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Reduction of the primary donor P700 of photosystem I during steady-state photosynthesis under low light in Arabidopsis

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Abstract

During steady-state photosynthesis in low-light, 830-nm absorption (A830) by leaves was close to that in darkness in Arabidopsis, indicating that the primary donor P700 in the reaction center of photosystem I (PSI) was in reduced form. However, P700 was not fully oxidized by a saturating light pulse, suggesting the presence of a population of PSI centers with reduced P700 that remains thermodynamically stable during the application of the saturating light pulse (i.e., reduced-inactive P700). To substantiate this, the effects of methyl viologen (MV) and far-red light on P700 oxidation by the saturating light pulse were analyzed, and the cumulative effects of repetitive application of the saturating light pulse on photosynthesis were analyzed using a mutant crr2-2 with impaired PSI cyclic electron flow. We concluded that the reduced-inactive P700 in low-light as revealed by saturating light pulse indicates limitations of electron flow at the PSI acceptor side.

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Abbreviations

A830 :

Leaf absorption at 830 nm

Chl:

Chlorophyll

Fm and Fm′:

Maximum fluorescence level in the dark- and light-adapted leaf, respectively

Fs and Fo :

Steady state- and minimum-fluorescence level, respectively

FR:

Far-red light

MV:

Methyl viologen

P700:

Primary donor pigment in the reaction center of PSI

References

  • Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134. doi:10.1016/0005-2728(93)90134-2

    Article  PubMed  CAS  Google Scholar 

  • Asada K, Neubauer C, Heber U, Schreiber U (1990) Methyl viologen-dependent cyclic electron transport in spinach chloroplasts in the absence of oxygen. Plant Cell Physiol 31:557–564

    CAS  Google Scholar 

  • Baker NR, Harbinson J, Kramer DM (2007) Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant Cell Environ 30:1107–1125. doi:10.1111/j.1365-3040.2007.01680.x

    Article  PubMed  CAS  Google Scholar 

  • Barth C, Krause GH, Winter K (2001) Responses of photosystem I compared with photosystem II to high-light stress in tropical shade and sun leaves. Plant Cell Environ 24:163–176. doi:10.1111/j.1365-3040.2001.00673.x

    Article  CAS  Google Scholar 

  • Brettel K, Leibl W (2001) Electron transfer in photosystem I. Biochim Biophys Acta 1507:100–114. doi:10.1016/S0005-2728(01)00202-X

    Article  PubMed  CAS  Google Scholar 

  • Cerovic ZG, Bergher M, Goulas Y, Tosti S, Moya I (1993) Simultaneous measurement of changes in red and blue fluorescence in illuminated isolated chloroplasts and leaf pieces: the contribution of NADPH to the blue fluorescence signal. Photosynth Res 36:193–204. doi:10.1007/BF00033038

    Article  CAS  Google Scholar 

  • Dietz KJ, Heber U (1984) Rate-limiting factors in leaf photosynthesis. I. Carbon fluxes in the Calvin cycle. Biochim Biophys Acta 767:432–443. doi:10.1016/0005-2728(84)90041-0

    Article  CAS  Google Scholar 

  • Endo T, Kawase D, Sato F (2005) Stromal over-reduction by high-light stress as measured by decreases in P700 oxidation by far-red light and its physiological relevance. Plant Cell Physiol 46:775–781. doi:10.1093/pcp/pci084

    Article  PubMed  CAS  Google Scholar 

  • Forti G, Furia A, Bombelli P, Finazzi G (2003) In vivo changes of the oxidation-reduction state of NADP and of the ATP/ADP cellular ratio linked to the photosynthetic activity in Chlamydomonas reinhardtii. Plant Physiol 132:1464–1474. doi:10.1104/pp.102.018861

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Lelandais M, Harbinson J (1992) Control of the quantum efficiencies of photosystems I and II, electron flow, and enzyme activation following dark-to-light transitions in pea leaves. Relationship between NADP/NADPH ratios and NADP-Malate dehydrogenase activation state. Plant Physiol 99:979–986

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Golbeck JH, Cornelius JM (1986) Photosystem I charge separation in the absence of centres A and B. I. Optical characterization of centre A2 and evidence for its association with a 64 kDa peptide. Biochim Biophys Acta 849:16–24. doi:10.1016/0005-2728(86)90091-5

    Article  CAS  Google Scholar 

  • Golding AJ, Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218:107–114. doi:10.1007/s00425-003-1077-5

    Article  PubMed  CAS  Google Scholar 

  • Hampp R, Goller M, Füllgraf H (1984) Determination of compartmented metabolite pools by a combination of rapid fractionation of oat mesophyll protoplasts and enzymatic cycling. Plant Physiol 75:1017–1021

    PubMed  CAS  Google Scholar 

  • Harbinson J, Hedley CL (1989) The kinetics of P-700+ reduction in leaves: a novel in situ probe of thylakoid functioning. Plant Cell Environ 12:357–369. doi:10.1111/j.1365-3040.1989.tb01952.x

    Article  CAS  Google Scholar 

  • Harbinson J, Hedley CL (1993) Changes in P-700 oxidation during the early stages of the induction of photosynthesis. Plant Physiol 103:649–660

    PubMed  CAS  Google Scholar 

  • Harbinson J, Genty B, Foyer C (1990) Relationship between photosynthetic electron transport and stromal enzyme activity in pea leaves. Toward an understanding of the nature of photosynthetic control. Plant Physiol 94:545–553

    PubMed  CAS  Google Scholar 

  • Hashimoto M, Endo T, Peltier G, Tasaka M, Shikanai T (2003) A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis. Plant J 36:541–549. doi:10.1046/j.1365-313X.2003.01900.x

    Article  PubMed  CAS  Google Scholar 

  • Heineke D, Riens B, Grosse H, Hoferichter P, Peter U, Flügge UI et al (1991) Redox transfer across the inner chloroplast envelope membrane. Plant Physiol 95:1131–1137

    PubMed  CAS  Google Scholar 

  • Hiyama T (1985) Quantum yield and requirement for photo-oxidation of P700. Physiol Veg 23:605–610

    CAS  Google Scholar 

  • Hiyama T, Ke B (1971) A further study of P-430: a possible primary electron acceptor of photosystem I. Arch Biochem Biophys 147:99–108. doi:10.1016/0003-9861(71)90314-6

    Article  PubMed  CAS  Google Scholar 

  • Holtgrefe S, Bader KP, Horton P, Scheibe R, von Schaewen A, Backhausen JE (2003) Decreased content of leaf ferredoxin changes electron distribution and limits photosynthesis in transgenic potato plants. Plant Physiol 133:1768–1778. doi:10.1104/pp.103.026013

    Article  PubMed  CAS  Google Scholar 

  • Johnson GN (2005) Cyclic electron transport in C3 plants: fact or artifact? J Exp Bot 56:407–416. doi:10.1093/jxb/eri106

    Article  PubMed  CAS  Google Scholar 

  • Joliot P, Joliot A (2002) Cyclic electron transfer in plant leaf. Proc Natl Acad Sci USA 99:10209–10214. doi:10.1073/pnas.102306999

    Article  PubMed  CAS  Google Scholar 

  • Joliot P, Joliot A (2005) Quantification of cyclic and linear flows in plants. Proc Natl Acad Sci USA 102:4913–4918. doi:10.1073/pnas.0501268102

    Article  PubMed  CAS  Google Scholar 

  • Joliot P, Béal D, Joliot A (2004) Cyclic electron flow under saturating excitation of dark-adapted Arabidopsis leaves. Biochim Biophys Acta 1656:166–176. doi:10.1016/j.bbabio.2004.03.010

    Article  PubMed  CAS  Google Scholar 

  • Kirchhoff H, Schöttler MA, Maurer J, Weis E (2004) Plastocyanin redox kinetics in spinach chloroplasts: evidence for disequilibrium in the high potential chain. Biochim Biophys Acta 1659:63–72. doi:10.1016/j.bbabio.2004.08.004

    Article  PubMed  CAS  Google Scholar 

  • Klughammer C, 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 46:233–244

    CAS  Google Scholar 

  • Klughammer C, Schreiber U (1994) An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. Planta 192:261–268. doi:10.1007/BF01089043

    Article  CAS  Google Scholar 

  • Laisk A, Siebke K, Gerst U, Eichelmann H, Oja V, Heber U (1991) Oscillations in photosynthesis are initiated and supported by imbalances in the supply of ATP and NADPH to the Calvin cycle. Planta 185:554–562. doi:10.1007/BF00202966

    Article  CAS  Google Scholar 

  • Laisk A, Eichelmann H, 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. doi:10.1016/j.bbabio.2005.01.007

    Article  PubMed  CAS  Google Scholar 

  • Nikolaeva MK (2001) Activation of ferredoxin-NADP+ oxidoreductase in Vicia faba leaves induced by a short-term increase in irradiance. Russ J Plant Physiol 48:601–607. doi:10.1023/A:1016799701081

    Article  CAS  Google Scholar 

  • Nuijs AM, Shuvalov VA, Van Gorkom HJ, Plijter JJ, 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. doi:10.1016/0005-2728(86)90186-6

    Article  CAS  Google Scholar 

  • Oja V, Eichelmann H, Peterson RB, Rasulov B, Laisk A (2003) Deciphering the 820 nm signal: redox state of donor side and quantum yield of photosystem I in leaves. Photosynth Res 78:1–15. doi:10.1023/A:1026070612022

    Article  PubMed  CAS  Google Scholar 

  • Rebeille F, Hatch MD (1986) Regulation of NADP-Malate dehydrogenase in C4 plants: relationship among enzyme activity, NADPH to NADP ratios, and thioredoxin redox states in intact maize mesophyll chloroplasts. Arch Biochem Biophys 249:171–179. doi:10.1016/0003-9861(86)90572-2

    Article  PubMed  CAS  Google Scholar 

  • Rumeau D, Bécuwe-Linka N, Beyly A, Louwagie M, Garin J, Peltier G (2005) New subunits NDH-M, -N, and -O, encoded by nuclear genes, are essential for plastid Ndh complex functioning in higher plants. Plant J 17:219–232

    CAS  Google Scholar 

  • Sage RF (1990) A model describing the regulation of ribulose-1, 5-bisphosphate carboxylase, electron transport and triose phosphate use in response to light intensity and CO2 in C3 plants. Plant Physiol 94:1728–1734

    PubMed  CAS  Google Scholar 

  • Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217. doi:10.1146/annurev.arplant.58.091406.110525

    Article  PubMed  CAS  Google Scholar 

  • Shinkarev VP, Zybailov B, Vassiliev IR, Golbeck JH (2002) Modeling of the P700+ charge recombination kinetics with phylloquinone and plastoquinone in the A1 site of photosystem I. Biophys J 83:2885–2897

    PubMed  CAS  Google Scholar 

  • Siebke K, von Caemmerer S, Badger M, Furbank R (1997) Expressing an RbcS antisense gene in transgenic Flaveria bidentis leads to an increased quantum requirement for CO2 fixed in photosystem I and II. Plant Physiol 115:1163–1174

    PubMed  CAS  Google Scholar 

  • Sonoike K, Terashima I, Iwaki M, Itoh S (1995) Destruction of photosystem I iron-sulfur centers in leaves of Cucumis sativus L. by weak illumination at chilling temperatures. FEBS Lett 362:235–238. doi:10.1016/0014-5793(95)00254-7

    Article  PubMed  CAS  Google Scholar 

  • Takahama U, Shimizu-Takahama M, Heber U (1981) The redox state of the NADP system in illuminated chloroplasts. Biochim Biophys Acta 637:530–539. doi:10.1016/0005-2728(81)90060-8

    Article  CAS  Google Scholar 

  • Takahashi Y, Katoh S (1984) Triplet states in a photosystem I reaction center complex. Inhibition of radical pair recombination by bipyridinium dyes and naphthoquinones. Plant Cell Physiol 25:785–794

    CAS  Google Scholar 

  • Talts E, Oja V, Rämma H, Rasulov B, Anijalg A, Laisk A (2007) Dark inactivation of ferredoxin-NADP reductase and cyclic electron flow under far-red light in sunflower leaves. Photosynth Res 94:109–120. doi:10.1007/s11120-007-9224-7

    Article  PubMed  CAS  Google Scholar 

  • Usuda H (1988) Adenine nucleotide levels, the redox state of the NADP system, and assimilatory force in nonaqueously purified mesophyll chloroplasts from maize leaves under different light intensities. Plant Physiol 88:1461–1468

    PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Dr. Toshiharu Shikanai (Kyoto University) for helpful discussions and suggestions. This work was supported by a Grant-in-aid for Young Scientists B (18780117) from MEXT to Michito Tsuyama, for Young Scientists from Kyushu University to Michito Tsuyama, and for Scientific Research on Priority Areas (16085206) from MEXT to Toshiharu Shikanai.

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Tsuyama, M., Kobayashi, Y. Reduction of the primary donor P700 of photosystem I during steady-state photosynthesis under low light in Arabidopsis . Photosynth Res 99, 37–47 (2009). https://doi.org/10.1007/s11120-008-9379-x

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