Home LiteratureArticle Details
PMID: 24311216 Published · ppublish English Journal Article

Photoinhibition of photosynthesis in chilled potato leaves is not correlated with a loss of Photosystem-II activity : Preferential inactivation of Photosystem I.

Photosynthesis research ·Vol. 40 ·No. 1 ·1994-04-00 ·Pages 75-92

Havaux M, Davaud A

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.

Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Havaux M
Département de Physiologie Végétale et Ecosystèmes, CEA-Sciences du Vivant, Centre d'Etudes de Cadarache, F-13108, Saint-Paul-lez-Durance, France.
Davaud A
References (29)
29 references, click to expand
  1. The involvement of the photoinhibition of photosystem II and impaired membrane energization in the reduced quantum yield of carbon assimilation in chilled maize.
    Planta. 1990 Apr;181(1):78-84 PMID: 24196677
  2. Fluorescence induction studies in isolated chloroplasts. 3. On the electron-transfer equilibria in the pool of electron acceptors of photosystem II.
    Biochim Biophys Acta. 1971 Jun 15;234(3):415-27 PMID: 5117580
  3. Simultaneous measurement of oxygen evolution and chlorophyll fluorescence from leaf pieces.
    Plant Physiol. 1983 Nov;73(3):534-41 PMID: 16663254
  4. Directed mutagenesis of an iron-sulfur protein of the photosystem I complex in the filamentous cyanobacterium Anabaena variabilis ATCC 29413.
    Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10168-72 PMID: 1658798
  5. A theoretical and experimental analysis of the qP and q N coefficients of chlorophyll fluorescence quenching and their relation to photochemical and nonphotochemical events.
    Photosynth Res. 1991 Jan;27(1):41-55 PMID: 24414444
  6. Characterization of damage to photosystems I and II in a cyanobacterium lacking detectable iron superoxide dismutase activity.
    Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8716-20 PMID: 1528884
  7. Biological effects of the superoxide radical.
    Arch Biochem Biophys. 1986 May 15;247(1):1-11 PMID: 3010872
  8. PsaE Is Required for in Vivo Cyclic Electron Flow around Photosystem I in the Cyanobacterium Synechococcus sp. PCC 7002.
    Plant Physiol. 1993 Sep;103(1):171-180 PMID: 12231924
  9. Inhibition of photosynthetic reactions by light : A study with isolated spinach chloroplasts.
    Planta. 1985 Feb;163(2):218-26 PMID: 24249342
  10. Photolability of Photosynthesis in Two Separate Mutants of Scenedesmus obliquus: Preferential Inactivation of Photosystem I.
    Plant Physiol. 1978 Sep;62(3):330-6 PMID: 16660511
  11. Role of cyclic electron transport in photosynthesis as measured by the photoinduced turnover of P700 in vivo.
    Biochemistry. 1976 Sep 7;15(18):3975-81 PMID: 963015
  12. Photoinhibition at chilling temperature : Fluorescence characteristics of unhardened and cold-acclimated spinach leaves.
    Planta. 1989 Mar;177(3):409-16 PMID: 24212435
  13. Photoinhibition of Photosystem II. Inactivation, protein damage and turnover.
    Biochim Biophys Acta. 1993 Jul 5;1143(2):113-34 PMID: 8318516
  14. The Nature of Light-Induced Inhibition of Photosystem II in Pumpkin (Cucurbita pepo L.) Leaves Depends on Temperature.
    Plant Physiol. 1989 Nov;91(3):1069-74 PMID: 16667113
  15. Analysis of dark-relaxation kinetics of variable fluorescence in intact leaves.
    Planta. 1992 Apr;187(1):122-7 PMID: 24177976
  16. Photoinhibition and P700 in the Marine Diatom Amphora sp.
    Plant Physiol. 1981 Sep;68(3):699-702 PMID: 16661982
  17. Photoinhibition of Reaction Centers of Photosystems I and II in Intact Bryopsis Chloroplasts under Anaerobic Conditions.
    Plant Physiol. 1982 Oct;70(4):1004-8 PMID: 16662603
  18. Localization of electron transport inhibition in plastoquinone reactions.
    J Bioenerg Biomembr. 1982 Jun;14(3):181-90 PMID: 7096321
  19. Superoxide production by thylakoids during chilling and its implication in the susceptibility of plants to chilling-induced photoinhibition.
    Planta. 1991 Jan;183(2):222-8 PMID: 24193624
  20. Functioning of photosystems I and II in pea leaves exposed to heat stress in the presence or absence of light : Analysis using in-vivo fluorescence, absorbance, oxygen and photoacoustic measurements.
    Planta. 1991 Dec;186(1):88-98 PMID: 24186579
  21. Mono- bi- tri- and polypartite models in photosynthesis.
    Photosynth Res. 1986 Jan;10(3):255-76 PMID: 24435372
  22. Effects of CO2, O2 and temperature on a high-affinity form of ribulose diphosphate carboxylase-oxygenase from spinach.
    Biochem Biophys Res Commun. 1974 Sep 9;60(1):204-10 PMID: 4418741
  23. Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone.
    Biochim Biophys Acta. 1975 Jan 31;376(1):105-15 PMID: 1125215
  24. Resistance to low temperature photoinhibition is not associated with isolated thylakoid membranes of winter rye.
    Plant Physiol. 1991 Oct;97(2):804-10 PMID: 16668470
  25. Protective systems against active oxygen species in spinach: response to cold acclimation in excess light.
    Planta. 1990 Feb;180(3):383-9 PMID: 24202017
  26. Na+ and K+ transport damage induced by oxygen free radicals in human red cell membranes.
    J Biol Chem. 1983 Mar 10;258(5):3107-13 PMID: 6298224
  27. Superoxide production in aprotic interior of chloroplast thylakoids.
    Arch Biochem Biophys. 1988 Dec;267(2):714-22 PMID: 2850770
  28. Inhibition of photosynthesis by chilling in moderate light: a comparison of plants sensitive and insensitive to chilling.
    Planta. 1989 Dec;178(4):545-52 PMID: 24213052
  29. Photosynthesis and temperature, with particular reference to effects on quantum yield.
    Symp Soc Exp Biol. 1988;42:347-75 PMID: 3077864
Article Info
Journal
Photosynthesis research
Abbr.
Photosynth Res
ISSN
0166-8595
Published
1994-04-00
Pages
75-92
Language
English
Region
Netherlands
NLM ID
100954728
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]