Cited by 321Algal biology and biofuel productionMicrobial Metabolic Engineering and BioproductionLipid metabolism and biosynthesis

The DOI matches its Crossref record; 51 of the 51 references it cites were found in a registry or an index.

Genetic improvement of the microalga Phaeodactylum tricornutum for boosting neutral lipid accumulation

Open access

Xue, Jiao, Niu, Ying-Fang, Huang, Tan, Yang, Wei-Dong, Liu, Jie-Sheng, Li, Hong-Ye·2015·Metabolic Engineering

DOI 10.1016/j.ymben.2014.10.002

Open this paper in CoChat — free account Open PDF

Abstract

To obtain fast growing oil-rich microalgal strains has been urgently demanded for microalgal biofuel. Malic enzyme (ME), which is involved in pyruvate metabolism and carbon fixation, was first characterized in microalgae here. Overexpression of Phaeodactylum tricornutum ME (PtME) significantly enhanced the expression of PtME and its enzymatic activity in transgenic P. tricornutum. The total lipid content in transgenic cells markedly increased by 2.5-fold and reached a record 57.8% of dry cell weight with a similar growth rate to wild type, thus keeping a high biomass. The neutral lipid content was further increased by 31% under nitrogen-deprivation treatment, still 66% higher than that of wild type. Transgenic microalgae cells exhibited obvious morphological changes, as the cells were shorter and thicker and contained larger oil bodies. Immuno-electron microscopy targeted PtME to the mitochondrion. This study markedly increased the oil content in microalgae, suggesting a new route for developing ideal microalgal strains for industrial biodiesel production.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1016/j.ymben.2014.10.002

Cites

51 of 51 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0
Tamura, K., Dudley, J. T., Nei, M., & Kumar, S. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm092 · Cited by 28,734
Biodiesel from microalgae
Chisti, Y. (2007) · Biotechnology Advances · doi:10.1016/j.biotechadv.2007.02.001 · Cited by 9,524
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
Subcutaneous and visceral adipose tissue: Structural and functional differences
Ibrahim, M. M. (2010) · Obesity Reviews · doi:10.1111/j.1467-789x.2009.00623.x · Cited by 2,238
The Genome of the Diatom Thalassiosira Pseudonana : Ecology, Evolution, and Metabolism
Armbrust, E. V., Berges, J. A., Bowler, C., Green, B. R., Martínez, D., Putnam, N. H., Zhou, S., Allen, A. E., Apt, K. E., Bechner, M., et al. (2004) · Science · doi:10.1126/science.1101156 · Cited by 2,029
Improved recovery of fatty acid through direct transesterification without prior extraction or purification.
Lepage, G., & ROY, C. C. (1984) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)34457-6 · Cited by 1,028
Challenges in Engineering Microbes for Biofuels Production
Stephanopoulos, G. N. (2007) · Science · doi:10.1126/science.1139612 · Cited by 731
A high throughput Nile red method for quantitative measurement of neutral lipids in microalgae
Chen, W., Zhang, C., Song, L., Sommerfeld, M., & Hu, Q. (2009) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2009.01.001 · Cited by 681
Reciprocal regulation of p53 and malic enzymes modulates metabolism and senescence
Jiang, P., Du, W., Mancuso, A., Wellen, K. E., & Yang, X. (2013) · Nature · doi:10.1038/nature11776 · Cited by 491
Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants
Hibberd, J. M., & Quick, W. P. (2002) · Nature · doi:10.1038/415451a · Cited by 420
The pathways of glutamate and glutamine oxidation by tumor cell mitochondria. Role of mitochondrial NAD(P)+-dependent malic enzyme.
Moreadith, R. W., & Lehninger, A. L. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(20)82128-0 · Cited by 415
Metabolic engineering of Saccharomyces cerevisiae for production of fatty acid-derived biofuels and chemicals
Runguphan, W., & Keasling, J. D. (2013) · Metabolic Engineering · doi:10.1016/j.ymben.2013.07.003 · Cited by 413
Molecular and cellular mechanisms of neutral lipid accumulation in diatom following nitrogen deprivation
Yang, Z.-K., Niu, Y., Ma, Y.-H., Xue, J., Zhang, M.-H., Yang, W.-D., Liu, J.-S., Lu, S.-H., Guan, Y., & Li, H. (2013) · Biotechnology for Biofuels · doi:10.1186/1754-6834-6-67 · Cited by 366
Self-citation
Molecular toolbox for studying diatom biology in Phaeodactylum tricornutum
Siaut, M., Heijde, M., Mangogna, M., Montsant, A., Coesel, S., Allen, A. E., Manfredonia, A., Falciatore, A., & Bowler, C. (2007) · Gene · doi:10.1016/j.gene.2007.05.022 · Cited by 345
Metabolic engineering of Phaeodactylum tricornutum for the enhanced accumulation of omega-3 long chain polyunsaturated fatty acids
Hamilton, M. L., Haslam, R. P., Napier, J. A., & Sayanova, O. V. (2013) · Metabolic Engineering · doi:10.1016/j.ymben.2013.12.003 · Cited by 316
Trophic Conversion of an Obligate Photoautotrophic Organism Through Metabolic Engineering
Zaslavskaia, L. A., Lippmeier, J. C., Shih, C., Ehrhardt, D., Grossman, A. R., & Apt, K. E. (2001) · Science · doi:10.1126/science.160015 · Cited by 307
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
Zhang, Y., Adams, I. P., & Ratledge, C. (2007) · Microbiology · doi:10.1099/mic.0.2006/002683-0 · Cited by 286
Automated Subcellular Location Determination and High-Throughput Microscopy
Glory, E., & Murphy, R. F. (2007) · Developmental Cell · doi:10.1016/j.devcel.2006.12.007 · Cited by 285
Improvement of Neutral Lipid and Polyunsaturated Fatty Acid Biosynthesis by Overexpressing a Type 2 Diacylglycerol Acyltransferase in Marine Diatom Phaeodactylum tricornutum
Niu, Y., Zhang, M., Li, D., Yang, W., Liu, J., Bai, W., & Li, H. (2013) · Marine Drugs · doi:10.3390/md11114558 · Cited by 275
Self-citation
Feasibility of a Mitochondrial Pyruvate Malate Shuttle in Pancreatic Islets
MacDonald, M. J. (1995) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)94588-6 · Cited by 274
Genetic engineering of fatty acid chain length in Phaeodactylum tricornutum
Radakovits, R., Eduafo, P. M., & Posewitz, M. C. (2010) · Metabolic Engineering · doi:10.1016/j.ymben.2010.10.003 · Cited by 264
Structure and Function of Malic Enzymes, A New Class of Oxidative Decarboxylases
Chang, G., & Tong, L. (2003) · Biochemistry · doi:10.1021/bi035251+ · Cited by 235
The role of malic enzyme in the regulation of lipid accumulation in filamentous fungi
Wynn, J. P., Hamid, A. A., & Ratledge, C. (1999) · Microbiology · doi:10.1099/13500872-145-8-1911 · Cited by 220
NADP‐malic enzyme from plants: a ubiquitous enzyme involved in different metabolic pathways
Drincovich, M. F., Casati, P., & Andreo, C. S. (2001) · FEBS Letters · doi:10.1016/s0014-5793(00)02331-0 · Cited by 209
Anaplerosis of the citric acid cycle: role in energy metabolism of heart and skeletal muscle
Gibala, M. J., Young, M. E., & Taegtmeyer, H. (2000) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.2000.00717.x · Cited by 180
Cytosolic and Mitochondrial Malic Enzyme Isoforms Differentially Control Insulin Secretion
Pongratz, R. L., Kibbey, R. G., Shulman, G. I., & Cline, G. W. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m602954200 · Cited by 156
Rapid screening method for lipid production in alga based on Nile red fluorescence
Huang, G.-H., Chen, G., & Chen, F. (2009) · Biomass and Bioenergy · doi:10.1016/j.biombioe.2009.05.022 · Cited by 147
Desaturation of polyunsaturated fatty acids in Mucor circinelloides and the involvement of a novel membrane‐bound malic enzyme
Kendrick, A., & Ratledge, C. (1992) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1992.tb17334.x · Cited by 145
Efficient free fatty acid production in Escherichia coli using plant acyl-ACP thioesterases
Zhang, X., Li, M., Agrawal, A., & San, K. (2011) · Metabolic Engineering · doi:10.1016/j.ymben.2011.09.007 · Cited by 141
Metabolic engineering of omega-3 long-chain polyunsaturated fatty acids in plants using an acyl-CoA Δ6-desaturase with ω3-preference from the marine microalga Micromonas pusilla
Petrie, J. R., Shrestha, P., Mansour, M. P., Nichols, P. D., Liu, Q., & Singh, S. P. (2010) · Metabolic Engineering · doi:10.1016/j.ymben.2009.12.001 · Cited by 132
Ethylene- and pathogen-inducible Arabidopsis acyl-CoA-binding protein 4 interacts with an ethylene-responsive element binding protein
Li, H., Xiao, S., & Chye, M. (2008) · Journal of Experimental Botany · doi:10.1093/jxb/ern241 · Cited by 115
Self-citation
High Level Expression of C4-Specific NADP-Malic Enzyme in Leaves and Impairment of Photoautotrophic Growth in a C3 Plant, Rice
Tsuchida, H., Tamai, T., Fukayama, H., Agarie, S., Nomura, M., Onodera, H., Ono, K., Nishizawa, Y., Lee, B.-H., Hirose, S., et al. (2001) · Plant and Cell Physiology · doi:10.1093/pcp/pce013 · Cited by 114
Reconstitution of EPA and DHA biosynthesis in Arabidopsis: Iterative metabolic engineering for the synthesis of n−3 LC-PUFAs in transgenic plants
Ruiz‐López, N., Haslam, R. P., Usher, S. L., Napier, J. A., & Sayanova, O. V. (2013) · Metabolic Engineering · doi:10.1016/j.ymben.2013.03.001 · Cited by 104
Malic Enzyme is a Major Source of NADPH for Lipid Accumulation by Aspergillus Nidulans
Wynn, J. P., & Ratledge, C. (1997) · Microbiology · doi:10.1099/00221287-143-1-253 · Cited by 103
Transformation of Diatom Phaeodactylum Tricornutum by Electroporation and Establishment of Inducible Selection Marker
Niu, Y., Yang, Z.-K., Zhang, M., Zhu, C.-C., Yang, W., Liu, J., & Li, H. (2012) · BioTechniques · doi:10.2144/000113881 · Cited by 96
Self-citation
Evidence that the rate-limiting step for the biosynthesis of arachidonic acid in Mortierella alpina is at the level of the 18:3 to 20:3 elongase
Wynn, J. P., & Ratledge, C. (2000) · Microbiology · doi:10.1099/00221287-146-9-2325 · Cited by 92
Overexpression of malic enzyme (ME) of Mucor circinelloides improved lipid accumulation in engineered Rhodotorula glutinis
Li, Z., Sun, H., Mo, X., Li, X., Xu, B., & Tian, P. (2012) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-012-4571-5 · Cited by 91
Biochemical and Genetic Engineering of Diatoms for Polyunsaturated Fatty Acid Biosynthesis
Li, H., Yang, L., Zheng, J.-W., Yang, W., & Liu, J. (2014) · Marine Drugs · doi:10.3390/md12010153 · Cited by 83
Self-citation
Construction of Novel Chloroplast Expression Vector and Development of an Efficient Transformation System for the Diatom Phaeodactylum tricornutum
Xie, W., Zhu, C.-C., Zhang, N., Li, D., Yang, W., Liu, J., Ramalingam, S., & Li, H. (2014) · Marine Biotechnology · doi:10.1007/s10126-014-9570-3 · Cited by 82
Self-citation
Cloning and analysis of the C4 photosynthetic NAD-dependent malic enzyme of amaranth mitochondria.
Long, J. J., Wang, J. L., & Berry, J. O. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)42017-5 · Cited by 76
Molecular Mechanism for the Regulation of Human Mitochondrial NAD(P)+-Dependent Malic Enzyme by ATP and Fumarate
Yang, Z., Lanks, C. W., & Tong, L. (2002) · Structure · doi:10.1016/s0969-2126(02)00788-8 · Cited by 69
Increasing fatty acid production in E. coli by simulating the lipid accumulation of oleaginous microorganisms
Meng, X., Yang, J., Cao, Y., Li, L., Jiang, X., Xu, X., Liu, W., Xian, M., & Zhang, Y. (2010) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-010-0861-z · Cited by 63
Distinct But Conserved Functions for Two Chloroplastic NADP-Malic Enzyme Isoforms in C3 and C4Flaveria Species
Lai, L. B. (2002) · PLANT PHYSIOLOGY · doi:10.1104/pp.128.1.125 · Cited by 60
Cytosolic Malic Enzyme 1 (ME1) Mediates High Fat Diet-Induced Adiposity, Endocrine Profile, and Gastrointestinal Tract Proliferation-Associated Biomarkers in Male Mice
Al‐Dwairi, A., Pabona, J. M. P., Simmen, R. C. M., & Simmen, F. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046716 · Cited by 59
Differential Regulation of Transcripts Encoding Cytosolic NADP-Malic Enzyme in C3 and C4Flaveria Species
Lai, L. B. (2002) · PLANT PHYSIOLOGY · doi:10.1104/pp.128.1.140 · Cited by 56
Molecular analysis of the malic enzyme gene (mae2) of Schizosaccharomyces pombe
Viljoen‐Bloom, M., Subden, R. E., Krizus, A., & Vuuren, H. J. J. V. (1994) · Yeast · doi:10.1002/yea.320100506 · Cited by 39
Short Communication Differential expression analysis of porcine MDH1, MDH2 and ME1 genes in adipose tissues
Zhou, S., Li, M., Li, Q. H., Guan, J., & Li, X. W. (2012) · Genetics and Molecular Research · doi:10.4238/2012.may.9.4 · Cited by 31
Early Soy Exposure via Maternal Diet Regulates Rat Mammary Epithelial Differentiation by Paracrine Signaling from Stromal Adipocytes
Su, Y., Shankar, K., & Simmen, R. C. M. (2009) · Journal of Nutrition · doi:10.3945/jn.108.103820 · Cited by 30
Annotation and analysis of malic enzyme genes encoding for multiple isoforms in the fungus Mucor circinelloides CBS 277.49
Vongsangnak, W., Zhang, Y., Chen, W., Ratledge, C., & Song, Y. (2012) · Biotechnology Letters · doi:10.1007/s10529-012-0859-x · Cited by 23
Improved recovery of fatty acid through direct
Lepage, G., & ROY, C. C. (1984) · Cited by 5
Subcellular Localization of Oxaloacetate Decarboxylase and Its Isolation from Maize Leaves
Trukhina, Y. O., Metalnikova, E. A., Popov, V. N., & Eprintsev, A. T. (2002) · Russian Journal of Plant Physiology · doi:10.1023/a:1020236901557 · Cited by 2

Sorted by citations

The lipid biochemistry of eukaryotic algae
Li-Beisson, Y., Thelen, J. J., Fedosejevs, E., & Harwood, J. L. (2019) · Progress in Lipid Research · doi:10.1016/j.plipres.2019.01.003 · Cited by 453
Lipid Production from Nannochloropsis
Ma, X.-N., Chen, T.-P., Yang, B., Liu, J., & Chen, F. (2016) · Marine Drugs · doi:10.3390/md14040061 · Cited by 394
Self-citation
An Overview of Potential Oleaginous Microorganisms and Their Role in Biodiesel and Omega-3 Fatty Acid-Based Industries
Patel, A., Karageorgou, D., Rova, E., Katapodis, P., Rova, U., Christakopoulos, P., & Μάτσακας, Λ. (2020) · Microorganisms · doi:10.3390/microorganisms8030434 · Cited by 342
Microbial oils as food additives: recent approaches for improving microbial oil production and its polyunsaturated fatty acid content
Bellou, S., Triantaphyllidou, I., Aggeli, D., Elazzazy, A. M., Baeshen, M. N., & Aggelis, G. (2015) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2015.09.005 · Cited by 323
Trends and novel strategies for enhancing lipid accumulation and quality in microalgae
Singh, P., Kumari, S., Guldhe, A., Misra, R., Rawat, I., & Bux, F. (2016) · Renewable and Sustainable Energy Reviews · doi:10.1016/j.rser.2015.11.001 · Cited by 309

See all 321

Authors: Xue, J., Niu, Y.-F., Huang, T., Yang, W.-D., Liu, J.-S., & Li, H.-Y.
Affiliations: Jinan University (CN)
ORCID: Xue, Jiao
Niu, Ying-Fang
Yang, Wei-Dong
Li, Hong-Ye
Venue: Metabolic Engineering
Publisher: Elsevier BV
Published: 2015-01
Volume: 27
Pages: 1-9
ISSN: 1096-7176 (ISSN-L)
DOI: 10.1016/j.ymben.2014.10.002
OpenAlex: W1986227133
Cited by: 321
References: 51
Citations by year: 2026: 12 · 2025: 20 · 2024: 22 · 2023: 31 · 2022: 30 · 2021: 41 · 2020: 34 · 2019: 36 · 2018: 26 · 2017: 27 · 2016: 29 · 2015: 13
FWCI: 7.59
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
creativecommons.org/licenses/by-nc-sa/3.0/ (vor)
Locations: Metabolic Engineering (publishedVersion, cc-by-nc-sa)
PubMed (publishedVersion)
Funders: National Science and Technology Support Program (2011BAD14B03)
Science and Technology Project of Guangdong (2009B050600005, 2010B030600005)
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: Phaeodactylum tricornutum, malic enzyme, neutral lipid accumulation, transgenic microalgae, nitrogen starvation, oil bodies, mitochondrial targeting, pyruvate metabolism, CO2 fixation, microalgae biodiesel, genetic improvement
MeSH terms: Genetic Engineering, Malate Dehydrogenase, Gene Expression, Diatoms, Algal Proteins, Organisms, Genetically Modified, Lipid Metabolism

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Genetic improvement of the microalga Phaeodactylum tricornutum for boosting neutral lipid accumulation

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks