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Stabilization of model membranes during drying by compatible solutes involved in the stress tolerance of plants and microorganisms
Open accessAbstract
Many organisms accumulate compatible solutes under environmental stress conditions. Cyanobacteria accumulate compatible solutes in response to increased external salinity, with tolerance increasing from Suc (sucrose) or trehalose to 2-O-(alpha-D-glucopyranosyl)-glycerol and glycinebetaine accumulating species. It is not clear how these different solutes influence salt tolerance. One possible explanation may be a differential ability of these solutes to stabilize membranes under stress conditions. We therefore performed drying experiments with liposomes in the presence of compatible solutes. Suc, trehalose and sorbitol protected liposomes from leakage of a soluble marker and from membrane fusion during drying and rehydration. 2-O-(alpha-D-glucopyranosyl)-glycerol was less effective and glycinebetaine showed hardly any effect. In combination with Suc, the latter two solutes showed improved protection. Lipid-phase transitions are known to contribute to solute leakage from liposomes. We determined phase transitions in dry membranes in the absence or presence of the solutes, using Fourier-transform infrared spectroscopy. The ability of the solutes to decrease the phase transition temperature corresponded closely to their ability to protect the liposomes against solute leakage. All solutes interacted with the phosphate in the lipid headgroups. The magnitude of the shift in the asymmetric P=O stretching vibration correlated closely with the lipid-phase transition temperature. This indicates that the degree of membrane protection afforded by the solutes is mainly determined by their ability to interact with the membrane lipids. However, this is not a determinant of cellular protection against salt stress, as the solutes show a reverse order when ranked with regard to protection against these stresses.
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“There are two strategies that cyanobacteria follow to mitigate the osmotic pressure: first, to pump out ions, especially Na + and Cl -, and second, to produce solutes that are compatible with the cell metabolism [75].”
From Arthrospira platensis as a Feasible Feedstock for Bioethanol Production (2021) · cites this paper as [75]
Citations
Cites
Living with Water Stress: Evolution of Osmolyte Systems
Yancey, P. H., Clark, M. E., Hand, S. C., Bowlus, R. D., & Somero, G. N. (1982) · Science · doi:10.1126/science.7112124 · Cited by 3,724
Small-volume extrusion apparatus for preparation of large, unilamellar vesicles
MacDonald, R. C., MacDonald, R. I., Menco, B. P. M., Takeshita, K., Subbarao, N. K., & Hu, L. (1991) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(91)90295-j · Cited by 1,494
Desiccation tolerance of prokaryotes
Potts, M. (1994) · Microbiological Reviews · doi:10.1128/mr.58.4.755-805.1994 · Cited by 1,382
Use of resonance energy transfer to monitor membrane fusion
Struck, D. K., Hoekstra, D., & Pagano, R. E. (1981) · Biochemistry · doi:10.1021/bi00517a023 · Cited by 1,281
Timasheff, S. N. (1993) · Annual Review of Biophysics and Biomolecular Structure · doi:10.1146/annurev.bb.22.060193.000435 · Cited by 1,119
Chen, T. H. H., & Murata, N. (2002) · Current Opinion in Plant Biology · doi:10.1016/s1369-5266(02)00255-8 · Cited by 992
Stabilization of dry phospholipid bilayers and proteins by sugars
Crowe, J. H., Crowe, L. M., Carpenter, J. F., & Wistrom, C. A. (1987) · Biochemical Journal · doi:10.1042/bj2420001 · Cited by 925
Infrared spectroscopy of biomolecules
Howland, J. L. (1996) · Biochemical Education · doi:10.1016/0307-4412(96)82531-3 · Cited by 799
Het mechanism of the protective action of glycerol against haemolysis by freezing and thawing
Lovelock, J. E. (1953) · Biochimica et Biophysica Acta · doi:10.1016/0006-3002(53)90005-5 · Cited by 651
Blume, A., Huebner, W., & Messner, G. (1988) · Biochemistry · doi:10.1021/bi00421a038 · Cited by 499
Crowe, J. H., Carpenter, J. F., Crowe, L. M., & Anchordoquy, T. J. (1990) · Cryobiology · doi:10.1016/0011-2240(90)90023-w · Cited by 468
Diamant, S., Eliahu, N., Rosenthal, D., & Goloubinoff, P. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m103081200 · Cited by 461
Modes of interaction of cryoprotectants with membrane phospholipids during freezing
Anchordoquy, T. J., Rudolph, A. S., Carpenter, J. F., & Crowe, J. H. (1987) · Cryobiology · doi:10.1016/0011-2240(87)90036-8 · Cited by 450
Papageorgiou, G. C., & Murata, N. (1995) · Photosynthesis Research · doi:10.1007/bf00048597 · Cited by 442
Increased thermal stability of proteins in the presence of naturally occurring osmolytes
Santoro, M. M., Liu, Y., Khan, S. M. A., Hou, L. X., & Bolen, D. W. (1992) · Biochemistry · doi:10.1021/bi00138a006 · Cited by 434
Stability of dry liposomes in sugar glasses
Sun, W. Q., Leopold, A. C., Crowe, L. M., & Crowe, J. H. (1996) · Biophysical Journal · doi:10.1016/s0006-3495(96)79740-0 · Cited by 330
A Fourier-transform infrared spectroscopy study of sugar glasses
Wolkers, W. F., Oliver, A. E., Tablin, F., & Crowe, J. H. (2004) · Carbohydrate Research · doi:10.1016/j.carres.2004.01.016 · Cited by 294
Metabolic engineering of plants for osmotic stress resistance
Nuccio, M. L., Rhodest, D., McNeil, S. D., & Hanson, A. D. (1999) · Current Opinion in Plant Biology · doi:10.1016/s1369-5266(99)80026-0 · Cited by 268
Crowe, J. H., Oliver, A. E., Hoekstra, F. A., & Crowe, L. M. (1997) · Cryobiology · doi:10.1006/cryo.1997.2020 · Cited by 226
Drennan, P. M., Smith, M. T., Goldsworthy, D., & van Staden, J. (1993) · Journal of Plant Physiology · doi:10.1016/s0176-1617(11)81257-5 · Cited by 220
Organic solute accumulation in osmotically stressed cyanobacteria
Reed, R. H., Borowitzka, L. J., Mackay, M. A., Chudek, J. A., Foster, R., Warr, S. R. C., Moore, D. J., & Stewart, W. D. P. (1986) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1986.tb01842.x · Cited by 218
Hincha, D. K., Zuther, E., Hellwege, E. M., & Heyer, A. G. (2002) · Glycobiology · doi:10.1093/glycob/12.2.103 · Cited by 210
Is Vitrification Sufficient to Preserve Liposomes during Freeze-Drying?
Crowe, J. H., Leslie, S., & Crowe, L. M. (1994) · Cryobiology · doi:10.1006/cryo.1994.1043 · Cited by 210
Murata, N., Mohanty, P., Hayashi, H., & Papageorgiou, G. C. (1992) · FEBS Letters · doi:10.1016/0014-5793(92)80376-r · Cited by 206
Hincha, D. K., Zuther, E., & Heyer, A. G. (2003) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(03)00116-0 · Cited by 201
Aspects of the glass transition behaviour of mixtures of carbohydrates of low molecular weight
Orford, P. D., Parker, R., & Ring, S. G. (1990) · Carbohydrate Research · doi:10.1016/0008-6215(90)84102-z · Cited by 201
Is vitrification involved in depression of the phase transition temperature in dry phospholipids?
Crowe, J. H., Hoekstra, F. A., Nguyen, K. H. N., & Crowe, L. M. (1996) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(95)00287-1 · Cited by 198
The unusual sugar composition in leaves of the resurrection plant Myrothamnus flabellifolia
Bianchi, G., Gamba, A., Limiroli, R., Pozzi, N., Elster, R., Salamini, F., & Bartels, D. (1993) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1993.tb00146.x · Cited by 193
Borges, N., Ramos, A., Raven, N. D. H., Sharp, R., & Santos, H. (2002) · Extremophiles · doi:10.1007/s007920100236 · Cited by 191
Microbiology and biogeochemistry of hypersaline environments
Melack, J. M. (1999) · Limnology and Oceanography · doi:10.4319/lo.1999.44.6.1597a · Cited by 179
Cayley, S., & Record, M. T. (2003) · Biochemistry · doi:10.1021/bi0347297 · Cited by 169
High-pressure infrared spectroscopic evidence of water binding sites in 1,2-diacyl phospholipids
Wong, P. T. T., & Mantsch, H. H. (1988) · Chemistry and Physics of Lipids · doi:10.1016/0009-3084(88)90024-2 · Cited by 161
Plant fructans stabilize phosphatidylcholine liposomes during freeze‐drying
Hincha, D. K., Hellwege, E. M., Heyer, A. G., & Crowe, J. H. (2000) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.2000.01028.x · Cited by 152
A New Mechanism of Model Membrane Fusion Determined from Monte Carlo Simulation
Müller, M., Katsov, K., & Michael Schick, C. (2003) · Biophysical Journal · doi:10.1016/s0006-3495(03)74592-5 · Cited by 151
The structure and organization of phospholipid bilayers as revealed by infrared spectroscopy
Lewis, R. N. A. H., & McElhaney, R. N. (1998) · Chemistry and Physics of Lipids · doi:10.1016/s0009-3084(98)00077-2 · Cited by 151
High Critical Temperature above Tg May Contribute to the Stability of Biological Systems
Buitink, J., van den Dries, I. J., Hoekstra, F. A., Alberda, M., & Hemminga, M. A. (2000) · Biophysical Journal · doi:10.1016/s0006-3495(00)76365-x · Cited by 151
Oliver, A. E., Crowe, L. M., & Crowe, J. H. (1998) · Seed Science Research · doi:10.1017/s0960258500004128 · Cited by 123
Popova, A. V., & Hincha, D. K. (2003) · Biophysical Journal · doi:10.1016/s0006-3495(03)74598-6 · Cited by 113
Glucosylglycerol, a Compatible Solute, Sustains Cell Division under Salt Stress
Ferjani, A., Mustárdy, L., Ronan Sulpice, A., Marin, K., Suzuki, I., Hagemann, M., & Murata, N. (2003) · PLANT PHYSIOLOGY · doi:10.1104/pp.102.017277 · Cited by 112
Non-Disaccharide-Based Mechanisms of Protection during Drying
Oliver, A. E., Leprince, O., Wolkers, W. F., Hincha, D. K., Heyer, A. G., & Crowe, J. H. (2001) · Cryobiology · doi:10.1006/cryo.2001.2359 · Cited by 108
Accumulation of Trehalose and Sucrose in Cyanobacteria Exposed to Matric Water Stress
Hershkovitz, N., Oren, A., & Cohen, Y. (1991) · Applied and Environmental Microbiology · doi:10.1128/aem.57.3.645-648.1991 · Cited by 104
Tsvetkova, N. M., Phillips, B. L., Crowe, L. M., Crowe, J. H., & Risbud, S. H. (1998) · Biophysical Journal · doi:10.1016/s0006-3495(98)77736-7 · Cited by 103
Eastmond, P. J. (2004) · The Plant Journal · doi:10.1111/j.1365-313x.2003.01989.x · Cited by 92
Oliver, A. E., Hincha, D. K., & Crowe, J. H. (2002) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/s1095-6433(01)00514-1 · Cited by 83
Iturriaga, G., Gaff, D. F., & Zentella, R. (2000) · Australian Journal of Botany · doi:10.1071/bt98062 · Cited by 83
Membrane Permeability Changes at Early Stages of Influenza Hemagglutinin-Mediated Fusion
Frolov, V. A., Dunina-Barkovskaya, A. Y., Samsonov, A. V., & Zimmerberg, J. J. (2003) · Biophysical Journal · doi:10.1016/s0006-3495(03)74602-5 · Cited by 78
Mikkat, S., Hagemann, M., & Schoor, A. (1996) · Microbiology · doi:10.1099/13500872-142-7-1725 · Cited by 71
Santarius, K. A. (1992) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1992.tb08769.x · Cited by 68
The effects of chloroplast lipids on the stability of liposomes during freezing and drying
Hincha, D. K., Oliver, A. E., & Crowe, J. H. (1998) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(97)00204-6 · Cited by 61
Angell, C. A., Stell, R. C., & Sichina, W. (1982) · The Journal of Physical Chemistry · doi:10.1021/j100206a015 · Cited by 60
Interactions of arbutin with dry and hydrated bilayers
Oliver, A. E., Hincha, D. K., Crowe, L. M., & Crowe, J. H. (1998) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(97)00246-0 · Cited by 53
Adapting to Water Stress: Convergence on Common Solutions
Somero, G. N. (1992) · Springer eBooks · doi:10.1007/978-3-642-76682-4_1 · Cited by 42
Hincha, D. K., Heber, U., & Schmitt, J. M. (1985) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/0005-2728(85)90183-5 · Cited by 42
Moore, D. J., Reed, R. H., & Stewart, W. D. P. (1987) · Archives of Microbiology · doi:10.1007/bf00406140 · Cited by 42
Freezing of isolated thylakoid membranes in complex media
Santarius, K. A. (1986) · Cryobiology · doi:10.1016/0011-2240(86)90008-8 · Cited by 34
Hincha, D. K. (1998) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1998.0866 · Cited by 19
Frequency and time-resolved spectroscopic study of liquid–glass transition in D-sorbitol
Tsujimi, Y., Kobayashi, M., & Yagi, T. (1999) · Physica B Condensed Matter · doi:10.1016/s0921-4526(98)01230-7 · Cited by 8
Tsujimi, Y., Kobayashi, M., Furuta, H., & Yagi, T. (1999) · Journal of Thermal Analysis and Calorimetry · doi:10.1023/a:1010162729842 · Cited by 2
Research works printed but not linked: 3
- Hagemann, 1999, The biochemistry and genetics of the synthesis of osmoprotective compounds in cyanobacteria, 177
- Weinstein, 1984, Self-quenching of carboxyfluorescein fluorescence: uses in studying liposome stability and liposome-cell interaction, 183
- Lewis, 1996, Fourier transform infrared spectroscopy in the study of hydrated lipids and lipid bilayer membranes, 159
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Verslues, P. E., Agarwal, M., Katiyar‐Agarwal, S., Zhu, J., & Zhu, J. (2006) · The Plant Journal · doi:10.1111/j.1365-313x.2005.02593.x · Cited by 1,731
Molecular biology of cyanobacterial salt acclimation
Hagemann, M. (2010) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2010.00234.x · Cited by 518
Fructan and its relationship to abiotic stress tolerance in plants
Livingston, D. P., Hincha, D. K., & Heyer, A. G. (2009) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-0002-x · Cited by 443
Plant fructans in stress environments: emerging concepts and future prospects
Valluru, R., & den Ende, W. V. (2008) · Journal of Experimental Botany · doi:10.1093/jxb/ern164 · Cited by 396
Trehalose As a “Chemical Chaperone”
Crowe, J. H. (2007) · Springer eBooks · doi:10.1007/978-0-387-39975-1_13 · Cited by 316
Metadata
- Authors
- HINCHA, D. K., & HAGEMANN, M.
- Affiliations
- Max Planck Institute of Molecular Plant Physiology (DE)
- University of Rostock (DE)
- Venue
- Biochemical Journal
- Publisher
- Portland Press Ltd.
- Published
- 2004-10-08
- Volume
- 383
- Issue
- 2
- Pages
- 277-283
- ISSN
- 0264-6021 (ISSN-L)
- 1470-8728
- PMC
- PMC1134068
- OpenAlex
- W1969189325
- Cited by
- 205
- References
- 59
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 7 · 2023: 2 · 2022: 7 · 2021: 9 · 2020: 9 · 2019: 5 · 2018: 6 · 2017: 8 · 2016: 12 · 2015: 13 · 2014: 11 · 2013: 9 · 2012: 13
- FWCI
- 3.55
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biochemical Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
- Physical Sciences › Physics and Astronomy › Atomic and Molecular Physics, and Optics › Spectroscopy and Quantum Chemical Studies
- Keywords
- osmolytes, membrane stabilization, salt tolerance, betaine, trehalose, sucrose, sorbitol, lipid phase transition, membrane hydration, solute leakage, cyanobacteria
- MeSH terms
- Cyanobacteria, Betaine, Desiccation, Glucosides, Hydrogen Bonding, Liposomes, Microbiology, Plant Diseases, Plants, Salts, Spectroscopy, Fourier Transform Infrared, Plant Cells
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