Skip to main content
SpringerLink
Log in

Regulatory Role of Membrane Fluidity in Gene Expression

  • Chapter
Lipids in Photosynthesis

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 30))

Summary

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

DPH:

1,6-Diphenyl-1,3,5-hexatriene

FTIR spectroscopy:

Fourier transform infrared spectroscopy

PAS domain:

Per-ARNT-Sim conservative motif

rbp:

RNA-binding protein

SRE:

Sterol responsive element

SREBP:

Sterol responsive element binding protein

References

  • Aguilar PS and de Mendoza D (2006) Control of fatty acid desaturation: a mechanism conserved from bacteria to humans. Mol Microbiol 62: 1507–1514

    Article  PubMed  CAS  Google Scholar 

  • 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: 1681–1691

    Article  PubMed  CAS  Google Scholar 

  • 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: 2655–2663

    Article  PubMed  CAS  Google Scholar 

  • 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: 2915–2920

    Article  PubMed  CAS  Google Scholar 

  • 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: 1219–1232

    Article  PubMed  CAS  Google Scholar 

  • Blount P and Moe PC (1999) Bacterial mechanosensitive channels: integrating physiology, structure and function. Trends Microbiol 7: 420–424

    Article  PubMed  CAS  Google Scholar 

  • Bossie MA and Martin CE (1989) Nutritional regulation of yeast Δ9 fatty acid desaturase activity. J Bacteriol 171: 6409–6413

    PubMed  CAS  Google Scholar 

  • 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: 4835–4840

    Article  PubMed  CAS  Google Scholar 

  • 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: 11041–11048

    Article  PubMed  CAS  Google Scholar 

  • 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: 3870–3875

    Article  PubMed  CAS  Google Scholar 

  • 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: 323–337

    PubMed  CAS  Google Scholar 

  • 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: 225–236

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Zhu J and Zhu J-K (2006) Gene regulation during cold acclimation in plants. Physiol Plant 126: 52–61

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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: 1379–1388

    Article  PubMed  CAS  Google Scholar 

  • 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: 1183–1193

    Article  PubMed  CAS  Google Scholar 

  • 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: 387–398

    Article  PubMed  CAS  Google Scholar 

  • De Wulf P, Akerley BJ and Lin EC (2000) Presence of the Cpx system in bacteria. Microbiology 146: 247–248

    PubMed  Google Scholar 

  • DiGiuseppe PA and Silhavy TJ (2003) Signal detection and target gene induction by the CpxRA two-component system. J Bacteriol 185: 2432–2440

    Article  PubMed  CAS  Google Scholar 

  • Edwards PA and Ericsson J (1999) Sterols and isoprenoids: signaling molecules derived from the cholesterol biosyn-thetic pathway. Annu Rev Biochem 68: 157–185

    Article  PubMed  CAS  Google Scholar 

  • 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: 48220–48229

    Google Scholar 

  • 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: 1675–1690

    Google Scholar 

  • Franklin KA and Whitelam GC (2007) Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nature Genet 39: 1410–1413

    Article  PubMed  CAS  Google Scholar 

  • 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: 4241–4257

    PubMed  CAS  Google Scholar 

  • 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: 1–12

    Article  CAS  Google Scholar 

  • 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: 22480–22489

    Article  PubMed  CAS  Google Scholar 

  • Grunberger D, Haimovitz R and Shinitzky M (1982) Resolution of plasma membrane lipid fluidity in intact cells labeled with diphenylhexatriene. Biochim Biophys Acta 688: 764–774

    Article  PubMed  CAS  Google Scholar 

  • 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: 2515–2519

    Article  PubMed  CAS  Google Scholar 

  • 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: 1727–1733

    PubMed  CAS  Google Scholar 

  • 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: 132–142

    Article  PubMed  Google Scholar 

  • Hazel JR (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57: 19–42

    Article  PubMed  CAS  Google Scholar 

  • 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: 1–7

    Article  PubMed  CAS  Google Scholar 

  • 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: 793–806

    PubMed  CAS  Google Scholar 

  • 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: 1719–1725

    Article  PubMed  CAS  Google Scholar 

  • Hohmann S (2003) Osmotic stress signaling and osmoadap-tation in yeasts. Microbiol Mol Biol Rev 66: 300–372

    Article  CAS  Google Scholar 

  • 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: 3513–3518

    Article  PubMed  Google Scholar 

  • Horváth I, Multhoff G, Sonnleitner A and Vígh L (2008) Membrane-associated stress proteins: more than simply chaperones. Biochim Biophys Acta 1778: 1653–1664

    Article  PubMed  CAS  Google Scholar 

  • 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: 12191–12198

    Article  PubMed  CAS  Google Scholar 

  • 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: 1003–1006

    Article  CAS  Google Scholar 

  • Jordt SE, McKemy DD and Julius D (2003) Lessons from peppers and peppermint: the molecular logic of thermosensation. Curr Opin Neurobiol 13: 487–492

    Article  PubMed  CAS  Google Scholar 

  • 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: 223–227

    Article  PubMed  CAS  Google Scholar 

  • 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: 339–348

    Article  PubMed  CAS  Google Scholar 

  • 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: 313–324

    Article  PubMed  CAS  Google Scholar 

  • 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: 267–278

    Article  PubMed  CAS  Google Scholar 

  • Knight H and Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6: 262–267

    Article  PubMed  CAS  Google Scholar 

  • 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: 489–503

    PubMed  CAS  Google Scholar 

  • 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: 249–254

    Article  PubMed  CAS  Google Scholar 

  • Lentz BR (1993) Use of fluorescent probes to monitor molecular order and motions within liposome bilayers. Chem Phys Lipids 64: 99–116

    Article  PubMed  CAS  Google Scholar 

  • 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: 1391–1406

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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: 137–142

    Article  PubMed  CAS  Google Scholar 

  • Los DA and Murata N. (1998) Structure and expression of fatty acid desaturases. Biochim Biophys Acta 1394: 3–15

    Article  PubMed  CAS  Google Scholar 

  • Los DA and Murata N (1999) Responses to cold shock in cyanobacteria. J Mol Microbiol Biotechnol 1: 221–230

    PubMed  CAS  Google Scholar 

  • Los DA and Murata N (2000) Regulation of enzymatic activity and gene expression by membrane fluidity. Science's Signal Transduction Knowledge Environment. Available at http://stke.sciencemag.org/cgi/content/full/ sigtrans;2000/62/pe1

    Google Scholar 

  • Los DA and Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666: 142–157

    Article  PubMed  CAS  Google Scholar 

  • 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: 57–60

    Article  PubMed  CAS  Google Scholar 

  • 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: 1167–1175

    Article  PubMed  CAS  Google Scholar 

  • 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. 117–157

    Google Scholar 

  • Lyons JM and Raison JK (1970) Oxidative activity of mitochondria isolated from plant tissues sensitive and resistant to chilling injury. Plant Physiol 45: 386–389

    Article  PubMed  CAS  Google Scholar 

  • 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. 129–139

    Google Scholar 

  • Macartney AI, Tiku PE and Cossins AR (1996) An isothermal induction of Δ9-desaturase in cultured carp hepato-cytes. Biochim Biophys Acta 1302: 207–216

    Article  PubMed  Google Scholar 

  • Maeda T, Wurgler-Murphy SM and Saito H (1994) A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369: 242–245

    Article  PubMed  CAS  Google Scholar 

  • Mansilla MC and de Mendoza D (2005) The Bacillus subtilis desaturase: a model to understand phospholipid modification and temperature sensing. Arch Microbiol 183: 229–235

    Article  PubMed  CAS  Google Scholar 

  • Mansilla MC, Cybulsky LE, Albanesi D and de Mendoza D (2004) Control of membrane fluidity by molecular ther-mosensors. J Bacteriol 186: 6681–6688

    Article  PubMed  CAS  Google Scholar 

  • 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: 247–249

    PubMed  CAS  Google Scholar 

  • 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: 9061–9066

    Article  PubMed  CAS  Google Scholar 

  • McKemy DD (2007) Temperature sensing across species. Pflugers Arch 454: 777–791

    Article  PubMed  CAS  Google Scholar 

  • McKemy DD, Neuhausser WM and Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416: 52–58

    Article  PubMed  CAS  Google Scholar 

  • Meyer GR, Gullingsrud J, Schulten K and Martinac B (2006) Molecular dynamics study of MscL interactions with a curved lipid bilayer. Biophys J 91: 1630–1637

    Article  PubMed  CAS  Google Scholar 

  • 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: 905–915

    Article  PubMed  CAS  Google Scholar 

  • 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: 1029–1034

    PubMed  CAS  Google Scholar 

  • Moe PC, Levin G and Blount P (2000) Correlating a protein structure with function of a bacterial mechanosensitive channel. J Biol Chem 275: 31121–31127

    Article  PubMed  CAS  Google Scholar 

  • Murata N and Los DA (1997) Membrane fluidity and temperature perception. Plant Physiol 115: 875–879

    PubMed  CAS  Google Scholar 

  • 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: 235–247

    CAS  Google Scholar 

  • Murata N and Wada H (1995) Acyl-lipid desaturases and their importance in the tolerance and acclimatization to cold of cyanobacteria. Biochem J 308: 1–8

    PubMed  CAS  Google Scholar 

  • 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: 43–47

    Article  PubMed  CAS  Google Scholar 

  • Nakashima K, Sugiura A and Mizuno T (1993a) Functional reconstitution of the putative Escherichia coli osmosen-sor, KdpD, into liposomes. J Biochem 114: 615–621

    CAS  Google Scholar 

  • 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: 109–116

    Article  CAS  Google Scholar 

  • 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: 1147–1153

    Article  PubMed  CAS  Google Scholar 

  • 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: 541–568

    Article  PubMed  CAS  Google Scholar 

  • 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: 478–490

    CAS  Google Scholar 

  • 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: 3515–3518

    PubMed  CAS  Google Scholar 

  • 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: 13–20

    Article  PubMed  CAS  Google Scholar 

  • 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: 447–450

    Article  PubMed  CAS  Google Scholar 

  • 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: 785–794

    Article  PubMed  CAS  Google Scholar 

  • Ota IM and Varshavsky A (1993) A yeast protein similar to bacterial two-component regulators. Science 262: 566–569

    Article  PubMed  CAS  Google Scholar 

  • 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: 53078–53086

    Article  PubMed  CAS  Google Scholar 

  • Patapoutian A, Peier AM, Story GM and Viswanath V (2003) ThermoTRP channels and beyond: mechanisms of temperature sensation. Nature Rev Neurosci 4: 529–539

    Article  CAS  Google Scholar 

  • 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: 4632–4638

    Article  PubMed  CAS  Google Scholar 

  • 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: 705–715

    Article  CAS  Google Scholar 

  • 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: 2046–2049

    Article  CAS  Google Scholar 

  • Plieth C (2005) Calcium: just another regulator in the machinery of life? Ann Bot 96: 1–8

    Article  PubMed  CAS  Google Scholar 

  • 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: 491–497

    Article  PubMed  CAS  Google Scholar 

  • 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: 889–902

    Article  PubMed  CAS  Google Scholar 

  • 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: 865–875

    Article  PubMed  CAS  Google Scholar 

  • 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: 24–32

    Article  PubMed  CAS  Google Scholar 

  • 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: 4623–4631

    Article  PubMed  CAS  Google Scholar 

  • Raivio TL and Silhavy TJ (2001) Periplasmic stress and ECF sigma factors. Annu Rev Microbiol 55: 591–624

    Article  PubMed  CAS  Google Scholar 

  • 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: 110–116

    Article  PubMed  CAS  Google Scholar 

  • 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: 629–638

    Article  PubMed  CAS  Google Scholar 

  • 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: 295–298

    Article  PubMed  CAS  Google Scholar 

  • 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: 61–72

    PubMed  CAS  Google Scholar 

  • 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: 217–223

    PubMed  CAS  Google Scholar 

  • 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: 161–170

    Article  PubMed  CAS  Google Scholar 

  • 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: 21531–21538

    Article  PubMed  CAS  Google Scholar 

  • Sinensky M (1974) Homeoviscous adaptation — a homeo-static process that regulates viscosity of membrane lipids in Escherichia coli. Proc Natl Acad Sci USA 71: 522–525

    Article  PubMed  CAS  Google Scholar 

  • 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: 845–864

    Article  PubMed  CAS  Google Scholar 

  • 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: 819–829

    Article  PubMed  CAS  Google Scholar 

  • Sugiura A, Hirokawa K, Nakashima K and Mizuno T (1994) Signal-sensing mechanisms of the putative osmosensor KdpD in Escherichia coli. Mol Microbiol 14: 929–938

    Article  PubMed  CAS  Google Scholar 

  • Sukharev S (1999) Mechanosensitive channels in bacteria as membrane tension reporters. FASEB J 13: S55–S61

    PubMed  CAS  Google Scholar 

  • 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: 265–268

    Article  PubMed  CAS  Google Scholar 

  • Sukharev SI, Betanzos M, Chiang CS and Guy HR (2001) The gating mechanism of the large mechanosensitive channel MscL. Nature 409: 720–724

    Article  PubMed  CAS  Google Scholar 

  • 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: 1327–1334

    Article  PubMed  CAS  Google Scholar 

  • 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: 235–244

    Article  PubMed  CAS  Google Scholar 

  • 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: 1409–1421

    Article  PubMed  CAS  Google Scholar 

  • 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: 409–419

    Article  PubMed  CAS  Google Scholar 

  • 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: 6416–6425

    PubMed  CAS  Google Scholar 

  • Thewke D, Kramer M and Sinensky MS (2003) Transcrip-tional homeostatic control of membrane lipid composition. Biochem Biophys Res Commun 273: 1–4

    Article  CAS  Google Scholar 

  • 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: 815–818

    Article  PubMed  CAS  Google Scholar 

  • 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: 435–444

    Article  PubMed  CAS  Google Scholar 

  • 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: 3098–3103

    Article  PubMed  Google Scholar 

  • 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: 20623–20628

    Article  PubMed  CAS  Google Scholar 

  • Trewavas AJ and Malho R (1998) Ca2+ signaling in plant cells: the big network! Curr Opin Plant Biol 1: 428–433

    Article  PubMed  CAS  Google Scholar 

  • 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: 6170–6177

    Article  PubMed  CAS  Google Scholar 

  • Upchurch RG (2008) Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotech-nol Lett 30: 967–977

    Article  CAS  Google Scholar 

  • 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: 1743–1754

    PubMed  CAS  Google Scholar 

  • 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: 7102–7106

    Article  PubMed  Google Scholar 

  • 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: 7022–7032

    Article  PubMed  Google Scholar 

  • 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: 382–397

    Article  PubMed  Google Scholar 

  • 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: 9090–9094

    Article  PubMed  CAS  Google Scholar 

  • 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: 369–374

    Article  PubMed  CAS  Google Scholar 

  • 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: 200–203

    Article  PubMed  CAS  Google Scholar 

  • 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: 1073–1077

    Article  PubMed  CAS  Google Scholar 

  • 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: 342–350

    Google Scholar 

  • Wood JM (1999) Osmosensing by bacteria: signals and membrane-based sensors. Microbiol Mol Biol Rev 63: 230–262

    PubMed  CAS  Google Scholar 

  • 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: 205–221

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Schumaker KS and Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14: S165–S183

    Article  PubMed  CAS  Google Scholar 

  • Yale J and Bohnert HJ (2001) Transcript expression in Sac-charomyces cerevisiae at high salinity. J Biol Chem 276: 15996–16007

    Article  PubMed  CAS  Google Scholar 

  • 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: 781–803

    Article  PubMed  CAS  Google Scholar 

  • 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: 3710–3715

    Article  PubMed  CAS  Google Scholar 

  • Zhu JK (2001) Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4: 401–406

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, Moscow, 127276, Russia

    Dmitry A. Los

  2. Department of Genetics, Moscow State University; Vorobievy Gory, Moscow, 119991, Russia

    Vladislav V. Zinchenko (Faculty of Biology)

Authors
  1. Dmitry A. Los
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vladislav V. Zinchenko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dmitry A. Los .

Editor information

Editors and Affiliations

  1. Department of Life Sciences, Graduate School of Arts and Science, University of Tokyo, Japan

    Hajime Wada

  2. National Institute for Basic Biology, Okazaki, Japan

    Norio Murata

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Los, D.A., Zinchenko, V.V. (2009). Regulatory Role of Membrane Fluidity in Gene Expression. In: Wada, H., Murata, N. (eds) Lipids in Photosynthesis. Advances in Photosynthesis and Respiration, vol 30. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-2863-1_15

Download citation

Publish with us

Policies and ethics

Search

Navigation