Abstract
The reduction of P700+, the primary electron donor of photosystem I (PSI), following a saturating flash of white light in the presence of the photosystem II (PSII) inhibitor 3-(3.4-dichlorophenyl)-1,1-dimethylurea (DCMU), was examined in barley plants exposed to a variety of conditions. The decay kinetic fitted to a double exponential decay curve, implying the presence of two distinct pools of PSI. A fast component, with a rate constant for decay of around 0.03–0.04 ms−1 was observed to be sensitive to the duration of illumination. This rate constant was slower than, but comparable to, that observed in non-inhibited samples (i.e. where linear flow was active). It was substantially faster than values typically reported for experiments where PSII activity is inhibited. The magnitude of this component rose in leaves that were dark-adapted or exposed to drought. This component was assigned to PSI centres involved in cyclic electron transport. The remaining slowly decaying P700+ population (rate constant of around 0.001–0.002 ms−1) was assigned to centres normally involved in linear electron transport (but inhibited here because of the presence of DCMU), or inactivated centres involved in the cyclic pathway. Processes that might regulate the relative flux through cyclic electron transport are discussed.
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Abbreviations
- DCMU:
-
3-(3.4-Dichlorophenyl)-1,1-dimethylurea
- ET:
-
Electron transport
- P700:
-
Primary donor of photosystem I
- PSI:
-
Photosystem I
- PSII:
-
Photosystem II
- ΔpH:
-
pH gradient across the thylakoid membrane
References
Albertsson P-A (2001) A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci 6:349–354
Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci 8:15–19
Arnon DI, Allen MB, Whatley FR (1954) Photosynthesis by isolated chloroplasts. Nature 174:394–396
Bendall DS, Manasse RS (1995) Cyclic photophosphorylation and electron transport. Biochim Biophys Acta 1229:23–38
Berry S, Rumberg B (1999) Proton to electron stoichiometry in electron transport of spinach thylakoids. Biochim Biophys Acta 1410:248–261
Burrows PA, Sazanov LA, Svab Z, Maliga P, Nixon PJ (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J 17:868–876
Clarke JE, Johnson GN (2001) In vivo temperature dependence of cyclic and pseudocyclic electron transport in barley. Planta 212:808–816
Cornic G, Bukhov NG, Wiese C, Bligny R, Heber U (2000) Flexible coupling between light-dependent electron and vectorial proton transport in illuminated leaves of C-3 plants. Role of photosystem I-dependent proton pumping. Planta 210:468–477
Egorova EA, Bukhov NG (2002) Effect of elevated temperatures on the activity of alternative pathways of photosynthetic electron transport in intact barley and maize leaves. Russ J Plant Physiol 49:575–584
Fork DC, Herbert SK (1993) Electron-transport and photophosphorylation by photosystem-I in-vivo in plants and cyanobacteria. Photosynth Res 36:149–168
Gerst U, Schreiber U, Neimanis S, Heber U (1995) Photosystem I-dependent cyclic electron flow contributes to the control of photosystem II in leaves when stomata close under water stress. In: Mathis P (ed) Photosynthesis: from light to biosphere, vol II. Kluwer, Dordrecht, pp 835–838
Golding AJ, Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218:107–114
Harbinson J, Foyer CH (1991) Relationships between the Efficiencies of photosystem-I and photosystem-II and stromal redox state in CO2-free air—evidence for cyclic electron flow in vivo. Plant Physiol 97:41–49
Harbinson J, Hedley CL (1993) Changes in P-700 oxidation during the early stages of the induction of photosynthesis. Plant Physiol 103:649–660
Harbinson J, Genty B, Baker NR (1989) Relationship between the quantum efficiencies of photosystem-I and photosystem-II in pea leaves. Plant Physiol 90:1029–1034
Heber U (2002) Irrungen, Wirrungen? The Mehler reaction in relation to cyclic electron transport in C3 plants. Photosynth Res 73:223–231
Heber U, Walker D (1992) Concerning a dual function of coupled cyclic electron-transport in leaves. Plant Physiol 100:1621–1626
Joet T, Cournac L, Peltier G, Havaux M (2002) Cyclic electron flow around photosystem I in C-3 plants. In vivo control by the redox state of chloroplasts and involvement of the NADH-dehydrogenase complex. Plant Physiol 128:760–769
Joliot P, Joliot A (2002) Cyclic electron transport in plant leaf. Proc Natl Acad Sci USA 99:10209–10214
Katona E, Neimanis S, Schonknecht G, Heber U (1992) Photosystem I-dependent cyclic electron-transport is important in controlling photosystem-II activity in leaves under conditions of water-stress. Photosynth Res 34:449–464
Lawlor DW (2002) Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and the role of ATP. Ann Bot 89:871–885
Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371
Ott T, Clarke J, Birks K, Johnson G (1999) Regulation of the photosynthetic electron transport chain. Planta 209:250–258
Rajagopal S, Bukhov NG, Tajmir-Riahi HA, Carpentier R (2003) Control of energy dissipation and photochemical activity in photosystem I by NADP-dependent reversible conformational changes. Biochemistry 42:11839–11845
Sacksteder CA, Kramer DM (2000) Dark-interval relaxation kinetics (DIRK) of absorbance changes as a quantitative probe of steady-state electron transfer. Photosynth Res 66:145–158
Sazanov LA, Burrows PA, Nixon PJ (1998) The chloroplast Ndh complex mediates the dark reduction of the plastoquinone pool in response to heat stress in tobacco leaves. FEBS Lett 429:115–118
Seelert H, Dencher NA, Muller DJ (2003) Fourteen protomers compose the oligomer III of the proton-rotor in spinach chloroplast ATP synthase. J Mol Biol 333: 337–344
Shinokazi K, Ohme M, Tanaka M, Wakasuki T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinokazi K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049
Sivak MN, Dietz KJ, Heber U, Walker DA (1985) The relationship between light-scattering and chlorophyll a fluorescence during oscillations in photosynthetic carbon assimilation. Arch Biochem Biophys 237:513–519
Acknowledgements
This work was completed during a research visit by G.N.J. and A.J.G. to the IBPC, Paris. All members of the UPR 1261 are thanked for their hospitality. The authors would like to thank Prof. Pierre Joliot (IBPC, Paris) in particular for many useful discussions. A.J.G. was in receipt of a UK Biotechnology and Biological Sciences Research Council studentship.
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Golding, A.J., Finazzi, G. & Johnson, G.N. Reduction of the thylakoid electron transport chain by stromal reductants—evidence for activation of cyclic electron transport upon dark adaptation or under drought. Planta 220, 356–363 (2004). https://doi.org/10.1007/s00425-004-1345-z
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DOI: https://doi.org/10.1007/s00425-004-1345-z