Abstract
The variation of the rate of cyclic electron transport around Photosystem I (PS I) during photosynthetic induction was investigated by illuminating dark-adapted spinach leaf discs with red + far-red actinic light for a varied duration, followed by abruptly turning off the light. The post-illumination re-reduction kinetics of P700+, the oxidized form of the photoactive chlorophyll of the reaction centre of PS I (normalized to the total P700 content), was well described by the sum of three negative exponential terms. The analysis gave a light-induced total electron flux from which the linear electron flux through PS II and PS I could be subtracted, yielding a cyclic electron flux. Our results show that the cyclic electron flux was small in the very early phase of photosynthetic induction, rose to a maximum at about 30 s of illumination, and declined subsequently to <10% of the total electron flux in the steady state. Further, this cyclic electron flow, largely responsible for the fast and intermediate exponential decays, was sensitive to 3-(3,4-dichlorophenyl)-1,1-dimethyl urea, suggesting an important role of redox poising of the cyclic components for optimal function. Significantly, our results demonstrate that analysis of the post-illumination re-reduction kinetics of P700+ allows the quantification of the cyclic electron flux in intact leaves by a relatively straightforward method.
Similar content being viewed by others
Abbreviations
- ATP:
-
Adenosine triphosphate
- Chl:
-
Chlorophyll
- DCMU:
-
3-(3,4-Dichlorophenyl)-1,1-dimethyl urea
- Fd:
-
Ferredoxin
- F v′ and F m′:
-
Variable and maximum Chl fluorescence during illumination
- MV:
-
Methyl viologen
- NADP+ :
-
Oxidized nicotinamide adenine dinucleotide phosphate
- P700:
-
Photoactive Chl of the reaction centre of PS I
- PS I and PS II:
-
Photosystem I and II, respectively
- PQ:
-
Plastoquinone
References
Albertsson P-Å (1995) The structure and function of the chloroplast photosynthetic membrane – a model for the domain organization. Photosynth Res 46:141–149
Arnon DI, Whatley FR, Allen MB (1955) Vitamin K as a cofactor of photosynthetic phosphorylation. Biochim Biophys Acta 16: 607–608
Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci 8:15–19
Bendall DS, Manasse R (1995) Cyclic photophosphorylation and electron transport. Biochim Biophys Acta 1229:23–38
Buhkov NG, Carpentier R (2004) Alternative Photosystem I-driven electron transport routes: mechanisms and functions. Photosynth Res 82:17–33
Buhkov NG, Egorova E, Carpentier R (2002) Electron flow to Photosystem I from stromal reductants in vivo: the size of the pool of stromal reductants controls the rate of electron donation to both rapidly and slowly reducing Photosystem I units. Planta 215:812–820
Buhkov NG, Weise C, Neimanis S, Heber U (1999) Heat sensitivity of chloroplasts and leaves: Leakage of protons from thylakoids and reversible activation of cyclic electron transport. Photosynth Res 59:81–93
Chow WS, Hope AB (2004) Electron fluxes through photosystem I in cucumber leaf discs probed by far-red light. Photosynth Res 81:77–89
Clarke JE, Johnson GN (2001) In vivo temperature dependence of cyclic and pseudocyclic electron transport in barley. Planta 212:808–816
Cornic G, Buhkov NG, Weise C, Bligny R, Heber U (2000) Flexible coupling between light-dependent electron and vectorial transport in illuminated leaves of C3 plants. Role of photosystem I-dependent proton pumping. Planta 210:468–477
Furbank RT, Jenkins CLD, Hatch MD (1990) C4 Photosynthesis: quantum requirement, C4 acid overcycling and Q-cycle involvement. Aust J Plant Physiol 17:1–7
Genty B, Briantais J-M, Baker NR (1989) The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92
Golding AJ, Finazzi G, Johnson GN (2004) 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
Golding AJ, Joliot P, Johnson GN (2005) Equilibrium between cytochrome f and P700 in intact leaves. Biochim Biophys Acta 1706:105–109
Havaux M (1996) Short-term responses of Photosystem I to heat stress. Induction of a PS II-independent electron transport through PS I fed by stromal components. Photosynth Res 47:85–97
Heber U, Walker D (1992) Concerning a dual function of coupled cyclic electron transport in leaves. Plant Physiol 100:1621–1626
Herbert SK, Fork DC, Malkin S (1990) Photoacoustic measurements in vivo of energy storage by cyclic electron flow in algae and higher plants. Plant Physiol 94:926–934
Hughes JL, Smith P, Pace R, Krausz E (2006) Charge separation in photosystem II core complexes induced by 690–730 nm excitation at 1.7 K. Biochim Biophys Acta 1757:841–851
Joët T, Cournac L, Peltier G, Havaux M (2002) Cyclic electron flow around photosystem I in C3 plants. In vivo control by the redox state of chloroplasts and involvement of the NADPH-dehydrogenase complex. Plant Physiol 128:760–769
Johnson GN (2005) Cyclic electron transport in C3 plants: fact or artefact? J Exp Bot 56:407–416
Joliot P, Joliot A (2002) Cyclic electron transfer in plant leaf. Proc Natl Acad Sci USA 99:10209–10214
Joliot P, Joliot A (2005) Quantification of cyclic and linear flows in plants. Proc Natl Acad Sci USA 102:4913–4919
Joliot P, Joliot A (2006) Cyclic electron flow in C3 plants. Biochim Biophys Acta 1757:362–368
Kramer DM, Avenson TJ, Edwards GE (2004) Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. Trends Plant Sci 9:349–357
Laisk A, Eichelmann, Oja V, Peterson RB (2005) Control of cytochrome b 6 f at low and high light intensity and cyclic electron transport in leaves. Biochim Biophys Acta 1708:79–90
Maxwell PC, Biggins J (1976) Role of cyclic electron transport in photosynthesis as measured by the photoinduced turnover of P700 in vivo. Biochemistry 15:3975–3981
Mi H, Endo T, Ogawa T, Asada K (1995) Thylakoid membrane-bound pyridine nucleotide dehydrogenase complex mediates cyclic electron transport in the cyanobacteria Synechocystis PCC 6803. Plant Cell Physiol 36:661–668
Munekage Y, Hashimoto M, Miyake C, Tomizawa K-I, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582
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
Schreiber U (2004) Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiou GC, Govindjee (eds) Advances in photosynthesis and respiration, vol 19, Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht, The Netherlands, pp 279–319
Schreiber U, Hormann H, Asada K, Neubauer C (1995) O2-dependent electron flow in spinach chloroplasts: properties and possible regulation of the Mehler-ascorbate-peroxidase cycle. In: Mathis P (ed) Photosynthesis: from light to biosphere, vol II. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 813–818
Whatley FR (1995) Photosynthesis by isolated chloroplasts: the early work in Berkeley. Photosynth Res 46: 17–26
Acknowledgements
DF is supported in part by the National Natural Science Foundation of China (No. 90302004) and Knowledge Innovation Program of the Chinese Academy of Sciences (KSCX2-SW-109). Partial financial support of this project from an ARC grant DP 0665363 to BJP and WSC is gratefully acknowledged. ABH is grateful for a Visiting Fellowship from RSBS, ANU. We thank Jan Anderson and Tom Wydrzynski for constructive comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Fan, DY., Nie, Q., Hope, A.B. et al. Quantification of cyclic electron flow around Photosystem I in spinach leaves during photosynthetic induction. Photosynth Res 94, 347–357 (2007). https://doi.org/10.1007/s11120-006-9127-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-006-9127-z