Regulatory Role of Membrane Fluidity in Gene Expression

  • Dmitry A. LosEmail author
  • Vladislav V. Zinchenko
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 30)


Plants and other photosynthetic organisms experience frequent changes in environment. Their ability to survive depends on their capacity to acclimate to such changes. In particular, fluctuations in temperature and/or osmolarity affect the fluidity of cytoplasmic and thylakoid membranes. The molecular mechanisms responsible for the perception of changes in membrane fluidity have not been fully characterized. However, the analysis of genome-wide gene expression with DNA microarrays has provided a powerful new approach to studies of the contribution of membrane fluidity to gene expression and to the identification of environmental sensors. In this chapter, we summarize the knowledge on the mechanisms that regulate membrane fluidity, on putative sensors that perceive changes in membrane fluidity, and on the subsequent expression of genes that ensures acclimation to a new set of environmental conditions.


Heat Stress Cold Stress Membrane Fluidity Histidine Kinase Glycine Betaine 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.




FTIR spectroscopy

Fourier transform infrared spectroscopy

PAS domain

Per-ARNT-Sim conservative motif


RNA-binding protein


Sterol responsive element


Sterol responsive element binding protein



This work was supported, in part, by grants from the Russian Foundation for Basic Research (nos. 09-04-01074 and 07-04-00117) to Dmitry A. Los and Vladislav V. Zinchenko, and by a grant from the “Molecular and Cell Biology Program” of the Russian Academy of Sciences to Dmitry A. Los.


  1. Aguilar PS and de Mendoza D (2006) Control of fatty acid desaturation: a mechanism conserved from bacteria to humans. Mol Microbiol 62: 1507–1514PubMedCrossRefGoogle Scholar
  2. Aguilar PS, Hernandez-Arriaga AM, Cybulski LE, Erazo AC and de Mendoza D (2001) Molecular basis of thermo-sensing: a two-component signal transduction thermometer in Bacillus subtilis. EMBO J 20: 1681–1691PubMedCrossRefGoogle Scholar
  3. Albanesi D, Mansilla MC and de Mendoza D (2004) The membrane fluidity sensor DesK of Bacillus subtilis controls the signal decay of its cognate response regulator. J Bacteriol 186: 2655–2663PubMedCrossRefGoogle Scholar
  4. Bartsevich VV and Shestakov SV (1995) The dspA gene product of the cyanobacterium Synechocystis sp. strain PCC 6803 influences sensitivity to chemically different growth inhibitors and has amino acid similarity to histi-dine protein kinases. Microbiology 141: 2915–2920PubMedCrossRefGoogle Scholar
  5. Benedict C, Geisler M, Trygg J, Huner N and Hurry V (2006) Consensus by democracy. Using meta-analyses of microarray and genomic data to model the cold acclimation signaling pathway in Arabidopsis. Plant Physiol 141: 1219–1232PubMedCrossRefGoogle Scholar
  6. Blount P and Moe PC (1999) Bacterial mechanosensitive channels: integrating physiology, structure and function. Trends Microbiol 7: 420–424PubMedCrossRefGoogle Scholar
  7. Bossie MA and Martin CE (1989) Nutritional regulation of yeast Δ9 fatty acid desaturase activity. J Bacteriol 171: 6409–6413PubMedGoogle Scholar
  8. Brauchi S, Orta G, Salazar M, Rosenmann E and Latorre R (2006) A hot-sensing cold receptor: C-terminal domain determines thermosensation in transient receptor potential channels. J Neurosci 26: 4835–4840PubMedCrossRefGoogle Scholar
  9. Brown MS and Goldstein JL (1999) A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood. Proc Natl Acad Sci USA 96: 11041–11048PubMedCrossRefGoogle Scholar
  10. Carratu L, Franceschelli S, Pardini CL, Kobayashi GS, Hor-váth I, Vigh L and Maresca B (1996) Membrane lipid perturbation modifies the set point of the temperature of heat shock response in yeast. Proc Natl Acad Sci USA 93: 3870–3875PubMedCrossRefGoogle Scholar
  11. Causton HC, Ren B, Koh SS, Harbison CT, Kanin E, Jennings EG, Lee TI, True HL, Lander ES and Young RA (2001) Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 12: 323–337PubMedGoogle Scholar
  12. Chinnusamy V, Schumaker K and Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55: 225–236PubMedCrossRefGoogle Scholar
  13. Chinnusamy V, Zhu J and Zhu J-K (2006) Gene regulation during cold acclimation in plants. Physiol Plant 126: 52–61CrossRefGoogle Scholar
  14. Cossins AR (1977) Adaptation of biological membranes to temperature. The effect of temperature acclimation of goldfish upon the viscosity of synaptosomal membranes. Biochim Biophys Acta 470: 395–411.PubMedCrossRefGoogle Scholar
  15. Cybulski LE, Mansilla MC, Aguilar PS and de Mendoza D (2002) Mechanism of membrane fluidity optimization: isothermal control of the Bacillus subtilis acyl-lipid desaturase. Mol Microbiol 45: 1379–1388PubMedCrossRefGoogle Scholar
  16. Danese PN and Silhavy TJ (1997) The σE and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli. Genes Dev 11: 1183–1193PubMedCrossRefGoogle Scholar
  17. Danese PN, Snyder WB, Cosma CL, Davis LJ and Silhavy TJ (1995) The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP. Genes Dev 9: 387–398PubMedCrossRefGoogle Scholar
  18. De Wulf P, Akerley BJ and Lin EC (2000) Presence of the Cpx system in bacteria. Microbiology 146: 247–248PubMedGoogle Scholar
  19. DiGiuseppe PA and Silhavy TJ (2003) Signal detection and target gene induction by the CpxRA two-component system. J Bacteriol 185: 2432–2440PubMedCrossRefGoogle Scholar
  20. Edwards PA and Ericsson J (1999) Sterols and isoprenoids: signaling molecules derived from the cholesterol biosyn-thetic pathway. Annu Rev Biochem 68: 157–185PubMedCrossRefGoogle Scholar
  21. Engelbrecht F, Marin K and Hagemann M (1999) Expression of the ggpS gene, involved in osmolyte synthesis in the marine cyanobacterium Synechococcus sp. strain PCC 7002, revealed regulatory differences between this strain and the freshwater strain Synechocystis sp. strain PCC 6803. Appl Environ Microbiol 65: 48220–48229Google Scholar
  22. Fowler S and Thomashow MF (2003) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold-response pathway. Plant Cell 14: 1675–1690Google Scholar
  23. Franklin KA and Whitelam GC (2007) Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nature Genet 39: 1410–1413PubMedCrossRefGoogle Scholar
  24. Gasch AP, Spelman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D and Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241–4257PubMedGoogle Scholar
  25. Glatz A, Vass I, Los DA and Vigh L (1999) The Syne-chocystis model of stress: from molecular chaperones to membranes. Plant Physiol Biochem 37: 1–12CrossRefGoogle Scholar
  26. Godon C, Lagniel G, Lee J, Buhler JM, Kieffer S, Perrot M, Boucherie H, Toledano MB and Labarre J (1998) The H2O2 stimulon in Saccharomyces cerevisiae. J Biol Chem 273: 22480–22489PubMedCrossRefGoogle Scholar
  27. Grunberger D, Haimovitz R and Shinitzky M (1982) Resolution of plasma membrane lipid fluidity in intact cells labeled with diphenylhexatriene. Biochim Biophys Acta 688: 764–774PubMedCrossRefGoogle Scholar
  28. Gudi S, Nolan JP and Frangos JA (1998) Modulation of GTPase activity of G proteins by fluid shear stress and phospholipid composition. Proc Natl Acad Sci USA 95: 2515–2519PubMedCrossRefGoogle Scholar
  29. Hagemann M, Schoor A, Jeanjean R, Zuther E and Joset F (1997) The stpA gene from Synechocystis sp. strain PCC 6803 encodes the glucosylglycerol-phosphate phosphatase involved in cyanobacterial osmotic response to salt shock. J Bacteriol 179: 1727–1733PubMedGoogle Scholar
  30. Hayward SA, Murray PA, Gracey AY and Cossins AR (2007) Beyond the lipid hypothesis: mechanisms underlying phenotypic plasticity in inducible cold tolerance. Adv Exp Med Biol 594: 132–142PubMedCrossRefGoogle Scholar
  31. Hazel JR (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57: 19–42PubMedCrossRefGoogle Scholar
  32. Heipieper HJ, Meinhardt F and Segura A (2003) The cistrans isomerase of unsaturated fatty acids in Pseudomonas and Vibrio: biochemistry, molecular biology and physiological function of a unique stress-adaptive mechanism. FEMS Microbiol Lett 229: 1–7PubMedCrossRefGoogle Scholar
  33. Hihara Y, Kamei A, Kanehisa M, Kaplan A and Ikeuchi M (2001) DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13: 793–806PubMedGoogle Scholar
  34. Hihara Y, Sonoike K, Kanehisa M and Ikeuchi M (2003) DNA microarray analysis of redox-responsive genes in the genome of the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 185: 1719–1725PubMedCrossRefGoogle Scholar
  35. Hohmann S (2003) Osmotic stress signaling and osmoadap-tation in yeasts. Microbiol Mol Biol Rev 66: 300–372CrossRefGoogle Scholar
  36. Horváth I, Glatz A, Varvasovszki V, Török Z, Pali T, Balogh G, Kovacs E, Nadasdi L, Benko S, Joo F and Vigh L (1998) Membrane physical state controls the signaling mechanism of the heat shock response in Synechocystis PCC 6803: identification of hsp17 as a “fluidity gene”. Proc Natl Acad Sci USA 95: 3513–3518PubMedCrossRefGoogle Scholar
  37. Horváth I, Multhoff G, Sonnleitner A and Vígh L (2008) Membrane-associated stress proteins: more than simply chaperones. Biochim Biophys Acta 1778: 1653–1664PubMedCrossRefGoogle Scholar
  38. Inaba M, Suzuki I, Szalontai B, Kanesaki Y, Los DA, Hayashi H and Murata N (2003) Gene-engineered rigidi-fication of membrane lipids enhances the cold inducibility of gene expression in Synechocystis. J Biol Chem 278: 12191–12198PubMedCrossRefGoogle Scholar
  39. Ishizaki-Nishizawa O, Fujii T, Azuma M, Sekiguchi K, Murata N, Ohtani T and Toguri T (1996) Low-temperature resistance of higher plants is significantly enhanced by a nonspecific cyanobacterial desaturase. Nature Biotechnol 14: 1003–1006CrossRefGoogle Scholar
  40. Jordt SE, McKemy DD and Julius D (2003) Lessons from peppers and peppermint: the molecular logic of thermosensation. Curr Opin Neurobiol 13: 487–492PubMedCrossRefGoogle Scholar
  41. Kabelitz N, Santos PM and Heipieper HJ (2003) Effect of aliphatic alcohols on growth and degree of saturation of membrane lipids in Acinetobacter calcoaceticus. FEMS Microbiol Lett 220: 223–227PubMedCrossRefGoogle Scholar
  42. Kanesaki Y, Suzuki I, Allakhverdiev SI, Mikami K and Murata N (2002) Salt stress and hyperosmotic stress regulate the expression of different sets of genes in Syn-echocystis sp. PCC 6803. Biochem Biophys Res Commun 290: 339–348PubMedCrossRefGoogle Scholar
  43. Kanesaki Y, Yamamoto H, Paithoonrangsarid K, Shoum-skaya M, Suzuki I, Hayashi H and Murata N (2007) His-tidine kinases play important roles in the perception and signal transduction of H2O2 in the cyanobacterium, Syn-echocystis. Plant J 49: 313–324PubMedCrossRefGoogle Scholar
  44. Kiegle E, Moore CA, Haseloff J, Tester MA and Knight MR (2000) Cell-type-specific calcium responses to drought, salt and cold in the Arabidopsis root. Plant J 23: 267–278PubMedCrossRefGoogle Scholar
  45. Knight H and Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6: 262–267PubMedCrossRefGoogle Scholar
  46. Knight H, Trewavas AJ and Knight MR (1996) Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8: 489–503PubMedGoogle Scholar
  47. Laroche C, Beney L, Marechal PA and Gervais P (2001) The effect of osmotic pressure on the membrane fluidity of Saccharomyces cerevisiae at different physiological temperatures. Appl Microbiol Biotechnol 56: 249–254PubMedCrossRefGoogle Scholar
  48. Lentz BR (1993) Use of fluorescent probes to monitor molecular order and motions within liposome bilayers. Chem Phys Lipids 64: 99–116PubMedCrossRefGoogle Scholar
  49. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K and Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA-binding domain separate two cellular signal trans-duction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10: 1391–1406PubMedGoogle Scholar
  50. Logue JA, de Vries AL, Fodor E and Cossins AR (2000) Lipid compositional correlates of temperature-adaptive interspecific differences in membrane physical structure. J Exp Biol 203: 2105–2114.PubMedGoogle Scholar
  51. Lopez CS, Heras H, Garda H, Rusal S, Sanches-Rivas C and Rivas E (2000) Biochemical and biophysical studies of Bacillus subtilis envelopes under hyperosmotic stress. Int J Food Microbiol 55: 137–142PubMedCrossRefGoogle Scholar
  52. Los DA and Murata N. (1998) Structure and expression of fatty acid desaturases. Biochim Biophys Acta 1394: 3–15PubMedCrossRefGoogle Scholar
  53. Los DA and Murata N (1999) Responses to cold shock in cyanobacteria. J Mol Microbiol Biotechnol 1: 221–230PubMedGoogle Scholar
  54. Los DA and Murata N (2000) Regulation of enzymatic activity and gene expression by membrane fluidity. Science's Signal Transduction Knowledge Environment. Available at sigtrans;2000/62/pe1Google Scholar
  55. Los DA and Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666: 142–157PubMedCrossRefGoogle Scholar
  56. Los D, Horváth I, Vigh L and Murata N (1993) The temperature-dependent expression of the desaturase gene desA in Syne-chocystis PCC 6803. FEBS Lett 318: 57–60PubMedCrossRefGoogle Scholar
  57. Los DA, Ray MK and Murata N (1997) Differences in the control of the temperature-dependent expression of four genes for desaturases in Synechocystis sp. PCC 6803. Mol Microbiol 25: 1167–1175PubMedCrossRefGoogle Scholar
  58. Los DA, Suzuki I, Zinchenko VV and Murata N (2008) Stress responses in Synechocystis: regulated genes and regulatory systems. In: Herrero A and Flores E (eds) The Cyanobacteria: Molecular Biology, Genomics and Evolution. Caister Academic Press, Norfolk, pp. 117–157Google Scholar
  59. Lyons JM and Raison JK (1970) Oxidative activity of mitochondria isolated from plant tissues sensitive and resistant to chilling injury. Plant Physiol 45: 386–389PubMedCrossRefGoogle Scholar
  60. Macartney AI, Maresca B, Cossins AR (1994) Acyl-CoA desaturases and the adaptive regulation of membrane lipid composition. In: Cossins AR (ed) Temperature Adaptation of Biological Membranes. Portland Press, London, pp. 129–139Google Scholar
  61. Macartney AI, Tiku PE and Cossins AR (1996) An isothermal induction of Δ9-desaturase in cultured carp hepato-cytes. Biochim Biophys Acta 1302: 207–216PubMedCrossRefGoogle Scholar
  62. Maeda T, Wurgler-Murphy SM and Saito H (1994) A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369: 242–245PubMedCrossRefGoogle Scholar
  63. Mansilla MC and de Mendoza D (2005) The Bacillus subtilis desaturase: a model to understand phospholipid modification and temperature sensing. Arch Microbiol 183: 229–235PubMedCrossRefGoogle Scholar
  64. Mansilla MC, Cybulsky LE, Albanesi D and de Mendoza D (2004) Control of membrane fluidity by molecular ther-mosensors. J Bacteriol 186: 6681–6688PubMedCrossRefGoogle Scholar
  65. Maresca B and Kobayashi G (1993) Changes in membrane fluidity modulate heat shock gene expression and produced attenuated strains in the dimorphic fungus Histo-plasma capsulatum. Arch Med Res 24: 247–249PubMedGoogle Scholar
  66. Marin K, Suzuki I, Yamaguchi K, Ribbeck K, Yamamoto H, Kanesaki Y, Hagemann M and Murata N (2003) Identification of histidine kinases that act as sensors in the perception of salt stress in Synechocystis sp. PCC 6803. Proc Natl Acad Sci USA 100: 9061–9066PubMedCrossRefGoogle Scholar
  67. McKemy DD (2007) Temperature sensing across species. Pflugers Arch 454: 777–791PubMedCrossRefGoogle Scholar
  68. McKemy DD, Neuhausser WM and Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416: 52–58PubMedCrossRefGoogle Scholar
  69. Meyer GR, Gullingsrud J, Schulten K and Martinac B (2006) Molecular dynamics study of MscL interactions with a curved lipid bilayer. Biophys J 91: 1630–1637PubMedCrossRefGoogle Scholar
  70. Mikami K, Kanesaki Y, Suzuki I and Murata N (2002) The histidine kinase Hik33 perceives osmotic stress and cold stress in Synechocystis sp. PCC 6803. Mol Microbiol 46: 905–915PubMedCrossRefGoogle Scholar
  71. Mileykovskaya E and Dowhan W (1997) The Cpx two-component signal transduction pathway is activated in Escherichia coli mutant strains lacking phosphatidyleth-anolamine. J Bacteriol 179: 1029–1034PubMedGoogle Scholar
  72. Moe PC, Levin G and Blount P (2000) Correlating a protein structure with function of a bacterial mechanosensitive channel. J Biol Chem 275: 31121–31127PubMedCrossRefGoogle Scholar
  73. Murata N and Los DA (1997) Membrane fluidity and temperature perception. Plant Physiol 115: 875–879PubMedGoogle Scholar
  74. Murata N and Los DA (2006) Genome-wide analysis of gene expression characterizes histidine kinase Hik33 as an important component of the cold-signal transduction in cyanobacteria. Physiol Plant 57: 235–247Google Scholar
  75. Murata N and Wada H (1995) Acyl-lipid desaturases and their importance in the tolerance and acclimatization to cold of cyanobacteria. Biochem J 308: 1–8PubMedGoogle Scholar
  76. Nakashima K, Kanamaru K, Aiba H and Mizuno T (1991) Osmoregulatory expression of the porin genes in Escherichia coli: evidence for signal titration in the signal transduction through EnvZ-OmpR phosphotransfer. FEMS Microbiol Lett 66: 43–47PubMedCrossRefGoogle Scholar
  77. Nakashima K, Sugiura A and Mizuno T (1993a) Functional reconstitution of the putative Escherichia coli osmosen-sor, KdpD, into liposomes. J Biochem 114: 615–621Google Scholar
  78. Nakashima K, Sugiura A, Kanamaru K and Mizuno T (1993b) Signal transduction between the two regulatory components involved in the regulation of the kdpABC operon in Escherichia coli: phosphorylation-dependent functioning of the positive regulator, KdpE. Mol Micro-biol 7: 109–116CrossRefGoogle Scholar
  79. Nazarenko LV, Andreev IM, Lyukevich AA, Pisareva TV and Los DA (2003) Calcium release from Synechocystis cells induced by depolarization of the plasma membrane: MscL as an outward Ca2+ channel. Microbiology 149: 1147–1153PubMedCrossRefGoogle Scholar
  80. Nishida I and Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 47: 541–568PubMedCrossRefGoogle Scholar
  81. Novikova GV, Moshkov IE and Los DA (2007) Protein sensors and transducers of cold, hyperosmotic and salt stresses in cyanobacteria and plants. Mol Biol (Mosk) 41: 478–490Google Scholar
  82. Okuyama H, Sasaki S, Higashi S and Murata N (1990) A trans-unsaturated fatty acid in a psychrophilic bacterium, Vibrio sp. strain ABE-1. J Bacteriol 172: 3515–3518PubMedGoogle Scholar
  83. Okuyama H, Okajima N, Sasaki S, Higashi S and Murata N (1991) The cis/trans isomerization of the double bond of a fatty acid as a strategy for adaptation to changes in ambient temperature in the psychrophilic bacterium, Vibrio sp. strain ABE-1. Biochim Biophys Acta 1084: 13–20PubMedCrossRefGoogle Scholar
  84. Orlova IV, Serebriiskaya TS, Popov V, Merkulova N, Nosov AM, Trunova TI, Tsydendambaev VD and Los DA (2003) Transformation of tobacco with a gene for the thermophilic acyl-lipid desaturase enhances the chilling tolerance of plants. Plant Cell Physiol 44: 447–450PubMedCrossRefGoogle Scholar
  85. Orvar BL, Sangwan V, Omann F and Dhindsa RS (2000) Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant J 23: 785–794PubMedCrossRefGoogle Scholar
  86. Ota IM and Varshavsky A (1993) A yeast protein similar to bacterial two-component regulators. Science 262: 566–569PubMedCrossRefGoogle Scholar
  87. Paithoonrangsarid K, Shoumskaya MA, Kanesaki Y, Satoh S, Tabata S, Los DA, Zinchenko VV, Hayashi H, Tan-ticharoen M, Suzuki I and Murata N (2004) Five histidine kinases perceive osmotic stress and regulate distinct sets of genes in Synechocystis. J Biol Chem 279: 53078–53086PubMedCrossRefGoogle Scholar
  88. Patapoutian A, Peier AM, Story GM and Viswanath V (2003) ThermoTRP channels and beyond: mechanisms of temperature sensation. Nature Rev Neurosci 4: 529–539CrossRefGoogle Scholar
  89. Pehowich DJ, Macdonald PM, McElhaney RN, Cossins AR and Wang LC (1988) Calorimetric and spectroscopic studies of lipid thermotropic phase behavior in liver inner mitochondrial membranes from a mammalian hibernator. Biochemistry 27: 4632–4638PubMedCrossRefGoogle Scholar
  90. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, Bevan S and Patapoutian A (2002a) A TRP channel that senses cold stimuli and menthol. Cell 108: 705–715CrossRefGoogle Scholar
  91. Peier AM, Reeve AJ, Andersson DA, Moqrich A, Earley TJ, Hergarden AC, Story GM, Colley S, Hogenesch JB, McIntyre P, Bevan S and Patapoutian A (2002b) A heat-sensitive TRP channel expressed in keratinocytes. Science 296: 2046–2049CrossRefGoogle Scholar
  92. Plieth C (2005) Calcium: just another regulator in the machinery of life? Ann Bot 96: 1–8PubMedCrossRefGoogle Scholar
  93. Plieth C, Hansen U-P, Knight H and Knight MR (1999) Temperature sensing by plants: the primary mechanisms of signal perception and calcium response. Plant J 18: 491–497PubMedCrossRefGoogle Scholar
  94. Poolman B, Blount P, Folgering JH, Friesen RH, Moe PC and van der Heide T (2002) How do membrane proteins sense water stress? Mol Microbiol 44: 889–902PubMedCrossRefGoogle Scholar
  95. Posas F, Wurgler-Murphy SM, Maeda T, Witten EA, Thai TC and Saito H (1996) Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 “two-component” osmosensor. Cell 86: 865–875PubMedCrossRefGoogle Scholar
  96. Qin L, Dutta R, Kurokawa H, Ikura M and Inouye M (2000) A monomeric histidine kinase derived from EnvZ, an Escherichia coli osmosensor. Mol Microbiol 36: 24–32PubMedCrossRefGoogle Scholar
  97. Raitt DC, Posas F and Saito H (2000) Yeast Cdc42 GTPase and Ste20 PAK-like kinase regulate Sho1-dependent activation of the Hog1 MAP kinase pathway. EMBO J 19: 4623–4631PubMedCrossRefGoogle Scholar
  98. Raivio TL and Silhavy TJ (2001) Periplasmic stress and ECF sigma factors. Annu Rev Microbiol 55: 591–624PubMedCrossRefGoogle Scholar
  99. Rodríguez-Vargas S, Sánchez-García A, Martínez-Rivas JM, Prieto JA and Randez-Gil F (2007) Fluidization of membrane lipids enhances the tolerance of Saccharomy-ces cerevisiae to freezing and salt stress. Appl Environ Microbiol 73: 110–116PubMedCrossRefGoogle Scholar
  100. Sangwan V, Orvar BL, Beyerly J, Hirt H and Dhindsa RS (2002) Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J 31: 629–638PubMedCrossRefGoogle Scholar
  101. Sarcina M, Murata N, Tobin MJ and Mullineaux CW (2003) Lipid diffusion in the thylakoid membranes of the cyano-bacterium Synechococcus sp.: effect of fatty acid desaturation (2003) FEBS Lett 553: 295–298PubMedCrossRefGoogle Scholar
  102. Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y and Shinozaki K (2001) Monitoring the expression pattern of 1300 Arabi-dopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13: 61–72PubMedGoogle Scholar
  103. Shinozaki K and Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3: 217–223PubMedGoogle Scholar
  104. Shinwari ZK, Nakashima K, Miura S, Kasuga M, Seki M, Yamaguchi-Shinozaki K and Shinozaki K (1998) An Ara-bidopsis gene family encoding DRE/CRT-binding proteins involved in low-temperature-responsive gene expression. Biochem Biophys Res Commun 250: 161–170PubMedCrossRefGoogle Scholar
  105. Shoumskaya MA, Paithoonrangsarid K., Kanesaki Y, Los DA, Zinchenko VV, Tanticharoen M, Suzuki I and Murata N (2005) Identical Hik-Rre systems are involved in perception and transduction of salt signals and hyperosmotic signals but regulate the expression of individual genes to different extents in Synechocystis. J Biol Chem 280: 21531–21538PubMedCrossRefGoogle Scholar
  106. Sinensky M (1974) Homeoviscous adaptation — a homeo-static process that regulates viscosity of membrane lipids in Escherichia coli. Proc Natl Acad Sci USA 71: 522–525PubMedCrossRefGoogle Scholar
  107. Slabas AR, Suzuki I, Murata N, Simon WJ and Hall JJ (2006) Proteomic analysis of the heat shock response in Synechocystis PCC6803 and a thermally tolerant knockout strain lacking the histidine kinase 34 gene. Proteomics 6: 845–864PubMedCrossRefGoogle Scholar
  108. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S and Patapou-tian A (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112: 819–829PubMedCrossRefGoogle Scholar
  109. Sugiura A, Hirokawa K, Nakashima K and Mizuno T (1994) Signal-sensing mechanisms of the putative osmosensor KdpD in Escherichia coli. Mol Microbiol 14: 929–938PubMedCrossRefGoogle Scholar
  110. Sukharev S (1999) Mechanosensitive channels in bacteria as membrane tension reporters. FASEB J 13: S55–S61PubMedGoogle Scholar
  111. Sukharev SI, Blount P, Martinac B, Blattner FR and Kung C (1994) A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature 368: 265–268PubMedCrossRefGoogle Scholar
  112. Sukharev SI, Betanzos M, Chiang CS and Guy HR (2001) The gating mechanism of the large mechanosensitive channel MscL. Nature 409: 720–724PubMedCrossRefGoogle Scholar
  113. Suzuki I, Los DA, Kanesaki Y, Mikami K and Murata N (2000) The pathway for perception and transduction of low-temperature signals in Synechocystis. EMBO J 19: 1327–1334PubMedCrossRefGoogle Scholar
  114. Suzuki I, Kanesaki Y, Mikami K, Kanehisa M and Murata N (2001) Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol Microbiol 40: 235–244PubMedCrossRefGoogle Scholar
  115. Suzuki I, Kanesaki Y, Hayashi H, Hall JJ, Simon WJ, Slabas AR and Murata N (2005) The histidine kinase Hik34 is involved in thermotolerance by regulating the expression of heat shock genes in Synechocystis. Plant Physiol 138: 1409–1421PubMedCrossRefGoogle Scholar
  116. Szalontai B, Nishiyama Y, Gombos Z and Murata N (2000) Membrane dynamics as seen by Fourier transform infrared spectroscopy in a cyanobacterium, Synechocystis PCC 6803: The effects of lipid unsaturation and the protein-to-lipid ratio. Biochim Biophys Acta 1509: 409–419PubMedCrossRefGoogle Scholar
  117. Tasaka Y, Gombos Z, Nishiyama Y, Mohanty P, Ohba T, Ohki K and Murata N (1996) Targeted mutagenesis of acyl-lipid desaturases in Synechocystis: evidence for the important roles of polyunsaturated membrane lipids in growth, respiration and photosynthesis. EMBO J 15: 6416–6425PubMedGoogle Scholar
  118. Thewke D, Kramer M and Sinensky MS (2003) Transcrip-tional homeostatic control of membrane lipid composition. Biochem Biophys Res Commun 273: 1–4CrossRefGoogle Scholar
  119. Tiku PE, Gracey AY, Macartney AI, Beynon RJ and Cossins AR (1996) Cold-induced expression of Δ9-desaturase in carp by transcriptional and posttranslational mechanisms. Science 271: 815–818PubMedCrossRefGoogle Scholar
  120. Tokishita S and Mizuno T (1994) Transmembrane signal transduction by the Escherichia coli osmotic sensor, EnvZ: intermolecular complementation of transmem-brane signaling. Mol Microbiol 13: 435–444PubMedCrossRefGoogle Scholar
  121. Török Z, Goloubinoff P, Horváth I, Tsvetkova NM, Glatz A, Balogh G, Varvasovszki V, Los DA, Vierling E, Crowe JH and Vigh L (2001) Synechocystis HSP17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone-mediated refolding. Proc Natl Acad Sci USA 98: 3098–3103PubMedCrossRefGoogle Scholar
  122. Tran LS, Urao T, Qin F, Maruyama K, Kakimoto T, Shi-nozaki K and Yamaguchi-Shinozaki K (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histi-dine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci USA 104: 20623–20628PubMedCrossRefGoogle Scholar
  123. Trewavas AJ and Malho R (1998) Ca2+ signaling in plant cells: the big network! Curr Opin Plant Biol 1: 428–433PubMedCrossRefGoogle Scholar
  124. Ueki T and Inouye S (2002) Transcriptional activation of a heat-shock gene, lonD, of Myxococcus xanthus by a two-component histidine-aspartate phosphorelay system. J Biol Chem 277: 6170–6177PubMedCrossRefGoogle Scholar
  125. Upchurch RG (2008) Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotech-nol Lett 30: 967–977CrossRefGoogle Scholar
  126. Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozaki K, Seki M, Hirayama T and Shinozaki K (1999) A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11: 1743–1754PubMedGoogle Scholar
  127. van der Heide T and Poolman B (2000) Osmoregulated ABC-transport system of Lactococcus lactis senses water stress via changes in the physical state of the membrane. Proc Natl Acad Sci USA 97: 7102–7106PubMedCrossRefGoogle Scholar
  128. van der Heide T, Stuart MC and Poolman B (2001) On the osmotic signal and osmosensing mechanism of an ABC transport system for glycine betaine. EMBO J 20: 7022–7032PubMedCrossRefGoogle Scholar
  129. van Wuytswinkel O, Reiser V, Siderius M, Kelders MC, Ammerer G, Ruis H and Mager WH (2000) Response of Saccharomyces cerevisiae to severe osmotic stress: evidence for a novel activation mechanism of the HOG MAP kinase pathway. Mol Microbiol 37: 382–397PubMedCrossRefGoogle Scholar
  130. Vigh L, Los DA, Horváth I and Murata N (1993) The primary signal in the biological perception of temperature: Pd-catalyzed hydrogenation of membrane lipids stimulated the expression of the desA gene in Synechocystis PCC 6803. Proc Natl Acad Sci USA 90: 9090–9094PubMedCrossRefGoogle Scholar
  131. Vigh L, Maresca B and Harwood JL (1998) Does the membrane's physical state control the expression of heat shock and other genes? Trends Biochem Sci 23: 369–374PubMedCrossRefGoogle Scholar
  132. Wada H, Gombos Z and Murata N (1990) Enhancement of chilling tolerance of a cyanobacterium by genetic manip-ulation of fatty acid desaturation. Nature 347: 200–203PubMedCrossRefGoogle Scholar
  133. Wilhelm KS and Thomashow MF (1993) Arabidopsis thaliana cor15b, an apparent homologue of cor15a, is strongly responsive to cold and ABA, but not drought. Plant Mol Biol 23: 1073–1077PubMedCrossRefGoogle Scholar
  134. Wodtke E and Cossins AR (1991) Rapid cold-induced changes of membrane order and Δ9-desaturase activity in endoplasmic reticulum of carp liver: a time-course study of thermal acclimation. Biochim Biophys Acta 1064: 342–350Google Scholar
  135. Wood JM (1999) Osmosensing by bacteria: signals and membrane-based sensors. Microbiol Mol Biol Rev 63: 230–262PubMedGoogle Scholar
  136. Xiong L, Ishitani M and Zhu JK (1999) Interaction of osmotic stress, temperature, and abscisic acid in the regulation of gene expression in Arabidopsis. Plant Physiol 119: 205–221PubMedCrossRefGoogle Scholar
  137. Xiong L, Schumaker KS and Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14: S165–S183PubMedCrossRefGoogle Scholar
  138. Yale J and Bohnert HJ (2001) Transcript expression in Sac-charomyces cerevisiae at high salinity. J Biol Chem 276: 15996–16007PubMedCrossRefGoogle Scholar
  139. Yamaguchi-Shinozaki K and Shinozaki K (2006) Transcrip-tional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57: 781–803PubMedCrossRefGoogle Scholar
  140. Yamazaki M, Ohnishi S and Ito T (1989) Osmoelastic coupling in biological structures: decrease in membrane fluidity and osmophobic association of phospholipid vesicles in response to osmotic stress. Biochemistry 28: 3710–3715PubMedCrossRefGoogle Scholar
  141. Zhu JK (2001) Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4: 401–406PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia
  2. 2.Department of GeneticsMoscow State University; Vorobievy GoryMoscowRussia

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