Abstract
The effects of short-term drought on the regulation of electron transport through photosystems I and II (PSI and PSII) have been studied in Hordeum vulgare L. cv. Chariot. Fluorescence measurements demonstrated that electron flow through PSII decreased in response to both drought and CO2 limitation. This was due to regulation, as opposed to photoinhibition. We demonstrate that this regulation occurs between the two photosystems—in contrast to PSII, PSI became more oxidised and the rate constant for P700 re-reduction decreased under these conditions. Thus, when carbon fixation is inhibited, electron transport is down-regulated to match the reduced requirement for electrons and minimise reactive oxygen production. At the same time non-photochemical quenching (NPQ) increases, alleviating the excitation pressure placed on PSII. We observe an increase in the proportion of PSI centres that are ‘active’ (i.e. can be oxidised with a saturating flash and then rapidly re-reduced) under the conditions when NPQ is increased. We suggest that these additional centres are primarily involved in cyclic electron transport, which generates the ΔpH to support NPQ and protect PSII.
Similar content being viewed by others
Abbreviations
- A :
-
assimilation rate
- Ci:
-
internal CO2 concentration
- ETC:
-
electron transport chain
- g :
-
stomatal conductance
- FR:
-
far red
- k :
-
pseudo first-order rate constant for the reduction of oxidised P700
- NPQ:
-
non-photochemical quenching
- P700:
-
primary electron donor of photosystem I
- PSI, PSII:
-
photosystem I, II
- qP:
-
proportion of open PSII centres
- ROS:
-
reactive oxygen species
- ΔpH:
-
pH gradient across the thylakoid membrane
- ΦPSII:
-
quantum yield of photosystem II
References
Albertsson P-A (1995) The structure and organization of the chloroplast photosynthetic membrane—a model for the domain organization. Photosynth Res 46:141–149
Anderson JM (1992) Cytochrome b 6 f complex: dynamic molecular organization, function and acclimation. Photosynth Res 34:341–357
Andreasson E, Svensson P, Weibull C, Albertsson P-A (1988) Separation and characterisation of stroma and grana membranes—evidence for heterogeneity in antenna size of both PSI and PSII. Biochim Biophys Acta 936:339–350
Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639
Boyer JS, Wong SC, Farquhar GD (1997) CO2 and water vapour exchange across leaf cuticle (epidermis) at various water potentials. Plant Physiol 14:185–191
Clarke JE, Johnson GN (2001) In vivo temperature dependence of cyclic and pseudocyclic electron transport in barley. Planta 192:261–268
Cornic G (1994) Drought stress and high light effects on leaf photosynthesis. In: Baker NR (ed) Photoinhibition of photosynthesis: from molecular mechanisms to the field. BIOS, Oxford, pp 297–313
Cornic G, Briantais J-M (1991) Partitioning of photosynthetic electron flow between CO2 and O2 reduction in a C3 leaf (Phaseolus vulgaris L.) at different CO2 concentrations and during drought stress. Planta 183:178–184
Cornic G, Bukhov NG, Weise C, Bligny R, Heber U (2000) Flexible coupling between light dependent electron and vectorial proton transport in illuminated leaves of C3 plants. Role of PSI-dependent proton pumping. Planta 210:468–477
Epron D, Dreyer E (1992) Effect of a severe dehydration on leaf photosynthesis in Quercus petrea (Mtt.) Liebl.: photosystem II and electrolyte leakage. Tree Physiol 10:273–284
Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of the photosynthetic electron transport chain and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92
Giardi MT, Cona A, Geiken B, Kucera T, Masojidek J, Mattoo AK (1996) Long-term drought stress induces structural and functional reorganization of photosystem II. Planta 199:118–125
Haehnel W (1984) Photosynthetic electron transport in higher plants. Annu Rev Plant Physiol Plant Mol Biol 35:659–693
Harbinson J (1994) The responses of thylakoid electron transport and light utilization efficiency to sink limitation of photosynthesis. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis from molecular mechanisms to the field. BIOS, Oxford, pp 273–296
Harbinson J, Woodward FI (1987) The use of light-induced absorbance changes at 820 nm to monitor the oxidation state of P-700 in leaves. Plant Cell Environ 10:131–140
Haupt-Herting S, Fock HP (2002) Oxygen exchange in relation to carbon assimilation in water-stressed leaves during photosynthesis. Ann Bot 89:851–859
Havaux M (1992) Photoacoustic measurements of cyclic electron flow around photosystem I in leaves adapted to light-states 1 and 2. Plant Cell Physiol 33:799–803
Heber U, Neimanis S, Dietz KJ (1988) Fractional control of photosynthesis by the QB-protein, the cytochrome-f cytochrome-B6 complex and other components of the photosynthetic apparatus. Planta 173:267–274
Heber U, Neimanis S, Siebke K, Schonknecht G, Katona E. (1992) Chloroplast energization and oxidation of P700 plastocyanin in illuminated leaves of reduced levels of CO2 or oxygen. Photosynth Res 34:433–447
Johnson GN (2003) Thiol regulation of the thylakoid electron transport chain—a missing link in the regulation of photosynthesis? Biochemistry 42:3040–3044
Joliot P, Joliot A (2002) Cyclic electron transport in plant leaf. Proc Natl Acad Sci USA 98:4437–4442
Klughammer C, Schreiber U (1994) An improved method, using saturating light pulses, for the determination of photosystem-I quantum yield via P700+-absorbency changes at 830 nm. Planta 192:261–268
Kanazawa A, Kramer DM (2002) In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase. Proc Natl Acad Sci USA 99:12789–12794.
Loggini B, Scartazza A, Brugnoli E, Navari-Izzo F (1999) Antioxidative defense system, pigment composition, and photosynthetic efficiency in two wheat cultivars subjected to drought. Plant Physiol 119:1091–1099
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668
Mehler AH (1951) Studies on reactions of illuminated chloroplasts I. Mechanism of the reduction of oxygen and other Hill reagents. Arch Biochem Biophys 33:65–77
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
Nuijs AM, Shuvalov VA, van Gorkom HS, Plitjer JJ, Duysens LNH (1987) Picosecond absorbance difference spectroscopy on the primary reactions and the antenna-excited states in PSI particles. Biochim Biophys Acta 850:310–318
Ortiz-Lopez A, Ort DR, Boyer JS (1991) Photophosphorylation in attached leaves of Helianthus annuus at low water potentials. Plant Physiol 96:1018–1025
Osmond CD (1994) What is photoinhibition? Some insights from comparisons of sun and shade plants. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis. From molecular mechanisms to the field. BIOS, Oxford, pp 1–24
Ott T, Clarke J, Birks K, Johnson G (1999) Regulation of the photosynthetic electron transport chain. Planta 209:250–258
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
Sánchez-Rodriguez J, Martínez-Carrasco R, Pérez P (1997) Photosynthetic electron transport and carbon-reduction-cycle enzyme activities under long-term drought stress in Casuarina equisetifolia Forst. & Forst. Photosynth Res 52:255–262
Smirnoff N (1993) The role of active oxygen in response of plants to water deficit and desiccation. New Phytol 125:27–58
Stiehl HH, Witt HL (1969) Quantitative treatment of the function of plastoquinone in photosynthesis. Z Naturforsch Teil B 24:1588–1598
Tourneux C, Peltier G (1995) Effect of water deficit on photosynthetic oxygen measured using 18O2 and mass spectrometry in Solanum tuberosum L. leaf discs. Planta 195:570–577
Von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387
Weis E, Ball JR, Berry J (1987) Photosynthetic control of electron transport in leaves of Phaseolus vulgaris. Evidence for regulation of PSII by the proton gradient. In: Biggins J (ed) Progress in photosynthesis research (Proc 7th Int Congr Photosynth) vol II. Nijhoff, Dordrecht, Netherlands, pp 553–556
Wollenberger L, Stefansson H, Yu SG, Albertsson P-A (1994) Isolation and characterisation of vesicles originating from the chloroplast grana margins. Biochim Biophys Acta 1184:93–102
Acknowledgements
We thank Prof. Pierre Joliot and Dr. Giovanni Finnazzi (IBPC, Paris) for useful and stimulating discussions relating to this work. A.J.G. was supported by a studentship from the UK Biotechnology and Biological Sciences Research Council
Author information
Authors and Affiliations
Corresponding author
Additional information
An erratum to this article can be found at http://dx.doi.org/10.1007/s00425-003-1188-z
Rights and permissions
About this article
Cite this article
Golding, A.J., Johnson, G.N. Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218, 107–114 (2003). https://doi.org/10.1007/s00425-003-1077-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-003-1077-5