Abstract
Effects of n-propyl gallate, a plastid terminal oxidase inhibitor involved in chlororespiration, on photosystem II efficiency in Dunaliella bardawil under low or high illumination was investigated. Rapid chlorophyll a fluorescence transients were recorded and analyzed according to JIP-test, which can quantify the photosystem II performance. The fluorescence transients O-J-I-P drastically decreased and almost reached a plateau when low light-grown cells were exposed for 96 h to 1, 2 and 4 mM n-propyl gallate. Very similar reductions in the efficiency of quantum yield of primary photochemistry (Φpo), the quantum yield for electron transport (ΦEo) and the inferred water-splitting complex activity (Fv/Fo) were found in the same inhibitor concentrations. However, no statistically significant change in fluorescence intensity and photosystem II efficiency was found when algal cells were exposed to the inhibitor concentrations up to 2 mM under high light intensity. The results indicated that inhibitory effects of n-propyl gallate on photosystem II electron flow in D. bardawil cells are dependent on environmental conditions. It is also demonstrated that n-propyl gallate is a multi-target inhibitor of growth kinetics as well as photosynthesis. In addition, we found that the donor side of photosystem II acts as main target place of the inhibitor.
Similar content being viewed by others
References
Allen JF, Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci 6:317–326
Aluru MR, Rodermel SR (2004) Control of chloroplast redox by the IMMUTANS terminal oxidase. Physiol Plant 120:4–11
Appenroth KJ, Stockel J, Srivastava A, Strasser RJ (2001) Multiple effects of chromate on the photosynthetic apparatus of Spirodela polyrhiza as probe by OJIP chlorophyll a fluorescence measurements. Environ Pollut 115:49–64
Arnon D (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15
Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134
Asada K (1996) Radical production and scavenging in the chloroplasts. In: Baker NR (ed) Photosynthesis and the Environment. Kluwer Academic Publishers, Dordrecht, pp 128–150
Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639
Barber J, Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17:61–66
Ben-Amotz A, Avron M (1983) On the factors which determine massive β-Carotene accumulation in the halo-tolerant alga Dunaliella bardawil. Plant Physiol 72:593–597
Bussotti F, Strasser RJ, Schaub M (2007) Photosynthetic behavior of woody species under high ozone exposure probed with the JIP-test: a review. Environ Pollu 147:430–437
Chaudhuri A, Kar RK (2008) Inhibition of seed germination by propyl gallate, a free radical scavenger and recovery of germination by hydrogen peroxide and ethylene in Vigna Radiata. World J Agr Sci 4:914–921
Cournac L, Redding K, Ravenel J, Rumeau D, Josse EM, Kuntz M, Peltier G (2000) Electron flow between photosystem II and oxygen in chloroplasts of photosystem I-deficient algae is mediated by a quinol oxidase involved in chlororespiration. J Biol Chem 275:17256–17262
Diaz M, Haro VD, Munoz M, Quiles MJ (2007) Chlororespiration is involved in the adaptation of Brassica plants to heat and high light intensity. Plant Cell Environ 30:1578–1585
Einali A, Shariati M (2012) Effects of n-propyl gallate on photosynthesis and physiological parameters in Dunaliella salina are affected by stressful conditions. Braz J Plant Physiol 24:193–202
Einali A, Shariati M, Sato F, Endo T (2013) Cyclic electron transport around photosystem I and its relationship to non-photochemical quenching in unicellular green alga Dunaliella salina under nitrogen deficiency. J Plant Res 126:179–186
Elich TD, Edelman M, Mattoo AK (1997) Evidence for light-dependent and light independent protein dephosphorilation in chloroplasts. FEBS Lett 411:236–238
Forti G, Caldiroli G (2005) state transitions in Chlamydomonas reinhardtii. The role of the Mehler reaction in state 2-to-state 1 transition. Plant Physiol 137:492–499
Fricke W, Peters WS (2002) The biophysics of leaf growth in salt-stressed barley. A study at the cell level. Plant Physiol 129:374–388
Gamboa J, Munoz M, Quiles MJ (2009) Effects of antimycin a and n-propyl gallate on photosynthesis in sun and shade plants. Plant Sci 177:643–647
Georgakopoulos JH, Argyroudi-Akoyunoglou JH (1998) Thylakoid protein phosphorilation is suppressed by free radical scavengers. Correlation between PSII core protein degradation and thylakoid protein phosphorylation. Photosynth Res 58:269–280
Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22:131–160
Ibanez H, Ballester A, Munoz R, Quiles MJ (2010) Chlororespiration and tolerance to drought, heat and high illumination. J Plant Physiol 167:732–738
Jegershold C, Virgin I, Stryring S (1990) Light-dependent degradation of the D1 protein in photosystem II is accelerated after inhibition of the water splitting reaction. Biochemistry 29:6179–6186
Kalaji HM, Govindjee Bosa K, Koscielniak J, Zuk-Golaszewska K (2011) Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environ Exp Bot 73:64–72
Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349
Kuntz M (2004) Plastid terminal oxidase and its biological significance. Planta 218:896–899
Lepedus H, Begovic L, Mlinaric S, Cimic D, Stolfa I, Paradikovic N, Uzarevic Z, Jurkovic V, Cesar V (2011) Physiology and biochemistry of leaf bleaching in prematurely aging maple (acer saccharinum l.) trees. II. Functional and molecular adjustment of PSII. Acta Bot Croat 70:133–146
Lu CM, Vonshak A (2002) Effects of salinity stress on photosysten II function in cyanobacterial Spirulina platensis cells. Physiol Plant 114:405–413
Miyake C, Shinzaki Y, Miyata M, Tomizawa K (2004) Enhancement of cyclic electron flow around PSI at high light and its contribution to the induction of non-photochemical quenching of chl fluorescence in intact leaves of tobacco plants. Plant Cell Physiol 45:1426–1433
Miyake C, Miyata M, Shinzaki Y, Tomizawa K (2005) CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves—Relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of Chl fluorescence. Plant Cell Physiol 46:629–637
Nagata T, Todoriki S, Kikuchi S (2004) Radial expansion root cells and elongation of root hairs of Arabidopsis thaliana induced by massive doses of gamma irradiation. Plant Cell Physiol 45:1557–1565
Niyogi KK (2000) Safety valves for photosynthesis. Curr Opin Plant Biol 3:455–460
Pereira WE, Desiqueira DL, Martinez CA, Puiatti M (2000) Gas exchange and chlorophyll fluorescence in four citrus root stocks under aluminium stress. J Plant Physiol 157:513–520
Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35:15–44
Prasil O, Adir N, Ohad I (1992) Dynamics of photosystem II: mechanism of photoinhibition and recovery processes. In: Barber J (ed) The photosystems: structure, function, and molecular biology. Topics in photosynthesis, Vol 11. Elsevier Science Publishers, Amsterdam, pp 295–348
Quiles MJ (2006) Stimulation of chlororespiration by heat and high light intensity in Oat plants. Plant Cell Environ 29:1463–1470
Raghavan S, Hultin HO (2005) Model system for testing the efficacy of antioxidants in muscle foods. J Agr Food Chem 53:4572–4577
Rizhsky L, Hallak-Herr E, Van Breusegem F, Rachmilevitch S, Barr JE, Rodermel S, Inze D, Mittler R (2002) Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J 32:329–342
Rosso D, Ivanov AG, Fu A, Geisler-Lee J, Hendrickson L, Geisler M, Stewart G, Krol M, Hurry V, Rodermel SR, Maxwell DP, Huner NPA (2006) IMMUTANS does not act as a stress-induced safety valve in the protection of the photosynthetic apparatus of Arabidopsis during steady-state photosynthesis. Plant Physiol 142:574–585
Savitch LV, Massacci A, Gray GR, Huner NPA (2000) Acclimation to low temperature or high light mitigates sensitivity to photoinhibition: roles of the Calvin cycle and the Mehler reaction. Aust J Plant Physiol 27:253–264
Schoen M (1988) Cell counting. In: Lobban C, Champan D, Kermer BP (eds) Experimental phycology. Cambridge University Press, Cambridge
Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a non- intrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze ED, Caldwell MM (eds) Ecophysiology of photosynthesis. Springer, New York, pp 49–70
Shariati M, McC Lilley (1994) Loss of intracellular glycerol from Dunaliella by electroporation at constant osmotic pressure: subsequent restoration of glycerol content and associated volume changes. Plant Cell Environ 17:1295–1304
Sonoike K (1995) Selective photoinhibition of Photosystem I in isolated thylakoid membranes from cucumber and spinach. Plant Cell Physiol 36:825–830
Stirbet AD, Rosenau P, Stroder AC, Strasser RJ (2001) Parameter optimization of fast chlorophyll fluorescence induction model. Math Comput Simul 56:443–450
Strasser RJ, Stirbet AD (2001) Estimation of the energetic connectivity of PSII centres in plants using the fluorescence rise O-J-I-P fitting of experimental data to three different PSII models. Math Comput Simul 56:451–461
Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transients to address environmental questions: the JIP test. In: Mathis P (ed) Photosynthesis: from light to biosphere, vol 5. Kluwer Academic Publisher, Dordrecht, pp 977–980
Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42
Strasser RJ, Srivastava A, Tsimilli Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanisms. Regulation and adaptation. Taylor and Francis, London, pp 445–483
Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis, advances in photosynthesis and respiration. Vol. 19, Kluwer Academic Publishers, Dordrecht, pp 321–362
Tsimilli-Michael M, Eggenberg P, Biro B, Voros I, Koves-Pechy K, Strasser RJ (2000) Synergistic and antagonistic effects of Arbuscular mycorrhizal fungi and Azospirillum and Rhizobium nitrogen-fixers on the photosynthetic activity of alfalfa, probed by the polyphasic chlorophyll a fluorescence transient O-J-I-P. Appl Soil Ecol 15:169–182
Wang WQ, Chapman DJ, Barber J (1992) Inhibition of water splitting increases the susceptibility of photosystem II to photoinhibition. Plant Physiol 99:16–20
Xia J, Li Y, Zou D (2004) Effects of salinity stress on PSII in Ulva lactuca as probed by chlorophyll fluorescence measurements. Aqua Bot 80:129–137
Zurita JL, Jos A, Peso AD, Salguero M, Lopez-Artiguez M, Repetto G (2007) Ecotoxicological effects of the antioxidant additive propyl gallate in five aquatic systems. Water Res 41:2599–2611
Acknowledgments
This work was supported by Grants from UI Deputy of Research to M. S. We would also like to thank the USB Deputy of Research and Education for supporting A. E. during research.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Einali, A., Shariati, M. Effects of propyl gallate on photosystem II efficiency in Dunaliella bardawil under high illumination as investigated by chlorophyll fluorescence measurements. Theor. Exp. Plant Physiol. 27, 61–73 (2015). https://doi.org/10.1007/s40626-015-0032-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40626-015-0032-8