Skip to main content
Log in

Effects of propyl gallate on photosystem II efficiency in Dunaliella bardawil under high illumination as investigated by chlorophyll fluorescence measurements

  • Published:
Theoretical and Experimental Plant Physiology Aims and scope Submit manuscript

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.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

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

    Article  CAS  PubMed  Google Scholar 

  • Aluru MR, Rodermel SR (2004) Control of chloroplast redox by the IMMUTANS terminal oxidase. Physiol Plant 120:4–11

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Arnon D (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Barber J, Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17:61–66

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Elich TD, Edelman M, Mattoo AK (1997) Evidence for light-dependent and light independent protein dephosphorilation in chloroplasts. FEBS Lett 411:236–238

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349

    Article  CAS  Google Scholar 

  • Kuntz M (2004) Plastid terminal oxidase and its biological significance. Planta 218:896–899

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Lu CM, Vonshak A (2002) Effects of salinity stress on photosysten II function in cyanobacterial Spirulina platensis cells. Physiol Plant 114:405–413

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Niyogi KK (2000) Safety valves for photosynthesis. Curr Opin Plant Biol 3:455–460

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35:15–44

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Quiles MJ (2006) Stimulation of chlororespiration by heat and high light intensity in Oat plants. Plant Cell Environ 29:1463–1470

    Article  CAS  PubMed  Google Scholar 

  • Raghavan S, Hultin HO (2005) Model system for testing the efficacy of antioxidants in muscle foods. J Agr Food Chem 53:4572–4577

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Schoen M (1988) Cell counting. In: Lobban C, Champan D, Kermer BP (eds) Experimental phycology. Cambridge University Press, Cambridge

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sonoike K (1995) Selective photoinhibition of Photosystem I in isolated thylakoid membranes from cucumber and spinach. Plant Cell Physiol 36:825–830

    CAS  Google Scholar 

  • Stirbet AD, Rosenau P, Stroder AC, Strasser RJ (2001) Parameter optimization of fast chlorophyll fluorescence induction model. Math Comput Simul 56:443–450

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Wang WQ, Chapman DJ, Barber J (1992) Inhibition of water splitting increases the susceptibility of photosystem II to photoinhibition. Plant Physiol 99:16–20

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Alireza Einali.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40626-015-0032-8

Keywords

Navigation