Oil accumulation mechanisms of the oleaginous microalga Chlorella protothecoides revealed through its genome, transcriptomes, and proteomes
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BACKGROUND: Microalgae-derived biodiesel is a promising substitute for conventional fossil fuels. In particular, the green alga Chlorella protothecoides sp. 0710 is regarded as one of the best candidates for commercial manufacture of microalgae-derived biofuel. This is due not only to its ability to live autotrophically through photosynthesis, but also to its capacity to produce a large amount of biomass and lipid through fermentation of glucose. However, until the present study, neither its genome sequence nor the platform required for molecular manipulations were available. RESULTS: We generated a draft genome for C. protothecoides, and compared its genome size and gene content with that of Chlorella variabilis NC64A and Coccomyxa subellipsoidea C-169. This comparison revealed that C. protothecoides has a reduced genome size of 22.9 Mbp, about half that of its close relatives. The C. protothecoides genome encodes a smaller number of genes, fewer multi-copy genes, fewer unique genes, and fewer genome rearrangements compared with its close relatives. In addition, three Chlorella-specific hexose-proton symporter (HUP)-like genes were identified that enable the consumption of glucose and, consequently, heterotrophic growth. Furthermore, through comparative transcriptomic and proteomic studies, we generated a global perspective regarding the changes in metabolic pathways under autotrophic and heterotrophic growth conditions. Under heterotrophic conditions, enzymes involved in photosynthesis and CO2 fixation were almost completely degraded, either as mRNAs or as proteins. Meanwhile, the cells were not only capable of quickly assimilating glucose but also showed accelerated glucose catabolism through the upregulation of glycolysis and the tricarboxylic acid (TCA) cycle. Moreover, the rapid synthesis of pyruvate, upregulation of most enzymes involved in fatty acid synthesis, and downregulation of enzymes involved in fatty acid degradation favor the synthesis of fatty acids within the cell. CONCLUSIONS: Despite similarities to other Chlorella, C. protothecoides has a smaller genome than its close relatives. Genes involved in glucose utilization were identified, and these genes explained its ability to grow heterotrophically. Transcriptomic and proteomic results provided insight into its extraordinary ability to accumulate large amounts of lipid. The C. protothecoides draft genome will promote the use of this species as a research model.
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In Auxenochlorella protothecoides, genome scale and core metabolic model targeting biodiesel enhanced lipid productivity and increased lipid content.
“| 1 | Auxenochlorella protothecoides | 22.92 | Genome scale and core metabolic model | Biodiesel | Sequencing, phenotypic characterization, lipid analysis | Endogenous promoters or heterologous expression constructs | Enhanced lipid productivity, increased lipid content | Biofuel production | [89] |”
From A Holistic Approach to Circular Bioeconomy Through the Sustainable Utilization of Microalgal Biomass for Biofuel and Other Value-Added Products (2024) · cites this paper as [89]
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Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482 · see citing works
MUSCLE: multiple sequence alignment with high accuracy and high throughput
Edgar, R. C. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh340 · Cited by 44,662 · see citing works
Gene Ontology: tool for the unification of biology
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., et al. (2000) · Nature Genetics · doi:10.1038/75556 · Cited by 43,206 · see citing works
KEGG: Kyoto Encyclopedia of Genes and Genomes
Kanehisa, M. (2000) · Nucleic Acids Research · doi:10.1093/nar/28.1.27 · Cited by 37,077 · see citing works
KEGG: Kyoto Encyclopedia of Genes and Genomes
Ogata, H., Goto, S., Sato, K., Fujibuchi, W., Bono, H., & Kanehisa, M. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.1.29 · Cited by 31,232 · see citing works
A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood
Guindon, S., & Gascuel, O. (2003) · Systematic Biology · doi:10.1080/10635150390235520 · Cited by 16,698 · 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
Mapping and quantifying mammalian transcriptomes by RNA-Seq
Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L., & Wold, B. (2008) · Nature Methods · doi:10.1038/nmeth.1226 · Cited by 13,696 · 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
Tandem repeats finder: a program to analyze DNA sequences
Benson, G. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.2.573 · Cited by 9,374 · see citing works
Genome sequencing in microfabricated high-density picolitre reactors
Margulies, M., Egholm, M., Altman, W. E., Attiya, S., Bader, J. S., Bemben, L. A., Berka, J., Braverman, M. S., Chen, Y.-J., Chen, Z., et al. (2005) · Nature · doi:10.1038/nature03959 · Cited by 7,693 · see citing works
Self-citationRepbase Update, a database of eukaryotic repetitive elements
Jurka, J., Kapitonov, V. V., Pavlı́ček, A., Klonowski, P., Kohany, O., & Walichiewicz, J. (2005) · Cytogenetic and Genome Research · doi:10.1159/000084979 · Cited by 3,332 · see citing works
Korf, I. F. (2004) · BMC Bioinformatics · doi:10.1186/1471-2105-5-59 · Cited by 3,160 · see citing works
De novo assembly of human genomes with massively parallel short read sequencing
Li, R., Zhu, H., Ruan, J., Qian, W., Fang, X., Shi, Z., Li, Y., Li, S., Shan, G., Kristiansen, K., et al. (2010) · Genome Research · doi:10.1101/gr.097261.109 · Cited by 2,926 · cited 1× · see citing works
“01 [37]”
AUGUSTUS: ab initio prediction of alternative transcripts
Stanke, M., Keller, O., Gunduz, I., Hayes, A., Waack, S., & Morgenstern, B. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl200 · Cited by 2,829 · see citing works
The Significance of Digital Gene Expression ProfilesPreprint
Audic, S., & Claverie, J. (1997) · Genome Research · doi:10.1101/gr.7.10.986 · Cited by 2,793 · see citing works
LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons
Xu, Z., & Wang, H. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm286 · Cited by 2,618 · see citing works
CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes
Parra, G., Bradnam, K. R., & Korf, I. F. (2007) · Bioinformatics · doi:10.1093/bioinformatics/btm071 · Cited by 2,159 · see citing works
De novo identification of repeat families in large genomes
Price, A. L., Jones, N. C., & Pevzner, P. A. (2005) · Bioinformatics · doi:10.1093/bioinformatics/bti1018 · Cited by 2,138 · see citing works
TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders
Majoros, W. H., Pertea, M., & Salzberg, S. L. (2004) · Bioinformatics · doi:10.1093/bioinformatics/bth315 · Cited by 1,938 · see citing works
Heterotrophic cultures of microalgae: Metabolism and potential products
Perez‐Garcia, O., Escalante, F. M. E., de‐Bashan, L. E., & Yoav Bashan, A. (2010) · Water Research · doi:10.1016/j.watres.2010.08.037 · Cited by 1,766 · see citing works
Biodiesel production from heterotrophic microalgal oil
Miao, X., & Wu, Q. (2006) · Bioresource Technology · doi:10.1016/j.biortech.2005.04.008 · Cited by 1,358 · see citing works
Self-citationBiodiesel from algae: challenges and prospects
Scott, S. A., Davey, M. P., Dennis, J. S., Horst, I., Howe, C. J., Lea-Smith, D. J., & Smith, A. G. (2010) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2010.03.005 · Cited by 1,183 · see citing works
The sequence and de novo assembly of the giant panda genome
Li, R., Fan, W., Tian, G., Zhu, H., He, L., Cai, J., Huang, Q., Cai, Q., Li, B., Bai, Y., et al. (2010) · Nature · doi:10.1038/nature08696 · Cited by 1,180 · see citing works
Self-citationXu, H., Miao, X., & Wu, Q. (2006) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2006.05.002 · Cited by 1,125 · see citing works
Self-citationKumar, A., & Bennetzen, J. L. (1999) · Annual Review of Genetics · doi:10.1146/annurev.genet.33.1.479 · Cited by 1,055 · see citing works
Extraction of oil from microalgae for biodiesel production: A review
Halim, R., Danquah, M. K., & Webley, P. A. (2012) · Biotechnology Advances · doi:10.1016/j.biotechadv.2012.01.001 · Cited by 1,043 · see citing works
InterPro in 2011: new developments in the family and domain prediction database
Hunter, S., Jones, P., Mitchell, A., Apweiler, R., Attwood, T. K., Bateman, A. G., Bernard, T., Binns, D., Peer Bork, B., Burge, S., et al. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr948 · Cited by 1,036 · see citing works
Evolution's cauldron: Duplication, deletion, and rearrangement in the mouse and human genomes
Kent, W. J., Baertsch, R., Hinrichs, A., Miller, W., & Haussler, D. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1932072100 · Cited by 850 · see citing works
Function and Regulation of Yeast Hexose Transporters
Özcan, S., & Johnston, M. (1999) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.63.3.554-569.1999 · Cited by 729 · see citing works
R EGULATION OF E NZYMES OF THE U REA C YCLE AND A RGININE M ETABOLISM
Morris, S. M. (2002) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.22.110801.140547 · Cited by 727 · see citing works
PILER: identification and classification of genomic repeats
Edgar, R. C., & Myers, E. W. (2005) · Bioinformatics · doi:10.1093/bioinformatics/bti1003 · Cited by 711 · see citing works
Palenik, B., Grimwood, J., Aerts, A., Rouzé, P., Salamov, A., Putnam, N., Dupont, C., Jorgensen, R., Derelle, E., Rombauts, S., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611046104 · Cited by 625 · see citing works
Xiong, W., Li, X., Xiang, J., & Wu, Q. (2007) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-007-1285-1 · Cited by 542 · see citing works
Self-citationTreeFam: a curated database of phylogenetic trees of animal gene families
Li, H. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkj118 · Cited by 523 · see citing works
Evolution and metabolic significance of the urea cycle in photosynthetic diatoms
Allen, A. E., Dupont, C. L., Obornı́k, M., Horák, A., Nunes‐Nesi, A., McCrow, J. P., Zheng, H., Johnson, D. A., Hu, H., Fernie, A. R., et al. (2011) · Nature · doi:10.1038/nature10074 · Cited by 518 · see citing works
Blanc, G., Duncan, G. A., Agarkova, I., Borodovsky, M. Y., Gurnon, J. R., Kuo, A., Lindquist, E., Lucas, S. M., Pangilinan, J. L., Polle, J. E. W., et al. (2010) · The Plant Cell · doi:10.1105/tpc.110.076406 · Cited by 504 · see citing works
Callister, S., Barry, R., Adkins, J., Johnson, E. T., Qian, W., Webb‐Robertson, B., Smith, R. D., & Lipton, M. S. W. (2006) · Journal of Proteome Research · doi:10.1021/pr050300l · Cited by 500 · see citing works
Sugar transporters in higher plants – a diversity of roles and complex regulation
Williams, L. E., Lemoine, R., & Sauer, N. (2000) · Trends in Plant Science · doi:10.1016/s1360-1385(00)01681-2 · Cited by 424 · see citing works
Swiss-Prot: Juggling between evolution and stability
Bairoch, A. (2004) · Briefings in Bioinformatics · doi:10.1093/bib/5.1.39 · Cited by 357 · see citing works
Creating a honey bee consensus gene set
Elsik, C. G., Mackey, A. J., Reese, J., Milshina, N. V., Roos, D. S., & Weinstock, G. M. (2007) · Genome biology · doi:10.1186/gb-2007-8-1-r13 · Cited by 327 · see citing works
Blanc, G., Agarkova, I. V., Grimwood, J., Kuo, A., Brueggeman, A. J., Dunigan, D. D., Gurnon, J. R., Ladunga, I., Lindquist, E., Lucas, S. M., et al. (2012) · Genome biology · doi:10.1186/gb-2012-13-5-r39 · Cited by 318 · see citing works
Carbon and nitrogen nutrient balance signaling in plants
Zheng, Z. (2009) · Plant Signaling & Behavior · doi:10.4161/psb.4.7.8540 · Cited by 308 · see citing works
Targeting of the Arabidopsis Homomeric Acetyl-Coenzyme A Carboxylase to Plastids of Rapeseeds
Roesler, K. R., Shintani, D. K., Savage, L., Boddupalli, S., & Ohlrogge, J. B. (1997) · PLANT PHYSIOLOGY · doi:10.1104/pp.113.1.75 · Cited by 307 · see citing works
Gao, C., Zhai, Y., Ding, Y. M., & Wu, Q. (2009) · Applied Energy · doi:10.1016/j.apenergy.2009.09.006 · Cited by 304 · see citing works
Self-citationGenome assembly forensics: finding the elusive mis-assembly
Phillippy, A. M., Schatz, M. C., & Pop, M. (2008) · Genome biology · doi:10.1186/gb-2008-9-3-r55 · Cited by 275 · see citing works
Regulatory links between carbon and nitrogen metabolism
Commichau, F. M., Forchhammer, K., & Stülke, J. (2006) · Current Opinion in Microbiology · doi:10.1016/j.mib.2006.01.001 · Cited by 226 · see citing works
Cheng, Y., Zhou, W., Gao, C., Lan, K., Gao, Y., & Wu, Q. (2009) · Journal of Chemical Technology & Biotechnology · doi:10.1002/jctb.2111 · Cited by 194 · see citing works
Self-citationXiong, W., Gao, C., Yan, D., Wu, C., & Wu, Q. (2009) · Bioresource Technology · doi:10.1016/j.biortech.2009.11.041 · Cited by 186 · see citing works
Self-citationYan, D., Lu, Y., Chen, Y.-F., & Wu, Q. (2011) · Bioresource Technology · doi:10.1016/j.biortech.2011.03.036 · Cited by 179 · see citing works
Self-citationThe mode and tempo of genome size evolution in eukaryotesPreprint
Oliver, M. J., Petrov, D. A., Ackerly, D. D., Falkowski, P. G., & Schofield, O. (2007) · Genome Research · doi:10.1101/gr.6096207 · Cited by 160 · see citing works
The hexose carrier from Chlorella
Sauer, N., & Tanner, W. (1989) · FEBS Letters · doi:10.1016/0014-5793(89)81489-9 · Cited by 156 · see citing works
Doebbe, A., Rupprecht, J., Beckmann, J., Mussgnug, J. H., Hallmann, A., Hankamer, B. D., & Kruse, O. (2007) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2007.05.017 · Cited by 149 · see citing works
Decoding algal genomes: tracing back the history of photosynthetic life on Earth.
Tirichine, L., & Bowler, C. (2011) · The Plant Journal · doi:10.1111/j.1365-313x.2011.04540.x · Cited by 134 · see citing works
Chen, M., & Thelen, J. J. (2010) · The Plant Cell · doi:10.1105/tpc.109.071837 · Cited by 122 · see citing works
McCurdy, D. W., Dibley, S. J., Cahyanegara, R., Martin, A., & Patrick, J. W. (2010) · Molecular Plant · doi:10.1093/mp/ssq050 · Cited by 96 · see citing works
Stadler, R., Wolf, K., Hilgarth, C., Tanner, W., & Sauer, N. (1995) · PLANT PHYSIOLOGY · doi:10.1104/pp.107.1.33 · Cited by 63 · see citing works
Shotgun proteomic analysis of the unicellular alga Ostreococcus tauri
Bihan, T. L., Martin, S. F., Salvo‐Chirnside, E., Gerben Van Ooijen, A., Barrios-Llerena, M. E., O'Neill, J. S., Shliaha, P. V., Kerr, L. E., & Millar, A. J. (2011) · Journal of Proteomics · doi:10.1016/j.jprot.2011.05.028 · Cited by 60 · see citing works
Triosephosphate isomerase deficiency: a neurodegenerative misfolding disease
Oláh, J., Orosz, F., Keserű, G. M., Kovári, Z., Kovács, J., Hollán, S. R., & Ovádi, J. (2002) · Biochemical Society Transactions · doi:10.1042/bst0300030 · Cited by 50 · see citing works
Simultaneous saccharification of cassava starch and fermentation of algae for biodiesel production
Lu, Y., Ding, Y. M., & Wu, Q. (2010) · Journal of Applied Phycology · doi:10.1007/s10811-010-9549-z · Cited by 48 · see citing works
Self-citationKato, Y., Ueno, S., & Imamura, N. (2005) · Plant Science · doi:10.1016/j.plantsci.2005.09.018 · Cited by 32 · see citing works
Km mutants of the Chlorella monosaccharide/H+ cotransporter randomly generated by PCR.
Will, A., Caspari, T., & Tanner, W. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.21.10163 · Cited by 26 · see citing works
Characterization of an ammonium transporter in the oleaginous alga Chlorella protothecoides
Yan, D., Dai, J., & Wu, Q. (2012) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-012-4534-x · Cited by 20 · see citing works
Self-citationZhang, N., Zhang, Z., Feng, S., Wang, Q., Malamud, D., & Deng, H. (2013) · Analytica Chimica Acta · doi:10.1016/j.aca.2013.02.038 · Cited by 15 · see citing works
Flagged first, then by citations
1 of the 65 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Heterotrophic cultivation of microalgae for pigment production: A review
Hu, J., Nagarajan, D., Zhang, Q., Chang, J., & Lee, D. (2017) · Biotechnology Advances · doi:10.1016/j.biotechadv.2017.09.009 · Cited by 456 · see citing works
The biochemistry and molecular biology of chlorophyll breakdown
Kuai, B., Chen, J., & Hörtensteiner, S. (2017) · Journal of Experimental Botany · doi:10.1093/jxb/erx322 · Cited by 334 · see citing works
Kumar, G., Shekh, A., Jakhu, S., Sharma, Y., Kapoor, R., & Sharma, T. R. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.00914 · Cited by 315 · see citing works
Wei, H., Shi, Y., Ma, X., Pan, Y., Hu, H., Li, Y., Luo, M., Gerken, H. G., & Liu, J. (2017) · Biotechnology for Biofuels · doi:10.1186/s13068-017-0858-1 · Cited by 154 · see citing works
Strategies to enhance production of microalgal biomass and lipids for biofuel feedstock
Chu, W.-L. (2017) · European Journal of Phycology · doi:10.1080/09670262.2017.1379100 · Cited by 146 · see citing works
Genomic Foundation of Starch-to-Lipid Switch in Oleaginous Chlorella spp.
Fan, J., Ning, K., Zeng, X., Luo, Y., Wang, D., Hu, J., Li, J., Xu, H., Huang, J., Wan, M., et al. (2015) · PLANT PHYSIOLOGY · doi:10.1104/pp.15.01174 · Cited by 144 · see citing works
Omics approaches for microalgal applications: Prospects and challenges
Mishra, A., Medhi, K., Malaviya, P., & Thakur, I. S. (2019) · Bioresource Technology · doi:10.1016/j.biortech.2019.121890 · Cited by 141 · see citing works
Comparative and Functional Algal Genomics
Blaby-Haas, C. E., & Merchant, S. S. (2019) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050718-095841 · Cited by 131 · see citing works
Ma, C., Wen, H.-Q., Xing, D., Pei, X., Zhu, J.-N., Ren, N., & Liu, B.-F. (2017) · Biotechnology for Biofuels · doi:10.1186/s13068-017-0797-x · Cited by 130 · see citing works
Lin, W., Tan, S., Hsiang, C., Sung, P.-K., & Ng, I. (2019) · Bioresource Technology · doi:10.1016/j.biortech.2019.121932 · Cited by 108 · see citing works
Roth, M., Gallaher, S. D., Westcott, D. J., Iwai, M., Louie, K., Mueller, M., Walter, A., Foflonker, F., Bowen, B. P., Ataii, N. N., et al. (2019) · The Plant Cell · doi:10.1105/tpc.18.00742 · Cited by 106 · see citing works
Wu, C., Xiong, W., Dai, J., & Wu, Q. (2015) · Plant Physiology · doi:10.1104/pp.114.250688 · Cited by 99 · see citing works
Self-citationAdvances and challenges in genetic engineering of microalgae
Fajardo, C., Donato, M. D., Carrasco-Reinado, R., Martı́nez-Rodrı́guez, G., Mancera, J. M., & Fernández‐Acero, F. J. (2019) · Reviews in Aquaculture · doi:10.1111/raq.12322 · Cited by 103 · see citing works
Ezhumalai, G., Arun, M., Manavalan, A., Rajkumar, R., & Heese, K. (2024) · Microbial Ecology · doi:10.1007/s00248-024-02376-1 · Cited by 99 · see citing works
Yang, B., Liu, J., Jiang, Y., & Chen, F. (2016) · Biotechnology Journal · doi:10.1002/biot.201500617 · Cited by 94 · see citing works
Algal Cell Factories: Approaches, Applications, and Potentials
Fu, W., Chaiboonchoe, A., Khraiwesh, B., Nelson, D. R., Al-Khairy, D., Mystikou, A., Alzahmi, A. S., & Salehi‐Ashtiani, K. (2016) · Marine Drugs · doi:10.3390/md14120225 · Cited by 90 · see citing works
Ota, S., Oshima, K., Yamazaki, T., Kim, S., Yu, Z., Yoshihara, M., Takeda, K., Takeshita, T., Hirata, A., Bišová, K., et al. (2016) · Biotechnology for Biofuels · doi:10.1186/s13068-016-0424-2 · Cited by 88 · see citing works
Metabolic co-dependence drives the evolutionarily ancient Hydra–Chlorella symbiosis
Hamada, M., Schröder, K., Bathia, J., Kürn, U., Fraune, S., Khalturina, M., Khalturin, K., Shinzato, C., Satoh, N., & Bosch, T. C. G. (2018) · eLife · doi:10.7554/elife.35122 · Cited by 83 · see citing works
Cecchin, M., Marcolungo, L., Rossato, M., Girolomoni, L., Cosentino, E., Cuine, S., Li‐Beisson, Y., Delledonne, M., & Ballottari, M. (2019) · The Plant Journal · doi:10.1111/tpj.14508 · Cited by 83 · see citing works
Rai, V., Muthuraj, M., Gandhi, M., Das, D., & Srivastava, S. (2017) · Scientific Reports · doi:10.1038/srep45732 · Cited by 82 · see citing works
Lipid Accumulation Mechanisms in Auto- and Heterotrophic Microalgae
Chen, H., & Jiang, J. (2017) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.7b03495 · Cited by 83 · see citing works
Suzuki, S., Yamaguchi, H., Nakajima, N., & Kawachi, M. (2018) · Scientific Reports · doi:10.1038/s41598-018-26331-6 · Cited by 78 · see citing works
Efficiency and biotechnological aspects of biogas production from microalgal substrates
Классен, В., Blifernez-Klassen, O., Wobbe, L., Schlüter, A., Kruse, O., & Mussgnug, J. H. (2016) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2016.07.015 · Cited by 73 · see citing works
Landscape of microalgae omics and metabolic engineering research for strain improvement: An overview
Stavridou, E., Karapetsi, L., Nteve, G., Tsintzou, G. P., Chatzikonstantinou, M., Tsaousi, M., Martı́nez, Á. T., Flores, P., Merino, M., Dobrovic, L., et al. (2024) · Aquaculture · doi:10.1016/j.aquaculture.2024.740803 · Cited by 74 · see citing works
Smith, S. R., Glé, C., Abbriano, R. M., Traller, J. C., Davis, A. K., Trentacoste, E. M., Vernet, M., Allen, A. E., & Hildebrand, M. (2016) · New Phytologist · doi:10.1111/nph.13843 · Cited by 75 · see citing works
Structure and properties of oil bodies in diatoms
Maeda, Y., Nojima, D., Yoshino, T., & Tanaka, T. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0408 · Cited by 70 · see citing works
Microalgae Biomass and Lipids as Feedstock for Biofuels: Sustainable Biotechnology Strategies
Babu, S. S., Gondi, R., Vincent, G. S., JohnSamuel, G. C., & Jeyakumar, R. B. (2022) · Sustainability · doi:10.3390/su142215070 · Cited by 67 · see citing works
Maroneze, M. M., Zepka, L. Q., Lopes, E. J., Pérez‐Gálvez, A., & Roca, M. (2019) · Antioxidants · doi:10.3390/antiox8120600 · Cited by 63 · see citing works
Huang, W., Ye, J., Zhang, J., Lin, Y., He, M., & Huang, J. (2016) · Algal Research · doi:10.1016/j.algal.2016.05.015 · Cited by 61 · see citing works
Green genes: bioinformatics and systems-biology innovations drive algal biotechnology
Reijnders, M. J. M. F., van Heck, R. G. A., Lam, C. M. C., Scaife, M. A., dos Santos, V. A. P. M., Smith, A. G., & Schaap, P. J. (2014) · Trends in biotechnology · doi:10.1016/j.tibtech.2014.10.003 · Cited by 60 · see citing works
Msanne, J., Polle, J. E. W., & Starkenburg, S. R. (2020) · Algal Research · doi:10.1016/j.algal.2020.101911 · Cited by 60 · see citing works
Rapid and efficient genetic transformation of the green microalga Chlorella vulgaris
Kumar, M., Jeon, J., Choi, J., & Kim, S. (2018) · Journal of Applied Phycology · doi:10.1007/s10811-018-1396-3 · Cited by 59 · see citing works
Piasecka, A., Nawrocka, A., Wiącek, D., & Krzemińska, I. (2020) · Scientific Reports · doi:10.1038/s41598-020-63184-4 · Cited by 59 · see citing works
Fan, J., Xu, H., & Li, Y. (2016) · Algal Research · doi:10.1016/j.algal.2016.02.032 · Cited by 58 · see citing works
Wang, H., Zhang, Y., Zhou, W., Leksawasdi, N., & Liu, T. (2018) · Biotechnology for Biofuels · doi:10.1186/s13068-018-1329-z · Cited by 57 · see citing works
Zhao, L. D., Dai, J., & Wu, Q. (2014) · Frontiers in Plant Science · doi:10.3389/fpls.2014.00400 · Cited by 55 · see citing works
Self-citationHe, X., Dai, J., & Wu, Q. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01047 · Cited by 55 · see citing works
Self-citationRibeiro, J. E. S., Martini, M., Altomonte, I., Salari, F., Nardoni, S., Sorce, C., da Silva, F. L. H., & Andreucci, A. C. (2017) · Biocatalysis and Agricultural Biotechnology · doi:10.1016/j.bcab.2017.07.007 · Cited by 55 · see citing works
Neochloris oleoabundans is worth its salt: Transcriptomic analysis under salt and nitrogen stress
de Jaeger, L., Carrères, B. M., Springer, J., Schaap, P. J., Eggink, G., dos Santos, V. A. P. M., Wijffels, R. H., & Martens, D. E. (2018) · PLoS ONE · doi:10.1371/journal.pone.0194834 · Cited by 55 · see citing works
Xing, G., Yuan, H., Yang, J., Li, J., Gao, Q., Li, W., & Wang, E. T. (2018) · Algal Research · doi:10.1016/j.algal.2018.04.028 · Cited by 55 · see citing works
Suzuki, S., Endoh, R., Manabe, R.-I., Ohkuma, M., & Hirakawa, Y. (2018) · Scientific Reports · doi:10.1038/s41598-017-18378-8 · Cited by 53 · see citing works
Microalgal Cultivation in Secondary Effluent: Recent Developments and Future Work
Lv, J., Feng, J., Liu, Q., & Xie, S. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18010079 · Cited by 51 · see citing works
Genomic Analysis of Picochlorum Species Reveals How Microalgae May Adapt to Variable Environments
Foflonker, F., Mollegard, D., Ong, M., Yoon, H. S., & Bhattacharya, D. (2018) · Molecular Biology and Evolution · doi:10.1093/molbev/msy167 · Cited by 52 · see citing works
Eisosome Ultrastructure and Evolution in Fungi, Microalgae, and Lichens
Lee, J.-H., Heuser, J., Roth, R., & Goodenough, U. (2015) · Eukaryotic Cell · doi:10.1128/ec.00106-15 · Cited by 47 · see citing works
Kuo, E. Y., Yang, R., Chin, Y. Y., Chien, Y., Chen, Y. C., Wei, C., Kao, L., Chang, Y., Li, Y., Chen, T., et al. (2022) · Biotechnology Journal · doi:10.1002/biot.202100603 · Cited by 51 · see citing works
Wu, T., Li, L., Jiang, X., Yong, Y., Song, Y., Chen, L., Xu, X., Shen, Y., & Gu, Y. (2019) · Scientific Reports · doi:10.1038/s41598-019-45511-6 · Cited by 49 · see citing works
Self-citationXing, G., Li, J., Li, W., Lam, S. M., Yuan, H., Shui, G., & Yang, J. (2021) · Biotechnology for Biofuels · doi:10.1186/s13068-021-01881-6 · Cited by 46 · see citing works
Sarayloo, E., Tardu, M., Unlu, Y. S., Simsek, S., Cevahir, G., Erkey, C., & Kavaklı, İ. H. (2017) · Algal Research · doi:10.1016/j.algal.2017.11.009 · Cited by 43 · see citing works
Meiotic genes and sexual reproduction in the green algal class Trebouxiophyceae (Chlorophyta)
Fučíková, K., Pažoutová, M., & Rindi, F. (2015) · Journal of Phycology · doi:10.1111/jpy.12293 · Cited by 44 · see citing works
Sharma, T., & Chauhan, R. S. (2016) · Algal Research · doi:10.1016/j.algal.2016.07.020 · Cited by 45 · see citing works
Microalgae mixotrophic cultivation for β-galactosidase production
Zanette, C. M., Mariano, A. B., Yukawa, Y. S., Mendes, I., & Spier, M. R. (2019) · Journal of Applied Phycology · doi:10.1007/s10811-018-1720-y · Cited by 41 · see citing works
A streamlined and predominantly diploid genome in the tiny marine green alga Chloropicon primus
Lemieux, C., Turmel, M., Otis, C., & Pombert, J. (2019) · Nature Communications · doi:10.1038/s41467-019-12014-x · Cited by 40 · see citing works
The synthetic future of algal genomes
Goold, H., Moseley, J. L., & Lauersen, K. (2024) · Cell Genomics · doi:10.1016/j.xgen.2024.100505 · Cited by 34 · see citing works
A giant type I polyketide synthase participates in zygospore maturation in Chlamydomonas reinhardtii
Heimerl, N., Hommel, E., Westermann, M., Meichsner, D., Lohr, M., Hertweck, C., Grossman, A. R., Mittag, M., & Sasso, S. (2018) · The Plant Journal · doi:10.1111/tpj.13948 · Cited by 38 · see citing works
Azaman, S. N. A., Wong, D. C. J., Tan, S. W., Yusoff, F. M., Nagao, N., & Yeap, S. K. (2020) · Scientific Reports · doi:10.1038/s41598-020-74410-4 · Cited by 38 · see citing works
Chlorophyll breakdown—Regulation, biochemistry and phyllobilins as its products
Hörtensteiner, S., Hauenstein, M., & Kräutler, B. (2019) · Advances in botanical research · doi:10.1016/bs.abr.2019.03.004 · Cited by 35 · see citing works
Ma, C., Ren, H., Xing, D., Xie, G.-J., Ren, N., & Liu, B.-F. (2019) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2019.04.079 · Cited by 35 · see citing works
Woodworth, B. D., Mead, R. L., Nichols, C. N., & Kolling, D. R. J. (2014) · Bioresource Technology · doi:10.1016/j.biortech.2014.11.098 · Cited by 34 · see citing works
Wu, C., Xiong, W., Dai, J., & Wu, Q. (2015) · Journal of Phycology · doi:10.1111/jpy.12374 · Cited by 34 · see citing works
Self-citationYan, D., Wang, Y., Murakami, T., Shen, Y., Gong, J., Jiang, H., Smith, D., Pombert, J.-F., Dai, J., & Wu, Q.-Y. (2015) · Scientific Reports · doi:10.1038/srep14465 · Cited by 30 · see citing works
Self-citationChu, F., Cheng, J., Zhang, X., Ye, Q., Chen, S., Zhou, J., & Cen, K. (2019) · Journal of Applied Phycology · doi:10.1007/s10811-019-01811-y · Cited by 33 · see citing works
Resolving the Sequence of RNA Strands by Tip-Enhanced Raman Spectroscopy
He, Z., Qiu, W., Kizer, M. E., Wang, J., Chen, W., Sokolov, A. V., Wang, X., Hu, J., & Scully, M. O. (2020) · ACS Photonics · doi:10.1021/acsphotonics.0c01486 · Cited by 32 · see citing works
De novo assembly of middle-sized genome using MinION and Illumina sequencers
Minei, R., Hoshina, R., & Ogura, A. (2018) · BMC Genomics · doi:10.1186/s12864-018-5067-1 · Cited by 32 · see citing works
Vello, V., Umashankar, S., Phang, S., Chu, W.-L., Lim, P., Majid, N. B. A., Liew, K. E., Swarup, S., & Chew, F. T. (2018) · Algal Research · doi:10.1016/j.algal.2018.08.014 · Cited by 31 · see citing works
Characterization of four untapped microalgae for the production of lipids and carotenoids
Gong, Y., & Huang, J. (2020) · Algal Research · doi:10.1016/j.algal.2020.101897 · Cited by 31 · see citing works
Evolution of chlorophyll degradation is associated with plant transition to land
Schumacher, I., Menghini, D., Ovinnikov, S., Hauenstein, M., Fankhauser, N., Zipfel, C., Hörtensteiner, S., & Aubry, S. (2021) · The Plant Journal · doi:10.1111/tpj.15645 · Cited by 31 · see citing works
Cobos, M., Pérez, S., Braga, J., Vargas-Arana, G., Ramos, L. F., Paredes, J. D., Maddox, J. D., Marapara, J. L., & Castro, J. C. (2020) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-020-02896-1 · Cited by 44 · see citing works
Karpagam, R., Jawaharraj, K., Ashokkumar, B., Sridhar, J., & Varalakshmi, P. (2017) · Algal Research · doi:10.1016/j.algal.2017.11.031 · Cited by 29 · see citing works
Vello, V., Chu, W.-L., Lim, P., Majid, N. B. A., & Phang, S. (2018) · Journal of Applied Phycology · doi:10.1007/s10811-018-1504-4 · Cited by 27 · see citing works
Li, Y., Luo, Y., Zhou, R., Zuo, X., Zhang, Y. A., Wang, Z., Li, X., Zhang, X., Qin, Z., & Lin, C. S. K. (2024) · Chemical Engineering Journal · doi:10.1016/j.cej.2024.150302 · Cited by 26 · see citing works
Panahi, B., Farhadian, M., & Hejazi, M. A. (2020) · PLoS ONE · doi:10.1371/journal.pone.0225677 · Cited by 26 · see citing works
Groussman, M., Blaskowski, S., Coesel, S., & Armbrust, E. (2023) · Scientific Data · doi:10.1038/s41597-023-02842-4 · Cited by 21 · see citing works
Jeffers, T. L., Purvine, S. O., Nicora, C., McCombs, R., Upadhyaya, S., Stroumza, A., Whang, K., Gallaher, S. D., Dohnalkova, A. C., Merchant, S., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-50170-x · Cited by 25 · see citing works
Early Evolution of the Mitogen-Activated Protein Kinase Family in the Plant Kingdom
Kalapos, B., Hlavová, M., Nádai, T. V., Galiba, G., Bišová, K., & Dóczi, R. (2019) · Scientific Reports · doi:10.1038/s41598-019-40751-y · Cited by 25 · see citing works
Lan, X.-Y., Yan, Y., Yang, B., Li, X., & Xu, F. (2018) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2018.06.168 · Cited by 25 · see citing works
Cultivation of Green Microalgae in Bubble Column Photobioreactors and an Assay for Neutral Lipids
Wang, Q., Peng, H., & Higgins, B. T. (2019) · Journal of Visualized Experiments · doi:10.3791/59106 · Cited by 26 · see citing works
Nelson, D. R., Khraiwesh, B., Fu, W., Alseekh, S., Jaiswal, A. K., Chaiboonchoe, A., Hazzouri, K. M., O’Connor, M. J., Butterfoss, G. L., Drou, N., et al. (2017) · eLife · doi:10.7554/elife.25783 · Cited by 24 · see citing works
Utilization of papaya waste and oil production by Chlorella protothecoides
Heller, W. P., Kissinger, K. R., Matsumoto, T. K., & Keith, L. M. W. (2015) · Algal Research · doi:10.1016/j.algal.2015.08.013 · Cited by 23 · see citing works
Song, H., He, M., Wu, C., Gu, C., & Wang, C. (2020) · Algal Research · doi:10.1016/j.algal.2020.101792 · Cited by 23 · see citing works
Kurotani, A., Yamada, Y., & Sakurai, T. (2016) · Plant and Cell Physiology · doi:10.1093/pcp/pcw212 · Cited by 22 · see citing works
Fan, W.-S., Guo, W.-H., van Etten, J., & Mower, J. (2017) · Scientific Reports · doi:10.1038/s41598-017-10388-w · Cited by 20 · see citing works
Heterotrophic Microalgal Cultivation
Nagarajan, D., Lee, D., & Chang, J. (2018) · Green energy and technology · doi:10.1007/978-981-10-7677-0_4 · Cited by 21 · see citing works
Higgins, B. T., Wang, Q., Du, S., Hennebelle, M., Taha, A. Y., Fiehn, O., & VanderGheynst, J. S. (2018) · Algal Research · doi:10.1016/j.algal.2018.05.019 · Cited by 21 · see citing works
Carrasco-Reinado, R., Escobar-Niño, A., Fajardo, C., Bermejo, I. M. M., Amil‐Ruíz, F., Martı́nez-Rodrı́guez, G., Fuentes-Almagro, C. A., Capilla, V., Tomás‐Cobos, L., Soriano-Romaní, L., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms22010096 · Cited by 21 · see citing works
Mansfeldt, C. B., Richter, L. V., Ahner, B. A., Cochlan, W. P., & Richardson, R. E. (2016) · PLoS ONE · doi:10.1371/journal.pone.0147527 · Cited by 20 · see citing works
Korozi, E., Tsagou, V., Kefalogianni, I., Μάρκου, Γ., Antonopoulos, D., Chakalis, L., Kotzamanis, Y. P., & Chatzipavlidis, I. (2022) · Microorganisms · doi:10.3390/microorganisms10030541 · Cited by 21 · see citing works
Hirai, K., Hayashi, T., Yuri, H., Sato, A., Tsuzuki, M., & Sato, N. (2016) · Scientific Reports · doi:10.1038/srep25825 · Cited by 20 · see citing works
Membrane Proteomic Insights into the Physiology and Taxonomy of an Oleaginous Green Microalga
Garibay‐Hernández, A., Barkla, B. J., Vera‐Estrella, R., Martı́nez, A., & Pantoja, O. (2016) · PLANT PHYSIOLOGY · doi:10.1104/pp.16.01240 · Cited by 20 · see citing works
Characterization of plant carbon substrate utilization by Auxenochlorella protothecoides
Vogler, B. W., Starkenburg, S. R., Sudasinghe, N. M., Schambach, J., Rollin, J. A., Pattathil, S., & Barry, A. N. (2018) · Algal Research · doi:10.1016/j.algal.2018.07.001 · Cited by 20 · see citing works
Inhibition of glucose assimilation in Auxenochlorella protothecoides by light
Xiao, Y., Guo, J., Zhu, H., Anwar, M., Deng, H., Hu, Z., & Wu, Q. (2020) · Biotechnology for Biofuels · doi:10.1186/s13068-020-01787-9 · Cited by 19 · see citing works
Self-citationFajardo, C., Amil‐Ruíz, F., Fuentes-Almagro, C. A., Donato, M. D., Martı́nez-Rodrı́guez, G., Escobar-Niño, A., Carrasco-Reinado, R., Mancera, J. M., & Fernández‐Acero, F. J. (2019) · Journal of Proteomics · doi:10.1016/j.jprot.2019.103502 · Cited by 18 · see citing works
Huang, Y. Y., Li, P., Huang, Y., Xia, A., Zhu, X., & Liao, Q. (2022) · Journal of Cleaner Production · doi:10.1016/j.jclepro.2022.130453 · Cited by 18 · see citing works
Lipid accumulation of Chlorella sp. TLD6B from the Taklimakan Desert under salt stress
Li, H., Tan, J., Mu, Y., & Gao, J. (2021) · PeerJ · doi:10.7717/peerj.11525 · Cited by 17 · see citing works
Nonato, J. V. A., Carvalho, H. F., Borges, K. L. R., Padilha, L., Maluf, M. P., Fritsche‐Neto, R., & Filho, O. G. (2021) · Euphytica · doi:10.1007/s10681-021-02922-9 · Cited by 17 · see citing works
Stoyneva-Gärtner, M. P., Uzunov, B., & Gärtner, G. (2022) · Cosmetics · doi:10.3390/cosmetics9010011 · Cited by 16 · see citing works
Li, R., Pan, J., Yan, M., Yang, J., & Qin, W. (2019) · International Journal of Phytoremediation · doi:10.1080/15226514.2019.1701982 · Cited by 16 · see citing works
Molecular Tools for Bioengineering Eukaryotic Microalgae
Kumar, A., Perrine, Z., Stroff, C., Postier, B. L., Coury, D. A., Sayre, R. T., & Allnutt, F. C. T. (2016) · Current Biotechnology · doi:10.2174/2211550105666160127002147 · Cited by 15 · see citing works
Zhang, H., Zhao, L., Chen, Y., Zhu, M., Xu, Q., Wu, M., Han, D., & Hu, Q. (2021) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2021.638726 · Cited by 15 · see citing works
Sun, X. K., Shen, J., Bai, F., & Xu, N. (2016) · Marine Genomics · doi:10.1016/j.margen.2016.05.002 · Cited by 15 · see citing works
Uchida, H., Sumimoto, K., Oki, T., Nishii, I., Mizohata, E., Matsunaga, S., & Okada, S. (2018) · Journal of Plant Research · doi:10.1007/s10265-018-1039-4 · Cited by 14 · see citing works
- Authors
- Gao, C., Wang, Y., Shen, Y., Yan, D., He, X., Dai, J., & Wu, Q.
- Affiliations
- China People's Public Security University (CN)
- BGI Group (China) (CN)
- Tsinghua University (CN)
- Corresponding author
- Dai, Junbiao
- Wu, Qingyu
- Venue
- BMC Genomics
- Published
- 2014-07-10
- Volume
- 15
- Issue
- 1
- Pages
- 582-582
- ISSN
- 1471-2164 (ISSN-L)
- PMC
- PMC4111847
- OpenAlex
- W1984532384
- Cited by
- 175
- References
- 65
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 15 · 2023: 10 · 2022: 14 · 2021: 17 · 2020: 16 · 2019: 25 · 2018: 18 · 2017: 16 · 2016: 18 · 2015: 7 · 2014: 5
- FWCI
- 5.06
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- BMC Genomics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China (41030210, 31370282)
- Tsinghua University (2012Z08128)
- Topics
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
- Keywords
- Chlorella protothecoides, lipid accumulation, draft genome sequence, genome size reduction, comparative genomics, heterotrophic growth, autotrophic growth, glucose catabolism, glycolysis, TCA cycle, fatty acid synthesis, Chlorella variabilis
- MeSH terms
- Carbon, Chlorella, Citric Acid Cycle, Energy Metabolism, Glycolysis, Plant Oils, Genome, Plant, Proteome, Metabolic Networks and Pathways, Comparative Genomic Hybridization, Biofuels, Transcriptome
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