Skip to main content
SpringerLink
Log in

Photoinhibition of photosynthesis in chilled potato leaves is not correlated with a loss of Photosystem-II activity

Preferential inactivation of Photosystem I

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

When 23 °C-grown potato leaves (Solanum tuberosum L.) were irradiated at 23 °C with a strong white light, photosynthetic electron transport and Photosystem-II (PS II) activity were inhibited in parallel. When the light treatment was given at a low temperature of 3 °C, the photoinhibition of photosynthesis was considerably enhanced, as expected. Surprisingly, no such stimulation of photoinhibition was observed with respect to the PS II function. A detailed functional analysis of the photosynthetic apparatus, using in-vivo fluorescence, absorbance, oxygen and photoacoustic measurements, and artificial electron donors/acceptors, showed a pronounced alteration of PS I activity during light stress at low temperature. More precisely, it was observed that both the pool of photooxidizeable reaction center pigment (P700) of PS I and the efficiency of PS I to oxidize P700 were dramatically reduced. Loss of P700 activity was shown to be essentially dependent on atmospheric O2 and to require a continued flow of electrons from PS II, suggesting the involvement of the superoxide anion radical which is produced by the interaction of O2 and the photosynthetic electron-transfer chain through the Mehler reaction. Mass spectrometric measurements of O2 exchange by potato leaves under strong illumination did not reveal, however, any stimulation of the Mehler reaction at low temperature, thus leading to the conclusion that O2 toxicity mainly resulted from a chilling-induced inhibition of the scavenging system for O2-radicals. Support for this interpretation was provided by the light response of potato leaves infiltrated with an inhibitor (diethyldithiocarbamate) of the chloroplastic Cu-Zn superoxide dismutase. It was indeed possible to simulate the differential inhibition of the PS II photochemical activity and the linear electron transport observed during light stress at low temperature by illuminating at 23 °C diethyldithiocarbamate-poisoned leaves. The experimental data presented here suggests that (i) the previously reported resistance of PS I to photoinhibition damage in-vivo is not an intrinsic property of PS I but results from efficient protective systems against O2 toxicity, (ii) PS I is photoinhibited in chilled potato leaf due to the inactivation of this PS I defence system and (iii) PS I is more sensitive to superoxide anion radicals than PS II.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

PS -:

Photosystem

E -:

Emerson enhancement

φ popen and φP :

maximal and actual quantum yields of PS II photochemistry

DDC -:

diethyldithiocarbamate

QA and QB -:

primary and secondary (quinone) electron acceptors of PS II

P680 and P700 -:

reaction center pigments of PS II and PS I, respectively

SOD -:

superoxide dismutase

References

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

    PubMed  Google Scholar 

  • Asada K and Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB and Arntzen CJ (eds) Photoinhibition, pp 227–287. Elsevier, Amsterdam

    Google Scholar 

  • Asada K, Heber U and Schreiber U (1992) Pool size of electrons that can be donated to P700+, as determined in intact leaves: Donation to P700+ from stromal components via the intersystem chain. Plant Cell Physiol 33: 927–932

    Google Scholar 

  • Badger MR and Andrews TJ (1974) Effects of CO2, O2 and temperature on a high-affinity form of ribulose diphosphate carboxylase/oxygenase from spinach. Biochem Biophys Res Commun 60: 204–210

    PubMed  Google Scholar 

  • Baker NR, Long SP and Ort DR (1988) Photosynthesis and temperature, with particular reference to effects on quantum yield. In: Long SP and Woodward FI (eds) Plants and Temperature, pp 347–375. The Company of Biologists Limited, Cambridge

    Google Scholar 

  • Barényi B and Krause GH (1985) Inhibition of photosynthetic reactions by light. A study with isolated spinach chloroplasts. Planta 163: 218–226

    Google Scholar 

  • Bukhov NG, Mohanty P, Rakhimberdieva MG and Karapetyan NV (1992) Analysis of dark-relaxation kinetics of variable fluorescence in intact leaves. Planta 187: 122–127

    Article  Google Scholar 

  • Canaani O and Malkin S (1984) Distribution of light excitation in an intact leaf between the two photosystems of photosynthesis. Changes in absorption cross-section following state 1-state 2 transitions. Biochim Biophys Acta 766: 513–524

    Google Scholar 

  • Canaani O, Havaux M and Malkin S (1986) Hydroxylmanine, hydrazine and methylamine donate electrons to the photooxidizing side of Photosystem II in leaves inhibited in oxygen evolution due to water stress. Biochim Biophys Acta 851: 151–155

    Google Scholar 

  • Delieu T and Walker DA (1983) Simultaneous measurement of oxygen evolution and chlorophyll fluorescence from leaf pieces. Plant Physiol 73: 534–541

    Google Scholar 

  • Dimon B, Gans P and Peltier G (1987) Mass-spectrometric measurement of photosynthetic and respiratory oxygen exchange. Methods Enzymol 167: 686–691

    Google Scholar 

  • Fridovich I (1986) Biological effects of superoxide radical. Arch Biochem Biophys 247: 1–11

    PubMed  Google Scholar 

  • Genty B, Briantais J-M and Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990: 87–92

    Google Scholar 

  • Gerber DW and Burris JE (1981) Photoinhibition and P700 in the marine diatom Amphora sp. Plant Physiol 68: 699–702

    Google Scholar 

  • Greenbaum NL and Mauzerall DC (1991) Effect of irradiance level on distribution of chlorophylls between PS II and PS I as determined from optical cross-sections. Biochim Biophys Acta 1057: 195–207

    Google Scholar 

  • Haehnel W and Trebst A (1982) Localization of electron transport inhibition in plastoquinone reactions. J Bioenerg Biomembr 14: 181–190

    PubMed  Google Scholar 

  • Harvey GW and Bishop NI (1978) Photolability of photosynthesis in two separate mutants of Scenedesmus obliouus. Plant Physiol 62: 330–336

    Google Scholar 

  • Havaux M (1993) Characterization of thermal damage to the photosynthetic electron transport system in potato leaves. Plant Sci (in press)

  • Havaux M and Eyletters M (1991) Is the in vivo Photosystem I function resistant to photoinhibition? An answer from photoacoustic and far-red absorbance measurements in intact leaves. Z Naturforsch 46c: 1038–1044

    Google Scholar 

  • Havaux M, Strasser RJ and Greppin H (1991a) A theoretical and experimental analysis of the qP and qN coefficients of chlorophyll fluorescence quenching and their relation to photochemical and non-photochemical events. Photosynth Res 27: 41–55

    Google Scholar 

  • Havaux M, Greppin H and Strasser RJ (1991b) Functioning of Photosystems I and II in pea leaves exposed to heat stress in the presence or absence of light. Planta 186: 88–98

    Article  Google Scholar 

  • Herbert SK, Samson G, Fork DC and Laudenbach DE (1992) Characterization of damage to Photosystems I and II in a cyanobacterium lacking detectable iron superoxide dismutase activity. Proc Natl Acad Sci USA 89: 8716–8720

    PubMed  Google Scholar 

  • Hodgson RAJ and Raison JK (1989) Inhibition of photosynthesis by chilling in moderate light: A comparison of plants sensitive and insensitive to chilling. Planta 178: 545–552

    Google Scholar 

  • Hodgson RAJ and Raison JK (1991) Superoxide production by thylakoids during chilling and its implication in the susceptibility of plants to chilling-induced photoinhibition. Planta 183: 222–228

    Article  Google Scholar 

  • Inoue K, Sakurai H and Hiyama T (1986) Photoinactivation sites of Photosystem I in isolated chloroplasts. Plant Cell Physiol 27: 961–968

    Google Scholar 

  • Izawa S (1980) Acceptors and donors for chloroplast electron transport. Methods Enzymol 69: 413–433

    Google Scholar 

  • Jung J and Kim H-S (1990) The chromophores as endogenous sensitizers involved in the photogeneration of singlet oxygen in spinach thylakoids. Photochem Photobiol 52: 1003–1009

    Google Scholar 

  • Jung J and Kim YW (1991) Involvement of thylakoid membrane-dependent photosensitization in photoinhibition of the Calvin cycle activity in spinach chloroplasts. Photochem Photobiol 54: 833–839

    Google Scholar 

  • Kim CS, Han GH, Kim JM and Jung J (1993) In situ susceptibilities of Photosystems I and II to photosensitized inactivation via singlet oxygen mechanism. Photochem Photobiol 57: 1069–1074

    Google Scholar 

  • Kitajima M and Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376: 105–115

    PubMed  Google Scholar 

  • Klughammer C and Schreiber U (1991) Analysis of light-induced absorbance changes in the near-infrared spectral region. I. Characterization of various components in isolated chloroplasts. Z Naturforsch 46c: 233–244

    Google Scholar 

  • Knox JP and Dodge AD (1985) Singlet oxygen and plants. Phytochemistry 24: 889–896

    Article  Google Scholar 

  • Lapointe L, Huner NPA, Carpentier R and Ottander C (1991) Resistance to low temperature photoinhibition is not associated with isolated thylakoid membranes of winter rye. Plant Physiol 97: 804–810

    Google Scholar 

  • Malkin S (1971) Fluorescence induction studies in isolated chloroplasts. III. On the electron-transfer equilibra in the pool of electron acceptors of Photosystem II. Biochim Biophys Acta 234: 415–427

    PubMed  Google Scholar 

  • Mannan RM, Whitmarsh J, Nyman P and Pakrasi HB (1991) Directed mutagenesis of an iron-sulfur protein of the Photosystem I complex in the filamentous cyanobacerium Anabaena variabilis ATCC 29413. Proc Natl Acad Sci USA 88, 10168–10172

    PubMed  Google Scholar 

  • Maridonneau I, Braguet P and Garay RP (1983) Na+ and K+ transport damage induced by oxygen free radicals in human red cell membranes. J Biol Chem 258: 3107–3113

    PubMed  Google Scholar 

  • Maxwell PC and Biggins J (1976) Role of cyclic electron transport in photosynthesis as measured by the photoinduced turnover of P700 in vivo. Biochemistry 15: 3975–3981

    PubMed  Google Scholar 

  • Melis A, Guenther GE, Morrissey PJ and Ghirardi ML (1988) Photosystem II heterogeneity in chloroplasts. In: Lichtenthaler HK (ed) Applications of Chlorophyll fluorescence, pp 33–43. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Mi H, Endo T, Schreiber U and Asada K (1992) Donation of electrons from cytosolic components to the intersystem chain in the cyanobacterium Synchococcus sp. PCC 7002 as determined by the reduction of P700+. Plant Cell Physiol 33: 1099–1105

    Google Scholar 

  • Myers J (1971) Enhancement studies in photosynthesis. Annu Rev Plant Physiol 22: 289–312

    Article  Google Scholar 

  • Nuijs AM, Shuvalov VA, vanGorkom HJ, Plijter JJ and Duysens LNM (1986) Picosecond absorbance difference spectroscopy on the primary reactions and the antenna-excited states in Photosystem I particles. Biochim Biophys Acta 850: 310–318

    Google Scholar 

  • Öquist G, Greer DH and Ögren E (1987) Light stress at low temperature. In: Kyle DJ, Osmond CB and Arntzen DJ (eds) Photoinhibition, pp 67–87. Elsevier, Amsterdam

    Google Scholar 

  • Ortiz-Lopez A, Nie GY, Ort DR and Baker NR (1990) The involvement of the photoinhibition of Photosystem II and impaired membrane energization in the reduced quantum yield of carban assimilation in chilled maize. Planta 181: 78–84

    Article  Google Scholar 

  • Poulet P, Cahen D and Malkin S (1983) Photoacoustic detection of photosynthetic oxygen evolution: Quantitative analysis by phase and amplitude measurements. Biochim Biophys Acta 275: 433–446

    Google Scholar 

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

    Google Scholar 

  • Prasil O, Adir N and Ohad I (1992) Dynamics of Photosystem II: mechanism of photoinhibition and recovery processes. In: Barber J (ed) The Photosystems: Structure, Function and Molecular Biology, pp 295–348. Elsevier, Amsterdam

    Google Scholar 

  • Ravenel J, Peltier G and Havaux M (1994) The cyclic electron pathways around Photosystem I in Chlamydomonas reinhardtii as determined in vivo by photoacoustic measurements of energy storage. Planta (in press).

  • Robinson HH and Crofts AR (1983) Kinetics of the oxidation-reduction reactions of the Photosystem II quinone acceptor complex, and the pathway for deactivation. FEBS Lett 153: 221–226

    Article  Google Scholar 

  • Salin ML (1987) Toxic oxygen species and protective systems of the chloroplast. Physiol Plant 72: 681–689

    Google Scholar 

  • Sassenrath GF, Ort DR and Portis AR (1987) Effect of chilling on the activity of enzymes of the photosynthetic carbon reduction cycle. In: Biggins J (ed) Progress in Photosynthesis Research, Vol IV, pp 103–106. Martinus Nijhoff Publishers, Dordrecht.

    Google Scholar 

  • Satoh K (1970) Mechanism of photoinactivation in photosynthetic systems. III. Site and mode of photoinactivation in Photosystem I. Plant Cell Physiol 11: 187–197

    Google Scholar 

  • Satoh K and Fork DC (1982) Photoinhibition of reaction centers of Photosystems I and II in intact Bryopsis chloroplasts under anaerobic conditions. Plant Physiol 70: 1004–1008

    Google Scholar 

  • Schöner S and Krause GH (1990) Protective systems against active oxygen species in spinach: response to cold acclimation in excess light. Planta 180: 383–389

    Article  Google Scholar 

  • Somersalo S and Krause GH (1989) Photoinhibition at chilling temperature. Fluorescence characteristics of unhardened and cold-acclimated spinach leaves. Planta 177: 409–416

    Google Scholar 

  • Strasser RJ (1986) Mono-, tri- and polypartite models of photosynthesis. Photosynth Res 10: 255–276

    Google Scholar 

  • Takahashi M and Asada K (1988) Superoxide production in aprotic interior of chloroplast thylakoids. Arch Biochem Biophys 267: 714–722

    PubMed  Google Scholar 

  • Terashima I, Funayama S and Sonoike K (1994) The site of photoinhibition of Cucumis sativus L. at low temperatures is Photosystem I, not Photosystem II. Planta (in press)

  • Tyystjärvi E, Ovaska J, Karunen P and Aro E-M (1989) The nature of light-induced inhibition of Photosystem II in pumpkin (Cucurbita pepo L.) leaves depends on temperature. Plant Physiol 91: 1069–1074

    Google Scholar 

  • VanGinkel G and Brown JS (1978) Endogenous catalase and superoxide dismutase activities in photosynthetic membranes. FEBS Lett 94: 284–286

    Article  Google Scholar 

  • Van Wijk KJ (1992) Photoinhibition of photosynthesis in higher plants: From Photosystem II particle to intact leaf. PhD Thesis, University of Groningen, The Netherlands

  • Yu L, Zhao J, Mühlenhoff U, Bryant DA and Golbeck JH (1993) PsaE is required for in vivo cyclic electron flow around Photosystem I in the cyanobacterium Synechococcus sp. PCC7002. Plant Physiol 103: 171–180

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Département de Physiologie Végétale et Ecosystèmes, CEA-Sciences du Vivant, Centre d'Etudes de Cadarache, F-13108, Saint-Paul-lez-Durance, France

    Michel Havaux & Alexis Davaud

Authors
  1. Michel Havaux
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexis Davaud
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Havaux, M., Davaud, A. Photoinhibition of photosynthesis in chilled potato leaves is not correlated with a loss of Photosystem-II activity. Photosynth Res 40, 75–92 (1994). https://doi.org/10.1007/BF00019047

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00019047

Key words

Search

Navigation