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Photosynthesis Research

, Volume 139, Issue 1–3, pp 509–522 | Cite as

Three phases of energy-dependent induction of \({\text{P}}_{{700}}^{+}\) and Chl a fluorescence in Tradescantia fluminensis leaves

  • Vasily V. Ptushenko
  • Tatiana V. Zhigalova
  • Olga V. Avercheva
  • Alexander N. TikhonovEmail author
Original Article

Abstract

In plants, the short-term regulation (STR, seconds to minute time scale) of photosynthetic apparatus is associated with the energy-dependent control in the chloroplast electron transport, the distribution of light energy between photosystems (PS) II and I, activation/deactivation of the Calvin–Benson cycle (CBC) enzymes, and relocation of chloroplasts within the plant cell. In this work, using a dual-PAM technique for measuring the time-courses of P700 photooxidation and Chl a fluorescence, we have investigated the STR events in Tradescantia fluminensis leaves. The comparison of Chl a fluorescence and \({\text{P}}_{{700}}^{+}\) induction allowed us to investigate the contribution of the trans-thylakoid pH difference (ΔpH) to the STR events. Two parameters were used as the indicators of ΔpH generation: pH-dependent component of non-photochemical quenching of Chl a fluorescence, and pHin-dependent rate of electron transfer from plastoquinol (PQH2) to \({\text{P}}_{{700}}^{+}\) (via the Cyt b6f complex and plastocyanin). In dark-adapted leaves, kinetics of \({\text{P}}_{{700}}^{+}\) induction revealed three phases. Initial phase is characterized by rapid electron flow to \({\text{P}}_{{700}}^{+}\) (τ1/2 ~ 5–10 ms), which is likely related to cyclic electron flow around PSI, while the outflow of electrons from PSI is restricted by slow consumption of NADPH in the CBC. The light-induced generation of ΔpH and activation of the CBC promote photooxidation of P700 and concomitant retardation of \({\text{P}}_{{700}}^{+}\) reduction (τ1/2 ~ 20 ms). Prolonged illumination induces additional slowing down of electron transfer to \({\text{P}}_{{700}}^{+}\) (τ1/2 ≥ 30–35 ms). The latter effect is not accompanied by changes in the Chl a fluorescence parameters which are sensitive to ΔpH generation. We suggest the tentative explanation of the latter results by the reversal of Q-cycle, which causes the deceleration of PQH2 oxidation due to the back pressure of stromal reductants.

Keywords

Photosynthesis Tradescantia fluminensis Induction events Regulation of photosynthetic electron transport 

Abbreviations

AL

Actinic light

b6f

Cytochrome b6f complex

CBC

Calvin–Benson cycle

Chl

Chlorophyll

CET1

Cyclic electron transport around photosystem I

ETC

Electron transport chain

ISP

Iron-sulfur protein

Fd

Ferredoxin

FNR

Ferredoxin-NADP-oxidoreductase

FQR

Ferredoxin-quinone-oxidoreductase

FRL

Far-red light

LEF

Linear electron flow

LTR

Long-term regulation

MV

Methylviologen

NPQ

Non-photochemical quenching

PAM

Pulse amplitude modulation

pmf

Proton motive force

PSA

Photosynthetic apparatus

PSI

Photosystem I

PSII

Photosystem II

P700

Reduced form of primary electron donor of PSI

\({\text{P}}_{{700}}^{+}\)

Oxidized form of primary electron donor of PSI

Pc

Plastocyanin

PQ

Plastoquinone

PQH2

Plastoquinol

ROS

Reactive oxygen species

SIF

Slow induction of fluorescence

SPQ

Semi-plastoquinone

STR

Short-term regulation

ΔpH

Trans-thylakoid pH difference

Notes

Acknowledgements

This work was supported in part by the Russian Foundation for Basic Researches (A.N. Tikhonov, projects 15-04-03790, 18-04-00214) and Russian Science Foundation (V.V. Ptushenko, Project 14-50-00029).

References

  1. Allakhverdiev SI (2011) Recent progress in the studies of structure and function of photosystem II. J Photochem Photobiol B 104:1–8Google Scholar
  2. Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1657:23–32Google Scholar
  3. Allakhverdiev SI, Klimov VV, Carpentier R (1997) Evidence for the involvement of cyclic electron transport in the protection of photosystem II against photoinhibition: influence of a new phenolic compound. Biochemistry 36:4149–4154Google Scholar
  4. Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci 8:15–19Google Scholar
  5. Andersson I (2008) Catalysis and regulation in Rubisco. J Exp Bot 59:1555–1568Google Scholar
  6. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Biol 50:601–639Google Scholar
  7. Asada K, Kiso K, Yoshikawa K (1974) Univalent reduction of molecular oxygen by spinach chloroplasts on illumination. J Biol Chem 249:2175–2181Google Scholar
  8. Bae A (2014) An intensive examination of chloroplast movement and NPQ in Arabidopsis thaliana wild type and mutants grown under different light conditions. Honors Thesis Collection. Paper 206Google Scholar
  9. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113Google Scholar
  10. Baker NR, Oxborough K (2004) Chlorophyll fluorescence as a probe of photosynthetic productivity. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence. Springer, Dordrecht, pp 65–82Google Scholar
  11. Balsera M, Schurmann P, Buchanan BB (2016) Redox regulation in chloroplasts. In: Kirchhoff H (ed) Chloroplasts: current research and future trends. Caister Academic Press, Norfolk, pp 187–207Google Scholar
  12. Berry EA, Guergova-Kuras M, Huang L, Crofts AR (2000) Structure and function of cytochrome bc complexes. Annu Rev Biochem 69:1005–1075Google Scholar
  13. Blankenship RE (2002) Molecular mechanisms of photosynthesis. Blackwell Science Inc., MaldenGoogle Scholar
  14. Brettel K (1997) Electron transfer and arrangement of the redox cofactors in photosystem I. Biochim Biophys Acta 1318:322–373Google Scholar
  15. Breyton C, Nandha B, Johnson G, Joliot P, Finazzi G (2006) Redox modulation of cyclic electron flow around photosystem I in C3 plants. Biochemistry 45:13465–13475Google Scholar
  16. Buchanan BB (1980) Role of light in the regulation of chloroplast enzymes. Annu Rev Plant Physiol 31:341–374Google Scholar
  17. Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187–220Google Scholar
  18. Bukhov N, Carpentier R (2004) Alternative photosystem I-driven electron transport routes: mechanisms and functions. Photosynth Res 82:17–33Google Scholar
  19. Bukhov N, 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 215:812–820Google Scholar
  20. Cape JL, Bowman MK, Kramer DM (2006) Understanding the cytochrome bc complexes by what they don’t do. The Q-cycle at 30. Trends Plant Sci 11:46–55Google Scholar
  21. Cape JL, Bowman MK, Kramer DM (2007) A semiquinone intermediate generated at the Qo site of the cytochrome bc 1 complex: importance for the Q-cycle and superoxide production. Proc Natl Acad Sci USA 104:7887–7892Google Scholar
  22. Cramer WA, Zhang H, Yan J, Kurisu G, Smith JL (2006) Transmembrane traffic in the cytochrome b 6 f complex. Annu Rev Biochem 75:769–790Google Scholar
  23. Cramer WA, Hasan SS, Yamashita E (2011) The Q cycle of cytochrome bc complexes: a structure perspective. Biochim Biophys Acta 1807:788–802Google Scholar
  24. Demmig-Adams B, Cohu CM, Muller O, Adams WW III (2012) Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. Photosynth Res 113:75–88Google Scholar
  25. Dietz K-J, Pfannschmidt T (2011) Novel regulators in photosynthetic redox control of plant metabolism and gene expression. Plant Physiol 155:1477–1485Google Scholar
  26. Eberhard S, Finazzi G, Wollman F-A (2008) The dynamics of photosynthesis. Annu Rev Genet 42:463–515Google Scholar
  27. Edwards G, Walker D (1983) C3, C4: mechanisms, and cellular and environmental regulation, of photosynthesis. Univ of California Press, BerkeleyGoogle Scholar
  28. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875Google Scholar
  29. Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18Google Scholar
  30. Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J (2012) Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 63:1637–1661Google Scholar
  31. Franck J, French CS, Puck TT (1941) The fluorescence of chlorophyll and photosynthesis. J Phys Chem 45:1268–1300Google Scholar
  32. Haehnel W (1984) Photosynthetic electron transport in higher plants. Annu Rev Plant Physiol 35:659–693Google Scholar
  33. Harbinson J, Hedley CL (1989) The kinetics of P-700 + reduction in leaves: a novel in situ probe of thylakoid functioning. Plant Cell Environ 12:357–369Google Scholar
  34. Hasan SS, Cramer WA (2012) On rate limitations of electron transfer in the photosynthetic cytochrome b 6 f complex. Phys Chem Chem Phys 14:13853–13860Google Scholar
  35. Horton P (2012) Optimization of light harvesting and photoprotection: molecular mechanisms and physiological consequences. Philos Trans R Soc B 367:3455–3465Google Scholar
  36. Ivanov BN (2014) Role of ascorbic acid in photosynthesis. Biochem (Moscow) 79:282–289Google Scholar
  37. Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193Google Scholar
  38. Joliot P, Joliot A (2005) Quantification of cyclic and linear flows in plants. Proc Natl Acad Sci USA 102:4913–4918Google Scholar
  39. Joliot P, Joliot A (2006) Cyclic electron flow in C3 plants. Biochim Biophys Acta 1757:362–368Google Scholar
  40. Joliot P, Béal D, Joliot A (2004) Cyclic electron flow under saturating excitation of dark-adapted Arabidopsis leaves. Biochim Biophys Acta 1656:166–176Google Scholar
  41. Kalaji HM, Schansker G, Ladle RJ et al (2014) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res 122:121–158Google Scholar
  42. Kangasjärvi S, Tikkanen M, Durian G, Aro E-M (2014) Photosynthetic light reactions—an adjustable hub in basic production and plant immunity signaling. Plant Physiol Biochem 81:128–134Google Scholar
  43. Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420:829–832Google Scholar
  44. Kasajima I, Suetsugu N, Wada M, Takahara K (2015) Collective calculation of actual values of non-photochemical quenching from their apparent values after chloroplast movement and photoinhibition. Am J Plant Sci 6:1792–1805Google Scholar
  45. Kautsky H, Hirsch A (1931) Neue versuche zur kohlensäureassimilation. Naturwissenschaften 19:964Google Scholar
  46. Kirchhoff H (2013) Architectural switches in plant thylakoid membranes. Photosynth Res 116:481–487Google Scholar
  47. Kono M, Terashima I (2014) Long-term and short-term responses of the photosynthetic electron transport to fluctuating light. J Photochem Photobiol B 137:89–99Google Scholar
  48. Kramer DM, Sacksteder CA, Cruz JA (1999) How acidic is the lumen? Photosynth Res 60:151–163Google Scholar
  49. 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 9:349–357Google Scholar
  50. Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b 6 f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1014Google Scholar
  51. Laisk A, Talts E, Oja V, Eichelmann H, Peterson RB (2010) Fast cyclic electron transport around photosystem I in leaves under far-red light: a proton-uncoupled pathway? Photosynth Res 103:79–95Google Scholar
  52. Laisk A, Oja V, Eichelmann H, Dall’Osto L (2014) Action spectra of photosystems II and I and quantum yield of photosynthesis in leaves in State 1. Biochim Biophys Acta 1837:315–325Google Scholar
  53. Lazár D (1999) Chlorophyll a fluorescence induction. Biochim Biophys Acta 1412:1–28Google Scholar
  54. Lazár D (2003) Chlorophyll a fluorescence rise induced by high light illumination of dark-adapted plant tissue studied by means of a model of photosystem II and considering photosystem II heterogeneity. J Theor Biol 220:469–503Google Scholar
  55. Lemeille S, Rochaix J-D (2010) State transitions at the crossroad of thylakoid signalling pathways. Photosynth Res 106:33–46Google Scholar
  56. Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260Google Scholar
  57. Lichtenthaler HK, Babani F (2004) Light adaptation and senescence of the photosynthetic apparatus. Changes in pigment composition, chlorophyll fluorescence parameters and photosynthetic activity. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence. Springer, Dordrecht, pp 713–736Google Scholar
  58. Lichtenthaler HK, Babani F, Navrátil M, Buschmann C (2013) Chlorophyll fluorescence kinetics, photosynthetic activity, and pigment composition of blue-shade and half-shade leaves as compared to sun and shade leaves of different trees. Photosynth Res 117:355–366Google Scholar
  59. Maksimov EG, Mironov KS, Trofimova MS, Nechaeva NL, Todorenko DA, Klementiev KE, Tsoraev GV, Tyutyaev EV, Zorina AA, Feduraev PV, Allakhverdiev SI, Paschenko VZ, Los DA (2017) Membrane fluidity controls redox-regulated cold stress responses in cyanobacteria. Photosynth Res 133:215–223Google Scholar
  60. Mamedov M, Govindjee, Nadtochenko V, Semenov A (2015) Primary electron transfer processes in photosynthetic reaction centers from oxygenic organisms. Photosynth Res 125:51–63Google Scholar
  61. Maxwell PC, Biggins J (1976) Role of cyclic electron transport in photosynthesis as measured by the photoinduced turnover of P700 in vivo. Biochemistry 15:3975–3981Google Scholar
  62. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668Google Scholar
  63. Mehler AH (1951) Studies on reactions of illuminated chloroplasts: I. Mechanism of the reduction of oxygen and other hill reagents. Arch Biochem Biophys 33:65–77Google Scholar
  64. Michelet L, Zaffagnini M, Morisse S, Sparla F, Pérez-Pérez ME, Francia F, Danon A, Marchand CH, Fermani S, Trost P, Lemaire SD (2013) Redox regulation of the Calvin-Benson cycle: something old, something new. Front Plant Sci 4:470Google Scholar
  65. Milanovsky GE, Petrova AA, Cherepanov DA, Semenov AY (2017) Kinetic modeling of electron transfer reactions in photosystem I complexes of various structures with substituted quinone acceptors. Photosynth Res 133:185–199Google Scholar
  66. Mishanin VI, Trubitsin BV, Benkov MA, Minin AA, Tikhonov AN (2016) Light acclimation of shade-tolerant and light-resistant Tradescantia species: induction of chlorophyll a fluorescence and P700 photooxidation, expression of PsbS and Lhcb1 proteins. Photosynth Res 130:275–291Google Scholar
  67. Mishanin VI, Trubitsin BV, Patsaeva SV, Ptushenko VV, Solovchenko AE, Tikhonov AN (2017) Acclimation of shade-tolerant and light-resistant Tradescantia species to growth light: chlorophyll a fluorescence, electron transport, and xanthophyll content. Photosynth Res 133:87–102Google Scholar
  68. Mitchell P (1976) Possible molecular mechanisms of the protonmotive function of cytochrome systems. J Theor Biol 62:327–367Google Scholar
  69. Mohanty P, Allakhverdiev SI, Murata N (2007) Application of low temperatures during photoinhibition allows characterization of individual steps in photodamage and the repair of photosystem II. Photosynth Res 94:217–224Google Scholar
  70. Munekage Y, Hashimoto M, Miyake C, Tomizawa K, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582Google Scholar
  71. Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421Google Scholar
  72. Nelson N, Yocum CF (2006) Structure and function of photosystems I and II. Annu Rev Plant Biol 57:521–565Google Scholar
  73. Oja V, Bichele I, Hüve K, Rasulov B, Laisk A (2004) Reductive titration of photosystem I and differential extinction coefficient of P700+ at 810-950 nm in leaves. Biochim Biophys Acta 1658:225–234Google Scholar
  74. Osyczka A, Moser CC, Dutton PL (2005) Fixing the Q cycle. Trends Biochem Sci 30:176–182Google Scholar
  75. Ptushenko VV, Ptushenko EA, Samoilova OP, Tikhonov AN (2013) Chlorophyll fluorescence in the leaves of Tradescantia species of different ecological groups: Induction events at different intensities of actinic light. Biosystems 114:85–97Google Scholar
  76. Ptushenko VV, Ptushenko OS, Samoilova OP, Solovchenko AE (2016) An exceptional irradiance-induced decrease of light trapping in two Tradescantia species: an unexpected relationship with the leaf architecture and zeaxanthin-mediated photoprotection. Biol Plant 60:385–393Google Scholar
  77. Ptushenko VV, Ptushenko OS, Samoilova OP, Solovchenko AE (2017) Analysis of photoprotection and apparent non-photochemical quenching of chlorophyll fluorescence in Tradescantia leaves based on the rate of irradiance-induced changes in optical transparence. Biochem (Moscow) 82:67–74Google Scholar
  78. Puthiyaveetil S, Kirchhoff H, Höhner R (2016) Structural and functional dynamics of the thylakoid membrane system. In: Kirchhoff H (ed) Chloroplasts: current research and future trends. Caister Academic Press, Norfolk, pp 59–87Google Scholar
  79. Rochaix J-D (2014) Regulation and dynamics of the light-harvesting system. Annu Rev Plant Biol 65:287–309Google Scholar
  80. Ruban AV (2012) The photosynthetic membrane: molecular mechanisms and biophysics of light harvesting. Wiley, ChichesterGoogle Scholar
  81. Ruban AV, Johnson MP, Duffy CDP (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta 1817:167–181Google Scholar
  82. Rumberg B, Siggel U (1969) pH changes in the inner phase of the thylakoids during photosynthesis. Naturwissenschaften 56:130–132Google Scholar
  83. Sarewicz M, Bujnowicz L, Bhaduri S, Singh SK, Cramer WA, Osyczka A (2017) Metastable radical state, nonreactive with oxygen, is inherent to catalysis by respiratory and photosynthetic cytochromes bc 1/b 6 f. Proc Natl Acad Sci 114:1323–1328Google Scholar
  84. 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 429:115–118Google Scholar
  85. Scheibe R (2004) Malate valves to balance cellular energy supply. Physiol Plant 120:21–26Google Scholar
  86. Schreiber U (2017) Redox changes of ferredoxin, P700, and plastocyanin measured simultaneously in intact leaves. Photosynth Res 134:343–360Google Scholar
  87. Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217Google Scholar
  88. Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B 104:236–257Google Scholar
  89. Stirbet A, Govindjee (2012) Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise. Photosynth Res 113:15–61Google Scholar
  90. Strand DD, Fisher N, Kramer DM (2016) Distinct energetics and regulatory functions of the two major cyclic electron flow pathways in chloroplasts. In: Kirchhoff H (ed) Chloroplasts: current research and future trends. Caister Academic Press, Norfolk, pp 89–100Google Scholar
  91. Stroebel D, Choquet Y, Popot J-L, Picot D (2003) An atypical heme in the cytochrome b 6 f complex. Nature 426:413–418Google Scholar
  92. Tikhonov AN (2012) Energetic and regulatory role of proton potential in chloroplasts. Biochem (Moscow) 77:956–974Google Scholar
  93. Tikhonov AN (2013) pH-Dependent regulation of electron transport and ATP synthesis in chloroplasts. Photosynth Res 116:511–534Google Scholar
  94. Tikhonov AN (2014) The cytochrome b 6 f complex at the crossroad of photosynthetic electron transport pathways. Plant Physiol Biochem 81:163–183Google Scholar
  95. Tikhonov AN (2015) Induction events and short-term regulation of electron transport in chloroplasts: an overview. Photosynth Res 125:65–94Google Scholar
  96. Tikhonov AN, Vershubskii AV (2017) Connectivity between electron transport complexes and modulation of photosystem II activity in chloroplasts. Photosynth Res 133:103–114Google Scholar
  97. Tikhonov AN, Khomutov GB, Ruuge EK, Blumenfeld LA (1981) Electron transport control in chloroplasts. Effects of photosynthetic control monitored by the intrathylakoid pH. Biochim Biophys Acta 637:321–333Google Scholar
  98. Tikhonov AN, Khomutov GB, Ruuge EK (1984) Electron transport control in chloroplasts. Effects of magnesium ions on the electron flow between two photosystems. Photobiochem Photobiophys 8:261–269Google Scholar
  99. Tikkanen M, Aro E-M (2012) Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants. Biochim Biophys Acta 1817:232–238Google Scholar
  100. Tikkanen M, Grieco M, Aro E-M (2011) Novel insights into plant light-harvesting complex II phosphorylation and “state transitions”. Trends Plant Sci 16:126–131Google Scholar
  101. Tikkanen M, Mekala NR, Aro E-M (2014) Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage. Biochim Biophys Acta 1837:210–215Google Scholar
  102. Tóth SZ, Schansker G, Strasser RJ (2007) A non-invasive assay of the plastoquinone pool redox state based on OJIP-transient. Photosynth Res 93:193–203Google Scholar
  103. Trubitsin BV, Mamedov MD, Semenov AY, Tikhonov AN (2014) Interaction of ascorbate with photosystem I. Photosynth Res 122:215–231Google Scholar
  104. Trubitsin BV, Vershubskii AV, Priklonskii VI, Tikhonov AN (2015) Short-term regulation and alternative pathways of photosynthetic electron transport in Hibiscus rosa-sinensis leaves. J Photochem Photobiol B 152:400–415Google Scholar
  105. Vener AV, Van Kan PJM, Rich PR, Ohad I, Andersson B (1997) Plastoquinol at the quinol oxidation site of reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single-turnover flash. Proc Natl Acad Sci 94:1585–1590Google Scholar
  106. Vredenberg WJ, Bulychev AA (2010) Photoelectrochemical control of the balance between cyclic-and linear electron transport in photosystem I. Algorithm for P700+ induction kinetics. Biochim Biophys Acta 1797:1521–1532Google Scholar
  107. Wada M, Kagawa T, Sato Y (2003) Chloroplast movement. Annu Rev Plant Biol 54:455–468Google Scholar
  108. Zurzycki J (1955) Chloroplasts arrangement as a factor in photosynthesis. Acta Soc Bot Pol 24:27–63Google Scholar

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Authors and Affiliations

  • Vasily V. Ptushenko
    • 1
    • 2
  • Tatiana V. Zhigalova
    • 3
  • Olga V. Avercheva
    • 3
  • Alexander N. Tikhonov
    • 2
    • 4
    Email author
  1. 1.A.N.Belozersky Institute of Physical-Chemical BiologyM.V.Lomonosov Moscow State UniversityMoscowRussia
  2. 2.N.M.Emanuel Institute of Biochemical Physics of Russian Academy of SciencesMoscowRussia
  3. 3.Faculty of BiologyM.V.Lomonosov Moscow State UniversityMoscowRussia
  4. 4.Faculty of PhysicsM.V.Lomonosov Moscow State UniversityMoscowRussia

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