Lipid Droplets Mediate Salt Stress Tolerance in Parachlorella kessleri 1
Open accessAbstract
Microalgae are known to respond to salinity stress via mechanisms that include accumulation of compatible solutes and synthesis of antioxidants. Here, we describe a salinity-tolerance mechanism mediated by lipid droplets (LDs). In the alga Parachlorella kessleri grown under salt-stress conditions, we observed significant increases in cell size and LD content. LDs that were closely grouped along the plasma membrane shrank as the plasma membrane expanded, and some LDs were engulfed by vacuoles. Transcriptome analysis showed that genes encoding lysophospholipid acyltransferases (LPLATs) and phospholipase A2 were significantly up-regulated following salt stress. Diacylglycerol kinase and LPLAT were identified in the proteome of salt-induced LDs, alongside vesicle trafficking and plastidial proteins and histone H2B. Analysis of fatty acid composition revealed an enrichment of C18:1 and C18:2 at the expense of C18:3 in response to salt stress. Pulse-chase experiments further suggested that variations of fatty acid composition were associated with LDs. Acetate stimulation research further confirmed a positive role of LDs in cell growth under salt stress. These results suggest that LDs play important roles in salt-stress tolerance, through harboring proteins, participating in cytoplasmic component recycling, and providing materials and enzymes for membrane modification and expansion.
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
Cites
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?
Saline stress not only increases the lipid content but also causes changes in the fatty acid profile.
“Moreover, saline stress not only increases the lipid content but also causes changes in the FAs profile [131, 132].”
From Microalgae biofuels: illuminating the path to a sustainable future amidst challenges and opportunities (2024) · cites this paper as [131]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302 · see citing works
Colorimetric Method for Determination of Sugars and Related Substances
DuBois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., & Smith, F. (1956) · Analytical Chemistry · doi:10.1021/ac60111a017 · Cited by 52,269 · see citing works
ASCORBATE AND GLUTATHIONE: Keeping Active Oxygen Under Control
Noctor, G., & Foyer, C. H. (1998) · Annual Review of Plant Physiology and Plant Molecular Biology · doi:10.1146/annurev.arplant.49.1.249 · Cited by 5,722 · see citing works
Valuable Products from Biotechnology of Microalgae
Pulz, O., & Gross, W. (2004) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-004-1647-x · Cited by 2,132 · see citing works
Rambold, A. S., Cohen, S., & Lippincott-Schwartz, J. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.01.029 · Cited by 1,038 · see citing works
Tang, D., Han, W., Li, P., Miao, X., & Zhong, J. (2010) · Bioresource Technology · doi:10.1016/j.biortech.2010.10.047 · Cited by 845 · see citing works
Self-citationSiaut, M., Cuiné, S., Cagnon, C., Fessler, B., Nguyen, H. M., Carrier, P., Beyly, A., Beisson, F., Triantaphylidès, C., Li‐Beisson, Y., et al. (2011) · BMC Biotechnology · doi:10.1186/1472-6750-11-7 · Cited by 754 · see citing works
Graham, I. A. (2008) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.59.032607.092938 · Cited by 735 · see citing works
Constraints to Commercialization of Algal Fuels
Chisti, Y. (2013) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2013.07.020 · Cited by 719 · see citing works
C HLAMYDOMONAS AS A M ODEL O RGANISM
Harris, E. H. (2001) · Annual Review of Plant Physiology and Plant Molecular Biology · doi:10.1146/annurev.arplant.52.1.363 · Cited by 711 · see citing works
Antioxidant Role for Lipid Droplets in a Stem Cell Niche of Drosophila
Bailey, A. P., Koster, G., Guillermier, C., Hirst, E. M. A., MacRae, J. I., Lechène, C., Postle, A. D., & Gould, A. P. (2015) · Cell · doi:10.1016/j.cell.2015.09.020 · Cited by 689 · see citing works
Harnessing Yarrowia lipolytica lipogenesis to create a platform for lipid and biofuel production
Blazeck, J., Hill, A. D., Liu, L., Knight, R., Miller, J., Pan, A., Otoupal, P. B., & Alper, H. S. (2014) · Nature Communications · doi:10.1038/ncomms4131 · Cited by 587 · see citing works
Lipid droplet functions beyond energy storage
Welte, M. A., & Gould, A. P. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2017.07.006 · Cited by 574 · see citing works
Molecular biology of cyanobacterial salt acclimation
Hagemann, M. (2010) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2010.00234.x · Cited by 510 · see citing works
Lipids and membrane function in green algae
Thompson, G. A. (1996) · Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism · doi:10.1016/0005-2760(96)00045-8 · Cited by 506 · see citing works
Lipidomics reveals that adiposomes store ether lipids and mediate phospholipid traffic,
Bartz, R., Li, W.-H., Venables, B. J., Zehmer, J. K., Roth, M. R., Welti, R., Anderson, R. G. W., Liu, P., & Chapman, K. D. (2007) · Journal of Lipid Research · doi:10.1194/jlr.m600413-jlr200 · Cited by 488 · see citing works
(2016) · doi:10.1007/978-3-319-24945-2 · Cited by 487 · see citing works
Eastmond, P. J. (2006) · The Plant Cell · doi:10.1105/tpc.105.040543 · Cited by 484 · see citing works
The Lipid-Droplet Proteome Reveals that Droplets Are a Protein-Storage Depot
Cermelli, S., Guo, Y., Gross, S. P., & Welte, M. A. (2006) · Current Biology · doi:10.1016/j.cub.2006.07.062 · Cited by 483 · see citing works
Acyl-CoA:Lysophospholipid Acyltransferases
Shindou, H., & Shimizu, T. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.r800046200 · Cited by 478 · see citing works
METABOLISM OF GLYCEROLIPIDES: A COMPARISON OF LECITHIN AND TRIGLYCERIDE SYNTHESIS
Lands, W. E. M. (1958) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)70453-5 · Cited by 476 · see citing works
Moellering, E. R., & Christoph Benning, A. (2009) · Eukaryotic Cell · doi:10.1128/ec.00203-09 · Cited by 401 · see citing works
The dynamic roles of intracellular lipid droplets: from archaea to mammals
Murphy, D. J. (2011) · PROTOPLASMA · doi:10.1007/s00709-011-0329-7 · Cited by 392 · see citing works
Sustainable biofuels from algae
Borowitzka, M. A., & Moheimani, N. R. (2013) · Mitigation and Adaptation Strategies for Global Change · doi:10.1007/s11027-010-9271-9 · Cited by 374 · see citing works
Autophagy Plays a Role in Chloroplast Degradation during Senescence in Individually Darkened Leaves
Wada, S., Ishida, H., Izumi, M., Yoshimoto, K., Ohsumi, Y., Mae, T., & Makino, A. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.108.130013 · Cited by 357 · see citing works
Ishida, H., Yoshimoto, K., Izumi, M., Reisen, D., Yano, Y., Makino, A., Ohsumi, Y., Hanson, M. R., & Mae, T. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.108.122770 · Cited by 356 · 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
The small GTPase Rab7 as a central regulator of hepatocellular lipophagy
Schroeder, B., Schulze, R. J., Weller, S. G., Sletten, A. C., Casey, C. A., & McNiven, M. A. (2015) · Hepatology · doi:10.1002/hep.27667 · Cited by 330 · 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
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
GENETIC TRANSFORMATION OF THE DIATOMS <i>CYCLOTELLA CRYPTICA</i> AND <i>NAVICULA SAPROPHILA</i>
Dunahay, T. G., Jarvis, E. E., & Roessler, P. G. (1995) · Journal of Phycology · doi:10.1111/j.0022-3646.1995.01004.x · Cited by 306 · see citing works
Yamashita, A., Sugiura, T., & Waku, K. (1997) · The Journal of Biochemistry · doi:10.1093/oxfordjournals.jbchem.a021715 · Cited by 302 · see citing works
Wältermann, M., & Steinbüchel, A. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.11.3607-3619.2005 · Cited by 297 · see citing works
Plant Lipid Droplets and Their Associated Proteins: Potential for Rapid Advances
Huang, A. H. C. (2017) · PLANT PHYSIOLOGY · doi:10.1104/pp.17.01677 · Cited by 287 · see citing works
Structure, function and biogenesis of storage lipid bodies and oleosins in plants
Murphy, D. J. (1993) · Progress in Lipid Research · doi:10.1016/0163-7827(93)90009-l · Cited by 272 · see citing works
Goodson, C. M., Roth, R. A., Wang, Z. T., & Goodenough, U. W. (2011) · Eukaryotic Cell · doi:10.1128/ec.05242-11 · Cited by 252 · see citing works
Lipid Droplets Control the Maternal Histone Supply of Drosophila Embryos
Li, Z., Thiel, K., Thul, P. J., Beller, M., Kühnlein, R. P., & Welte, M. A. (2012) · Current Biology · doi:10.1016/j.cub.2012.09.018 · Cited by 221 · see citing works
Nguyen, H. M., Baudet, M., Cuiné, S., Adriano, J.-M., Barthe, D., Billon, E., Bruley, C., Beisson, F., Peltier, G., Ferro, M., et al. (2011) · PROTEOMICS · doi:10.1002/pmic.201100114 · Cited by 219 · see citing works
Rodríguez‐Vargas, S., Sánchez‐García, A., Martínez‐Rivas, J. M., Prieto, J. A., & Rández‐Gil, F. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.01360-06 · Cited by 215 · see citing works
Rismani‐Yazdi, H., HAZNEDAROĞLU, B. Z., Hsin, C., & Peccia, J. (2012) · Biotechnology for Biofuels · doi:10.1186/1754-6834-5-74 · Cited by 213 · see citing works
Proteins under new management: lipid droplets deliver
Welte, M. A. (2007) · Trends in Cell Biology · doi:10.1016/j.tcb.2007.06.004 · Cited by 209 · see citing works
Cell-to-Cell Heterogeneity in Lipid Droplets Suggests a Mechanism to Reduce Lipotoxicity
Herms, A., Bosch, M., Ariotti, N., Reddy, B. J. N., Fajardo, A., Fernández‐Vidal, A., Álvarez-Guaita, A., Fernandez-Rojo, M. A., Rentero, C., Tebar, F., et al. (2013) · Current Biology · doi:10.1016/j.cub.2013.06.032 · Cited by 193 · see citing works
Lands, W. E. M. (2000) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/s1388-1981(99)00177-8 · Cited by 172 · see citing works
Effective acid-catalyzed transesterification for biodiesel production
Miao, X., Li, R., & Yao, H. (2009) · Energy Conversion and Management · doi:10.1016/j.enconman.2009.06.021 · Cited by 169 · see citing works
Self-citationTan, K. W. M., & Lee, Y. K. (2016) · Biotechnology for Biofuels · doi:10.1186/s13068-016-0671-2 · Cited by 166 · see citing works
Moessinger, C., Klizaite, K., Steinhagen, A., Philippou‐Massier, J., Shevchenko, A., Hoch, M., Ejsing, C. S., & Thiele, C. (2014) · BMC Cell Biology · doi:10.1186/s12860-014-0043-3 · Cited by 151 · see citing works
Martin, G. J. O., Hill, D. R., Olmstead, I. L. D., Amanda, B., Shears, M. J., Dias, D. A., Kentish, S. E., Scales, P. J., Botté, C. Y., & Callahan, D. L. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103389 · Cited by 149 · see citing works
Bišová, K., Krylov, D. M., & Umen, J. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.104.054155 · Cited by 140 · see citing works
Zhu, M. (2002) · Bioresource Technology · doi:10.1016/s0960-8524(02)00028-7 · Cited by 139 · see citing works
Lizaso, A., Tan, K. T., & Lee, Y. (2013) · Autophagy · doi:10.4161/auto.24893 · Cited by 128 · see citing works
Evolution of salt tolerance in a laboratory reared population of C hlamydomonas reinhardtii
Perrineau, M., Zelzion, E., Gross, J., Price, D. C., Boyd, J. M., & Bhattacharya, D. (2013) · Environmental Microbiology · doi:10.1111/1462-2920.12372 · Cited by 118 · see citing works
Cytosolic phospholipase A2: Biochemical properties and physiological roles
Shimizu, T., Ohto, T., & Kita, Y. (2006) · IUBMB Life · doi:10.1080/15216540600702289 · Cited by 105 · see citing works
Enhanced lipid productivity approaches in microalgae as an alternate for fossil fuels – A review
Sibi, G., Shetty, V., & Mokashi, K. (2016) · Journal of the Energy Institute · doi:10.1016/j.joei.2015.03.008 · Cited by 98 · see citing works
Mastrobuoni, G., Irgang, S., Pietzke, M., Assmus, H. E., Wenzel, M., Schulze, W. X., & Kempa, S. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-215 · Cited by 96 · see citing works
Remodeling of Membrane Lipids in Iron-starved Chlamydomonas
Urzica, E. I., Vieler, A., Hong‐Hermesdorf, A., Page, M. D., Casero, D., Gallaher, S. D., Kropat, J., Pellegrini, M. A., Christoph Benning, A., & Merchant, S. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.490425 · Cited by 92 · see citing works
Krell, A., Funck, D., Plettner, I., et al. (2007) · Journal of Phycology · doi:10.1111/j.1529-8817.2007.00366.x · Cited by 87 · see citing works
Spontaneous transfer of monoacyl amphiphiles between lipid and protein surfaces
Massey, J. B., Bick, D. H., & Pownall, H. J. (1997) · Biophysical Journal · doi:10.1016/s0006-3495(97)78819-2 · Cited by 82 · see citing works
Bromke, M. A., Giavalisco, P., Willmitzer, L., & Hesse, H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0067340 · Cited by 77 · see citing works
Hakkila, K., Antal, T. K., Rehman, A. U., et al. (2013) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2013.11.011 · Cited by 72 · see citing works
Goold, H. D., Cuiné, S., Légeret, B., Liang, Y., Brugière, S., Auroy, P., Javot, H., Tardif, M., Jones, B., Beisson, F., et al. (2016) · PLANT PHYSIOLOGY · doi:10.1104/pp.16.00718 · Cited by 72 · see citing works
Dibrova, D. V., Galperin, M. Y., & Mulkidjanian, A. Y. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq234 · Cited by 70 · see citing works
Lipid droplet growth: regulation of a dynamic organelle
Barneda, D., & Christian, M. (2017) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2017.02.002 · Cited by 67 · see citing works
Role of the Plasma Membrane in Saline Conditions: Lipids and Proteins
Mansour, M. M. F., Salama, K. H. A., & Allam, H. Y. H. (2015) · The Botanical Review · doi:10.1007/s12229-015-9156-4 · Cited by 65 · see citing works
Lipid droplet‐mediated lipid and protein homeostasis in budding yeast
Graef, M. (2018) · FEBS Letters · doi:10.1002/1873-3468.12996 · Cited by 65 · see citing works
Wang, H., Postier, B. L., & Burnap, R. L. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.02983.x · Cited by 58 · see citing works
Churchward, M. A., Brandman, D. M., Rogasevskaia, T. P., & Coorssen, J. R. (2008) · Journal of Chemical Biology · doi:10.1007/s12154-008-0007-1 · Cited by 56 · see citing works
Hicks, G. R., Hironaka, C. M., Dauvillée, D., Funke, R. P., d’Hulst, C., Waffenschmidt, S., & Ball, S. G. (2001) · PLANT PHYSIOLOGY · doi:10.1104/pp.010821 · Cited by 55 · see citing works
Jolivet, P., Acevedo, F., Boulard, C., et al. (2013) · PROTEOMICS · doi:10.1002/pmic.201200431 · Cited by 54 · see citing works
Rational selection of reverse phase columns for high throughput LC–MS lipidomics
Criscuolo, A., Zeller, M., Cook, K., et al. (2019) · Chemistry and Physics of Lipids · doi:10.1016/j.chemphyslip.2019.03.006 · Cited by 50 · see citing works
The Selective Breeding of the Freshwater Microalga Chlamydomonas reinhardtii for Growth in Salinity
Takouridis, S. J., Tribe, D. E., Gras, S. L., & Martin, G. J. O. (2015) · Bioresource Technology · doi:10.1016/j.biortech.2014.10.120 · Cited by 40 · see citing works
Avidan, O., & Pick, U. (2015) · Journal of Experimental Botany · doi:10.1093/jxb/erv424 · Cited by 37 · see citing works
Yokthongwattana, C., Mahong, B., Roytrakul, S., et al. (2012) · Planta · doi:10.1007/s00425-012-1594-1 · Cited by 34 · see citing works
MAPK Cell-Cycle Regulation in Saccharomyces Cerevisiae and Candida Albicans
Correia, I., Alonso‐Monge, R., & Plá, J. (2010) · Future Microbiology · doi:10.2217/fmb.10.72 · Cited by 33 · see citing works
Waku, K., & Nakazawa, Y. (1972) · The Journal of Biochemistry · doi:10.1093/oxfordjournals.jbchem.a129928 · Cited by 29 · see citing works
Biological Specimen Preparation for Transmission Electron Microscopy
Roomans, G. M. (1999) · Cell Biology International · doi:10.1006/cbir.1999.0409 · Cited by 29 · see citing works
Su, J., Ye, M., Lou, Y., Yang, Z., Sun, T., Zhang, R., Xu, J., Zhou, C., & Yan, X. (2017) · Algal Research · doi:10.1016/j.algal.2017.06.011 · Cited by 23 · see citing works
Kuroiwa, T., Ohnuma, M., Imoto, Y., et al. (2014) · CYTOLOGIA · doi:10.1508/cytologia.79.501 · Cited by 4 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Harris EH. (2001) Chlamydomonas as a model organism. Annu Rev Plant Physiol Plant Mol Biol 52: 363–406 [DOI] [PubMed] [Google Scholar]
Cited by
Sorted by citations
Wang, M., Ye, X., Bi, H., & Shen, Z. (2024) · Biotechnology for Biofuels and Bioproducts · doi:10.1186/s13068-024-02461-0 · Cited by 201 · see citing works
Yu, Z., Hou, Q., Liu, M., Xie, Z., Ma, M., Chen, H., & Pei, H. (2023) · Water Research · doi:10.1016/j.watres.2022.119471 · Cited by 52 · see citing works
Unconventional microalgae species and potential for their use in the food industry
Benavente-Valdés, J. R., Méndez-Zavala, A., Hernández-López, I., Carreón-González, B. A., Velázquez-Arellano, M. E., Morales-Oyervides, L., & Montañez-Saénz, J. C. (2021) · Cultured Microalgae for the Food Industry · doi:10.1016/b978-0-12-821080-2.00010-1 · Cited by 3 · see citing works
- Authors
- You, Z., Zhang, Q., Peng, Z., & Miao, X.
- Affiliations
- Shanghai Jiao Tong University (CN)
- Corresponding author
- Miao, Xiaoling
- Venue
- Plant Physiology
- Publisher
- Oxford University Press (OUP)
- Published
- 2019-07-24
- Volume
- 181
- Issue
- 2
- Pages
- 510-526
- ISSN
- 0032-0889 (ISSN-L)
- 1532-2548
- PMC
- PMC6776852
- OpenAlex
- W2963148454
- Cited by
- 87
- References
- 77
- Citations by year
- 2026: 11 · 2025: 18 · 2024: 14 · 2023: 6 · 2022: 16 · 2021: 13 · 2020: 9
- FWCI
- 3.97
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- PLANT PHYSIOLOGY (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China (41476122)
- National High Technology Research and Development Program (863 Program) of China (2013AA065805)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
- Keywords
- lipid droplets, salt tolerance, Parachlorella kessleri, microalgae, lysophospholipid acyltransferase, phospholipase A2, diacylglycerol kinase, fatty acid composition, membrane expansion, cell growth, membrane modification
- MeSH terms
- Chlorophyta, Fatty Acids, Salt Tolerance, Microalgae, Transcriptome, Lipid Droplets
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
