Electron Transport Activities of Isolated Thylakoids from Wheat Plants Grown in Salicylic Acid

Abstract

Wheat (Triticum aestivum cv. Sonalika) plants were grown with three different concentrations of salicylic acid (SA; 50/500/1000 μM) for 7 days and the effects on the level of thylakoid photochemical activities were examined. SA treatment stimulated photosystem II-catalyzed electron flow in all concentrations tested. Photosystem I-associated electron transport activity was stimulated at low concentrations of SA (50 μM) but at higher concentrations (500 and 1000 μM) the electron transport activity was drastically attenuated. Thylakoids isolated from the leaves of seedlings grown with high concentrations of SA (500 and 1000 μM) showed a substantial reduction in uncoupler (NH₄Cl)-mediated stimulation in electron flow. In addition, they failed to support ADP-dependent stimulation of electron transport activity and induced a significant reduction in ATPase activity. Incubation of isolated thylakoids with SA, however, had no effect on thylakoid photofunction, indicating no direct effect of SA on photoelectron transport activity. Furthermore, high concentrations of SA specifically reduce the thylakoid cytochrome f₅₅₄ level. The results suggest that SA, depending on its concentration, imparts differential effects on the photofunction of thylakoids. A low concentration of SA favours photosynthetic activity while the high concentration induces drastic attenuation of photosynthetic activity because of the decline in cytochrome f₅₅₄.

Abbreviations

DCBQ: 2,6-dichloro-p-benzoquinone

DCMU: 3-(3′,4′ dichlorophenyl)-1′,1′-dimethylurea

DCIPH₂: 2,6-dichlorophenolindophenol-reduced

FeCN: ferricyanide

Hepes: (N-[2-Hydroxyethyl] piperazine-N′-[2-ethanesulfonic acid])

TMPDH₂: N,N,N,′N′-tetramethyl-p-phenylenediamine

ATPase - electron transport - photophosphorylation - salicylic acid - thylakoids - wheat

References

• 01 Allen,  A. C., and Fluhr,  R.. (1997);  Two distinct sources of reactive oxygen species in tobacco epidermal cells.  Plant Cell. 9 1559-1572
• 02 Anderson,  M. D.,, Chen,  Z.,, and Klessig,  D. F.. (1998);  Possible involvement of lipid peroxidation in salicylic acid-mediated induction of PR-1 gene expression.  Phytochemistry. 47 555-566
• 03 Bendall,  D. S.,, Davenport,  H. E.,, and Hill,  R.. (1971) Cytochrome components in chloroplasts of higher plant. Methods in Enzymology, Vol. 23, Part A (San Pietro, A., ed.) Photosynthesis. Colowick, S. P. and Kaplan, N. O., Series eds. New York, London; Academic Press pp. 327-344
• 04 Chavez,  E.,, Bravo,  C.,, Gil,  H. A.,, and Reyes,  P. A.. (1985);  Ionophoretic-like action of diflunisal.  Life Science. 37 1491-1498
• 05 Chen,  P. S.,, Toribara,  J. T.,, and Warner,  H.. (1956);  Micro determination of phosphorus.  Analytical Chemistry. 28 1756-1758
• 06 Chen,  Z.,, Ricigliano,  J. W.,, and Klessig,  F.. (1993);  Purification and characterization of a soluble salicylic acid-binding protein from tobacco.  Proceedings of National Academy of Sciences (USA). 90 9533-9537
• 07 Dat,  J. F.,, Lopez-Delgado,  H.,, Foyer,  C. H.,, and Scott,  I. M.. (1998);  Parallel changes in H₂O₂ and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings.  Plant Physiology. 116 1351-1357
• 08 Durner,  J., and Klessig,  F.. (1996);  Salicylic acid is a modulator of tobacco and mammalian catalase.  Journal of Biological Chemistry. 271 28492-28501
• 09 Golbeck,  J. H.. (1987);  Structure, function and organization of the photosystem I reaction center complex.  Biochemica Biophysica Acta. 895 167-204
• 10 Gutknecht,  J.. (1990);  Salicylate and proton transport through lipid bilayer membranes: a model for salicylate-induced uncoupling and swelling in mitochondria.  Journal of Membrane Biology. 115 253-260
• 11 Harper,  J. P., and Balke,  N. E.. (1981);  Characterization of the inhibition of K⁺ absorption in oat roots by salicylic acid.  Plant Physiology. 68 1349-1353
• 12 Henry,  L. E. A., and Moller,  L. B.. (1981);  Polypeptide composition of an oxygen evolving photosystem II vesicle from spinach chloroplasts.  Carlsberg Research Communication. 46 227-242
• 13 Hoagland,  D. R., and Arnon,  D. I.. (1950);  The water culture method of growing plants without soil.  California Agricultural Experimental Station. Circular.. 374 1-32
• 14 Jorgensen,  T. G.,, Weis-Fogh,  U. S.,, Nielsen,  H. H.,, and Olesen,  H. P.. (1976);  Salicylate and aspirin-induced uncoupling of oxidative phosphorylation in mitochondria isolated from the mucosal membrane of the stomach.  Scand. J. Clin. Lab. Invest.. 36 649-654
• 15 Kimimura,  M., and Katoh,  S.. (1972);  Studies on electron transport associated with PS I. 1. Functional site of plastocyanin: Inhibitory effect of HgCl₂ on electron transport and plastocyanin in chloroplasts.  Biochim. Biophys. Acta. 283 279-292
• 16 Kok,  B.. (1976) Photosynthesis, the path of energy. Plant Biochem. Bonner, J. and Varner, J. E., eds. New York; Academic Press pp. 845-885
• 17 Kvaratskhelia,  M.,, George,  S. J.,, and Thorneley,  R. N. F.. (1997);  Salicylic acid is a reducing substrate and not an effective inhibitor of ascorbate peroxidase.  J. Biol. Chem.. 272 20998-21001
• 18 Larque-Saavedra,  A.. (1978);  The antitranspirant effect of acetylsalicylic acid in Phaseolus vulgaris. .  Plant Physiology. 43 126-128
• 19 Lian,  B.,, Zhou,  X.,, Miransari,  M.,, and Smith,  D. L.. (2000);  Effects of salicylic acid on the development and root nodulation of soybean seedlings.  Journal of Agronomy and Crop Science. 185 187-192
• 20 Lopez-Delgado,  H.,, Dat,  J. F.,, Foyer,  C. H.,, and Scott,  I. M.. (1998);  Induction of thermotolerance in potato microplants by acetylsalicylic acid and H₂O₂.  Journal of Experimental Botany. 49 713-720
• 21 Macri,  F.,, Vianello,  A.,, and Pennazio,  S.. (1986);  Salicylate-collapsed membrane potential in pea stem mitochondria.  Physiologia Plantarum. 67 136-140
• 22 Malamy,  J., and Klessig,  D. F.. (1992);  Salicylic acid and plant disease resistance.  The Plant Journal. 2 643-654
• 23 Marsho,  T. V., and Kok,  B.. (1971) Detection and isolation of P₇₀₀. Methods in Enzymology, Vol. 23, Part A (San Pietro, A., ed.) Photosynthesis. Colowick, S. P. and Kaplan, N. O., Series eds. New York, London; Academic Press pp. 515-522
• 24 Metraux,  J. P.,, Singer,  H.,, Ryals,  J.,, Ward,  E.,, Blum,  W.,, and Inveradi,  B.. (1990);  Increase in salicylic acid at the onset of systemic acquired resistance in cucumber.  Science. 250 10004-10006
• 25 Mills,  J. D.. (1986) Photophosphorylation. Photosynthesis Energy Transduction. A Practical Approach. Hipkins, M. F. and Baker, N. R., eds. Oxford-Washington; IRL Press pp. 143-187
• 26 Mishra,  A., and Choudhuri,  M. A.. (1997);  Ameliorating effects of salicylic acid on lead and murcury-induced inhibition of germination and early seeedling growth of two rice cultivars.  Seed Science and Technology. 25 263-270
• 27 Mishra,  A., and Choudhuri,  M. A.. (1999);  Effects of salicylic acid on heavy metal-induced membrane deterioration mediated by lipoxygenase in rice.  Biologia Plantarum. 42 409-415
• 28 Molina,  A.,, Volarth,  S.,, Guyer,  D.,, Maleck,  K.,, Ryals,  J.,, and Ward,  E.. (1999);  Inhibition of protoporphyrin oxygen oxidase expression in Arabidopsis causes a lesion-mimic phenotype that induces systemic acquired resistance.  The Plant Journal. 17 667-678
• 29 Ort,  D. R., and Oxborough,  K.. (1992);  In situ regulation of chloroplast coupling factor activity.   Annual Review of Plant Physiology and Plant Molecular Biology. 43 269-291
• 30 Pancheva,  T. V.,, Popova,  L. P.,, and Uzunova,  A. N.. (1996);  Effects of salicylic acid on growth and photosynthesis in barley plants.  Journal of Plant Physiology. 149 57-63
• 31 Pancheva,  T. V., and Popova,  L. P.. (1998);  Effect of salicylic acid on the synthesis of ribulose-1,5-bisphosphate carboxylase/oxygenase in barley leaves.  Journal of Plant Physiology. 152 381-386
• 32 Popova,  L.,, Pancheva,  T.,, and Uzunova,  A.. (1997);  Salicylic acid: Properties, biosynthesis and physiological role.  Bulgarian Journal of Plant Physiology. 23 85-93
• 33 Porra,  R. J.,, Thompson,  W. A.,, and Kriedemann,  P. E.. (1989);  Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy.  Biochimica Biophysica Acta. 975 384-394
• 34 Raskin,  I.. (1992 a);  Role of salicylic acid in plants.  Annual Review of Plant Physiology and Plant Molecular Biology. 43 439-463
• 35 Raskin,  I.. (1992 b);  Salicylate, a new plant hormone.  Plant Physiology. 99 799-803
• 36 Ruffera,  M.,, Steipeb,  B.,, and Zenka,  N. Z.. (1995);  Evidence against specific binding of salicylic acid to plant catalase.  FEBS Lett.. 377 175-180
• 37 Saha,  S.,, Izawa,  S.,, and Good,  N. E.. (1970);  Phosphorylation as a function of light intensity.  Biochemica Biophysica Acta. 223 158-164
• 38 Sanchez-Casas,  P., and Klessig,  D. F.. (1994);  A salicylic acid-binding activity and a salicylic acid-inhibitable catalase activity are present in a variety of plant species.  Plant Physiology. 106 1675-1679
• 39 van Rensen,  J. J. S.,, Wong,  D.,, and Govindjee. (1978);  Characterization of the inhibition of photosynthetic electron transport in pea chloroplasts by the herbicide 4,6-dinitro-o-Cresol by comparative studies with 3-(3,4-dichlorophenyl)-1,1-dimethyl urea.  Z. Naturforsch.. 33 C 413-420
• 40 Vernooij,  B.,, Friedrich,  L.,, Morse,  A.,, Reist,  R.,, Kolditz Jawhar,  R.,, Ward,  E.,, Uknes,  S.,, Kessmann,  H.,, and Ryals,  J.. (1994);  Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction.  Plant Cell. 6 959-968
• 41 Xie,  Z., and Chen,  Z.. (1999);  Salicylic acid induces rapid inhibition of mitochondrial electron transport and oxidative phosphorylation in tobacco cells.  Plant Physiology. 120 217-225
• 42 Yalpini,  N.,, Shulaev,  V.,, and Raskin,  I.. (1993);  Endogenous salicylic acid levels correlate with accumulation of pathogenesis-related proteins and virus resistance in tobacco.  Phytopathology. 83 702-708

Section Editor: U. Lüttge