Early events in signalling high-temperature stress in tobacco BY2 cells involve alterations in membrane fluidity and enhanced hydrogen peroxide production

Plant, Cell and Environment

Volumn 31, Issue 12, 2008, Pages 1771-1780

  Königshofer, Helga ^a   Tromballa, Hans Walter ^b   Löppert, Hans Georg ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b UNIVERSITY OF VIENNA   (Austria)

Author keywords

Heat stress; Heat shock proteins; Temperature signalling

Indexed keywords

BENZYL ALCOHOL; CATION; DIPHENYLIODONIUM SALT; HEAT SHOCK PROTEIN; HYDROGEN PEROXIDE; VEGETABLE PROTEIN;

CYTOLOGY; ENVIRONMENTAL STRESS; HEAT SHOCK; HYDROGEN PEROXIDE; MEMBRANE; PROTEIN; SIGNALING; TEMPERATURE EFFECT; TOBACCO;

ARTICLE; CELL CULTURE; CELL MEMBRANE; CYTOLOGY; DRUG EFFECT; HEAT SHOCK RESPONSE; MEMBRANE FLUIDITY; METABOLISM; SIGNAL TRANSDUCTION; TOBACCO;

BENZYL ALCOHOL; CELL MEMBRANE; CELLS, CULTURED; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; HYDROGEN PEROXIDE; MEMBRANE FLUIDITY; ONIUM COMPOUNDS; PLANT PROTEINS; SIGNAL TRANSDUCTION; TOBACCO;

NICOTIANA TABACUM;

EID: 55949137644     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2008.01880.x     Document Type: Article

References (52)

1. Allan A.C. Fluhr R. (1997) Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. The Plant Cell 9, 1559 1572.
2. Apel K. Hirt H. (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373 399.
3. Banzet N., Richaud C., Deveaux Y., Kazmaizer M., Gagnon J. Triantaphylides C. (1998) Accumulation of small heat shock proteins, including mitochondrial HSP22, induced by oxidative stress and adaptive response in tomato cells. The Plant Journal 13, 519 527.
4. Bowler C. Fluhr R. (2000) The role of calcium and activated oxygens as signals for controlling cross-tolerance. Trends in Plant Science 5, 241 246.
5. Bradford M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248 254.
6. Browse J. Xin Z. (2001) Temperature sensing and cold acclimation. Current Opinion in Plant Biology 4, 241 246.
7. Carratù L., Franceschelli S., Pardini C.L., Kobayashi G.S., Horvath I., Vigh L. Maresca B. (1996) Membrane lipid perturbation modifies the set point of the temperature of heat shock response in yeast. Proceedings of the National Academy of Sciences of the United States of America 93, 3870 3875.
8. Cazalé A.-C., Rouet-Mayer M.-A., Barbier-Brygoo H., Mathieu Y. Laurière C. (1998) Oxidative burst and hypoosmotic stress in tobacco cell suspensions. Plant Physiology 116, 659 669.
9. 2+ wave propagation in Fucus rhizoid cells. The Plant Cell 14, 2369 2381.
10. Dat J., Vandenabeele S., Vranova E., Van Montagu M., Inze D. Van Breusegem F. (2000) Dual action of the active oxygen species during plant stress responses. Cellular and Molecular Life Sciences 57, 779 795.
11. 2+- and K+-permeable channels in plant root cells. Journal of Cell Science 116, 81 88.
12. Desikan R., Hancock J.T., Coffey M.J. Neill S.J. (1996) Generation of active oxygen in elicited cells of Arabidopsis thaliana is mediated by a NADPH oxidase-like enzyme. FEBS Letters 382, 213 217.
13. Desikan R., Reynolds A., Hancock J.T. Neill S.J. (1998) Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on gene expression in Arabidopsis suspension cultures. Biochemical Journal 330, 115 120.
14. Desikan R., A.-H.-Mackerness S., Hancock J.T. Neill S.J. (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiology 127, 159 172.
15. Dwyer S.C., Legendre L., Low P.S. Leto T.L. (1996) Plant and human neutrophil oxidative burst complexes contain immunologically related proteins. Biochimica et Biophysica Acta 1289, 231 237.
16. Foreman J., Demidchik V., Bothwell J.H.F., Mylona P., Miedema H., Torres M.A., Linstead P., Costa S., Brownlee C. Jones J.D.G. (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442 446.
17. Foyer C.H., Lelandais M. Kunert K.J. (1994) Photooxidative stress in plants. Physiologia Plantarum 92, 696 717.
18. Foyer C.H., Lopez-Delgado H., Dat J.F. Scott I.M. (1997) Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiologia Plantarum 100, 241 254.
19. Groom Q.J., Torres M.A., Fordham-Skelton A.P., Hammond-Kosack K.E., Robinson N.J. Jones J.D.G. (1996) rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene. The Plant Journal 10, 515 522.
20. Grote K., Flach I., Luchtefeld M., Akin E., Holland S.M., Drexler H. Schieffer B. (2003) Mechanical stretch enhances mRNA expression and proenzyme release of matrix metalloproteinase-2 (MMP-2) via NAD(P)H oxidase-derived reactive oxygen species. Circulation Research 92, e80 e86.
21. Horváth I., Glatz A., Varvasovszki V., et al. (1998) Membrane physical state controls the signalling mechanism of the heat shock response in Synechocystis PCC 6803: identification of hsp 17 as a 'fluidity gene'. Proceedings of the National Academy of Sciences of the United States of America 95, 3513 3518.
22. 2+ binding motifs. The Plant Cell 10, 255 266.
23. Kitagawa S. Hirata H. (1992) Effects of alcohols on fluorescence anisotropies of diphenyl hexatriene and its derivatives in bovine blood platelets: relationships of the depth-dependent change in membrane fluidity by alcohols with their effects on platelet aggregation and adenylate cyclase activity. Biochimica et Biophysica Acta 1112, 14 18.
24. Knight H. Knight M.R. (1999) Calcium signalling in plants responding to stress. In Plant Responses To Environmental Stress (eds M.F. Smallwood, C.M. Calvert D.J. Bowles pp. 1 8. BIOS Scientific Publishers, Oxford, UK.
25. Königshofer H. Lechner S. (2002) Are polyamines involved in the synthesis of heat-shock proteins in cell suspension cultures of tobacco and alfalfa in response to high-temperature stress? Plant Physiology and Biochemistry 40, 51 59.
26. Kwak J.M., Mori I.C., Pei Z.-M., Leonhardt N., Torres M.A., Dangl J.L., Bloom R.E., Bodde S., Jones J.D.G. Schroeder J.I. (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. The EMBO Journal 22, 2623 2633.
27. Laemmli U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680 685.
28. Lee B.H., Won S.H., Lee H.S., Miyao M., Chung W.I., Kim I.J. Jo J. (2000) Expression of the chloroplast-located small heat shock protein by oxidative stress in rice. Gene 245, 283 290.
29. Madey E., Nowack L.M., Su L., Hong Y., Hudak K.A. Thompson J.E. (2001) Characterization of plasma membrane domains enriched in lipid metabolites. Journal of Experimental Botany 52, 669 679.
30. Mittler R., Vanderauwera S., Gollery M. Van Breusegem F. (2004) Reactive oxygen gene network of plants. Trends in Plant Science 9, 490 498.
31. Monroy A.F. Dhindsa R.S. (1995) Low-temperature signal transduction: induction of cold acclimation-specific genes of alfalfa by calcium at 25°C. The Plant Cell 7, 321 331.
32. 2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant Physiology 135, 702 708.
33. Mosmann T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunological Methods 65, 55 63.
34. Murata N. Los D.A. (1997) Membrane fluidity and temperature perception. Plant Physiology 115, 875 879.
35. Neill S.J., Desikan R., Clarke A., Hurst R. Hancock J. (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. Journal of Experimental Botany 53, 1237 1247.
36. Orozco-Cardenas M. Ryan C.A. (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proceedings of the Natlional Academy of Sciences of the United States of America 96, 6553 6557.
37. Örvar B.L., Sangwan V., Omann F. Dhindsa R.S. (2000) Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. The Plant Journal 23, 785 794.
38. Pei Z.-M., Murata Y., Benning G., Thomine S., Klüsener B., Allen G.I., Grill E. Schroeder J.I. (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406, 731 734.
39. Pellinen R., Palva T. Kangasjärvi J. (1999) Subcellular localization of ozone-induced hydrogen peroxide production in birch (Betula pendula) leaf cells. The Plant Journal 20, 349 356.
40. Plieth C., Hansen U.-P., Knight H. Knight M.R. (1999) Temperature sensing by plants: the primary characteristics of signal perception and calcium response. The Plant Journal 18, 491 497.
41. Rouet-Mayer M.A., Mathieu Y., Cazalé A.C., Guern J. Lauriè C. (1997) Extracellular alkalinization and oxidative burst induced by fungal pectin lyase in tobacco cells are not due to the perception of oligogalacturonide fragments. Plant Physiology and Biochemistry 35, 321 330.
42. 2+ influx. The Plant Journal 27, 1 12.
43. Sangwan V., Örvar B.L., Beyerly J., Hirt H. Dhindsa R.S. (2002) Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. The Plant Journal 31, 629 638.
44. Suri S.S. Dhindsa R.S. (2008) A heat-activated MAP kinase (HAMK) as a mediator of heat shock response in tobacco cells. Plant, Cell & Environment 31, 218 226.
45. Suzuki I., Los D.A., Kanesaki Y., Mikami K. Murata N. (2000) The pathway for perception and transduction of low-temperature signals in Synechocystis. The EMBO Journal 19, 1327 1334.
46. Torres M.A., Onouchi H., Hamada S., Machida C., Hammond-Kossack K.E. Jones J.D.G. (1998) Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). The Plant Journal 14, 365 370.
47. Vacca R.A., De Pinto M.C., Valenti D., Passarella S., Marra E. De Gara L. (2004) Production of reactive oxygen species, alteration of cytosolic ascorbate peroxidase, and impairment of mitochondrial metabolism are early events in heat shock-induced programmed cell death in tobacco bright-yellow 2 cells. Plant Physiology 134, 1100 1112.
48. Vandenabeele S., Van der Kelen K., Dat J., et al. (2003) A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proceedings of the National Academy of Sciences of the United States of America 100, 16113 16118.
49. Vierling E. (1997) The small heat shock proteins in plants are members of an ancient family of heat induced proteins. Acta Physiologiae Plantarum 19, 539 547.
50. Vigh L., Maresca B. Harwood J. (1998) Does the membrane's physical state control the expression of heat shock and other genes? Trends in Biochemical Sciences 23, 369 374.
51. 2 is required for effective expression of heat shock genes in Arabidopsis. Plant Molecular Biology 61, 733 746.
52. Waters E.R., Lee G.J. Vierling E. (1996) Evolution, structure and function of the small heat shock proteins in plants. Journal of Experimental Botany 47, 325 338.