens, L., et al. (2006) · Aquatic Toxicology · doi:10.1016/j.aquatox.2006.09.002 · Cited by 90 · see citing works
Pollard, M., & Ohlrogge, J. B. (1999) · PLANT PHYSIOLOGY · doi:10.1104/pp.121.4.1217 · Cited by 87 · see citing works
González-Ballester, D., Camargo, A., & Fernández, E. M. (2004) · Plant Molecular Biology · doi:10.1007/s11103-004-5292-7 · Cited by 84 · see citing works
Bulté, L., & Wollman, F.-A. (1992) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1992.tb16641.x · Cited by 81 · see citing works
The Stable Isotope-based Dynamic Metabolic Profile of Butyrate-induced HT29 Cell Differentiation
Boren, J., Lee, W.-N. P., Bassilian, S., Centelles, J. J., Lim, S., Ahmed, S., Boros, L. G., & Cascante, M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m302932200 · Cited by 78 · see citing works
Conservation and degradation of cytoplasmic and chloroplast ribosomes in Chlamydomonas reinhardtii
Siersma, P. W., & Chiang, K. (1971) · Journal of Molecular Biology · doi:10.1016/0022-2836(71)90239-7 · Cited by 74 · see citing works
Ledford, H. K., Baroli, I., Shin, J. W., Fischer, B. B., Eggen, R. I. L., & Niyogi, K. (2004) · Molecular Genetics and Genomics · doi:10.1007/s00438-004-1078-5 · Cited by 69 · see citing works
Turnover of chloroplast and cytoplasmic ribosomes during gametogenesis in Chlamydomonas reinhardi
Martín, N. C. R., Chiang, K., & Goodenough, U. W. (1976) · Developmental Biology · doi:10.1016/0012-1606(76)90137-8 · Cited by 65 · see citing works
Mamedov, T., Moellering, E. R., & Chollet, R. (2005) · The Plant Journal · doi:10.1111/j.1365-313x.2005.02416.x · Cited by 65 · see citing works
Self-citationNitrogen Assimilation and its Regulation
Fernández, E. M., Galván, A., & Quesada, A. (2006) · Kluwer Academic Publishers eBooks · doi:10.1007/0-306-48204-5_33 · Cited by 63 · see citing works
Evidence for a Role of ClpP in the Degradation of the Chloroplast Cytochrome b 6 f Complex
Majeran, W., Wollman, F.-A., & Vallon, O. (2000) · The Plant Cell · doi:10.2307/3871035 · Cited by 58 · see citing works
Baurain, D., Dinant, M., Coosemans, N., & Matagne, R. F. (2003) · PLANT PHYSIOLOGY · doi:10.1104/pp.013409 · Cited by 51 · see citing works
A Gamete-specific, Sex-limited Homeodomain Protein in Chlamydomonas
Kurvari, V., Grishin, N. V., & Snell, W. J. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.143.7.1971 · Cited by 51 · see citing works
Diacylglycerol kinase and phosphatidic acid phosphatase—enzymes metabolizing lipid second messengers
Kanoh, H., Sakane, F., Imai, S.-I., & Wada, I. (1993) · Cellular Signalling · doi:10.1016/0898-6568(93)90045-n · Cited by 46 · see citing works
Deshpande, R., Yang, T. H., & Heinzle, E. (2009) · Biotechnology Journal · doi:10.1002/biot.200800143 · Cited by 45 · see citing works
Self-citationAge-dependent induction of pyruvate, orthophosphate dikinase in Mesembryanthemum crystallinum L.
Fi�lthaler, B., Meyer, G., Bohnert, H., et al. (1995) · Planta · doi:10.1007/bf00203649 · Cited by 44 · see citing works
Nitrogen Assimilation and its Regulation
Fernández, E. M., Llamas, Á., & Galván, A. (2009) · Elsevier eBooks · doi:10.1016/b978-0-12-370873-1.00011-3 · Cited by 39 · see citing works
Global expression profiling of Chlamydomonas reinhardtii exposed to trace levels of free cadmium
Simon, D. F., Descombes, P., Zerges, W., et al. (2008) · Environmental Toxicology and Chemistry · doi:10.1897/07-649.1 · Cited by 37 · see citing works
Hachey, D. L., Parsons, W. R., McKay, S. V., & Haymond, M. W. (1999) · Analytical Chemistry · doi:10.1021/ac990724x · Cited by 35 · see citing works
Østerås, M., Driscoll, B. T., & Finan, T. M. (1997) · Microbiology · doi:10.1099/00221287-143-5-1639 · Cited by 34 · see citing works
Riekhof, W. R., & Benning, C. (2009) · Elsevier eBooks · doi:10.1016/b978-0-12-370873-1.00010-1 · Cited by 24 · see citing works
Self-citationChlamydomonas in the Laboratory
(2009) · Elsevier eBooks · doi:10.1016/b978-0-12-370873-1.00008-3 · Cited by 22 · see citing works
Unbalanced growth and macromolecular synthesis in Streptococcus mutans FA-1
Mattingly, S. J., DiPersio, J. R., Higgins, M. L., et al. (1976) · Infection and Immunity · doi:10.1128/iai.13.3.941-948.1976 · Cited by 16 · see citing works
MacLeod, J. K., Flanigan, I. L., Williams, J. F., et al. (2001) · Journal of Mass Spectrometry · doi:10.1002/jms.147 · Cited by 16 · see citing works
Harris, E. H. (1989) · Elsevier eBooks · doi:10.1016/b978-0-12-326880-8.50009-2 · Cited by 11 · see citing works
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Vieler, A., Wu, G., Tsai, C.-H., Bullard, B., Cornish, A. J., Harvey, C., Reca, I.-B., Thornburg, C., Achawanantakun, R., Buehl, C. J., et al. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003064 · Cited by 458 · see citing works
Self-citationLi, J., Han, D., Wang, D., Ning, K., Jia, J., Wei, L., Jing, X., Huang, S., Chen, J., Li, Y., et al. (2014) · The Plant Cell · doi:10.1105/tpc.113.121418 · Cited by 412 · see citing works
Hockin, N. L., Mock, T., Mulholland, F., Kopriva, S., & Malin, G. (2012) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.184333 · Cited by 372 · see citing works
Fan, J., Andre, C., & Xu, C. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.05.018 · Cited by 347 · see citing works
Fan, J., Cui, Y., Wan, M., Wang, W., & Li, Y. (2014) · Biotechnology for Biofuels · doi:10.1186/1754-6834-7-17 · Cited by 341 · see citing works
Li, X., Moellering, E. R., Liu, B., Johnny, C., Fedewa, M., Sears, B. B., Kuo, M.-H., & Benning, C. (2012) · The Plant Cell · doi:10.1105/tpc.112.105106 · Cited by 320 · see citing works
Self-citationMetabolism of acyl‐lipids in <i>Chlamydomonas reinhardtii</i>
Li‐Beisson, Y., Beisson, F., & Riekhof, W. (2015) · The Plant Journal · doi:10.1111/tpj.12787 · Cited by 310 · see citing works
Guarnieri, M. T., Nag, A., Smolinski, S. L., Darzins, A., Seibert, M., & Pienkos, P. T. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025851 · Cited by 234 · see citing works
Storage of starch and lipids in microalgae: Biosynthesis and manipulation by nutrients
Ran, W., Wang, H., Liu, Y., Qi, M., Xiang, Q., Yao, C., Zhang, Y., & Lan, X. (2019) · Bioresource Technology · doi:10.1016/j.biortech.2019.121894 · Cited by 224 · see citing works
Zienkiewicz, K., Du, Z.-Y., Ma, W., Vollheyde, K., & Benning, C. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2016.02.008 · Cited by 225 · see citing works
Singh, P., Guldhe, A., Kumari, S., Rawat, I., & Bux, F. (2015) · Biochemical Engineering Journal · doi:10.1016/j.bej.2014.10.019 · Cited by 202 · see citing works
Responses of<i>Nannochloropsis oceanica</i>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, A. R. (2013) · Plant Physiology · doi:10.1104/pp.113.214320 · Cited by 173 · see citing works
Overcoming biological constraints to enable the exploitation of microalgae for biofuels
Day, J. G., Slocombe, S. P., & Stanley, M. S. (2012) · Bioresource Technology · doi:10.1016/j.biortech.2011.05.033 · Cited by 162 · see citing works
Mao, X., Zhang, Y., Wang, X., & Liu, J. (2020) · Biotechnology for Biofuels · doi:10.1186/s13068-020-01714-y · Cited by 104 · see citing works
Algal omics: unlocking bioproduct diversity in algae cell factories
Guarnieri, M. T., & Pienkos, P. T. (2015) · Photosynthesis Research · doi:10.1007/s11120-014-9989-4 · Cited by 97 · see citing works
Vigeolas, H., Duby, F., Kaymak, E., Niessen, G., Motte, P., Franck, F., & Remacle, C. (2012) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2012.03.017 · Cited by 90 · see citing works
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Sulochana, S. B., & Arumugam, M. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.585632 · Cited by 47 · see citing works
Davis, R. W., Volponi, J. V., Jones, H. D. T., Carvalho, B. J., Wu, H., & Singh, S. (2012) · Biotechnology and Bioengineering · doi:10.1002/bit.24517 · Cited by 22 · see citing works
Sonkar, S., & Mallick, N. (2017) · Environmental Progress & Sustainable Energy · doi:10.1002/ep.12443 · Cited by 20 · see citing works
- Authors
- Miller, R., Wu, G., Deshpande, R. R., Vieler, A., Gärtner, K., Li, X., Moellering, E. R., Zäuner, 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.
- Affiliations
- Cell and Molecular Biology Program (R.M., G.W.), Department of Energy-Plant Research Laboratory (R.M., X.L., E.R.M.), Department of Plant Biology (R.R.D., X.L., B.B.S., Y.S.-H., S.-H.S.), and Department of Biochemistry and Molecular Biology (A.V., K.G., E.R.M., S.Z., A.J.C., B.L., B.B., M.-H.K., E.L.H., C.B.), Michigan State University, East Lansing, Michigan 48824
- Venue
- PLANT PHYSIOLOGY
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-10-08
- Volume
- 154
- Issue
- 4
- Pages
- 1737-1752
- ISSN
- 0032-0889 (ISSN-L)
- 1532-2548
- PMC
- PMC2996024
- OpenAlex
- W2120780572
- Cited by
- 511
- References
- 76
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- FWCI
- 15.86
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- PLANT PHYSIOLOGY (publishedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Joint Genome Institute
- Topics
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Keywords
- Chlamydomonas reinhardtii, nitrogen starvation, triglyceride accumulation, lipid droplets, mRNA levels, gene expression profiling, gametogenesis, fatty acid synthesis, acetate metabolism, glyoxylate cycle, gluconeogenesis, membrane remodeling, lipase gene, photosynthesis genes
- MeSH terms
- Base Sequence, Gas Chromatography-Mass Spectrometry, Nitrogen, Photosynthesis, RNA, Messenger, Transcription Factors, Blotting, Northern, Gene Expression, Chlamydomonas reinhardtii, DNA Primers, Reverse Transcriptase Polymerase Chain Reaction, Lipid Metabolism
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