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Repetitive light pulse-induced photoinhibition of photosystem I severely affects CO2 assimilation and photoprotection in wheat leaves

Abstract

It was previously found that photosystem I (PSI) photoinhibition represents mostly irreversible damage with a slow recovery; however, its physiological significance has not been sufficiently characterized. The aim of the study was to assess the effect of PSI photoinhibition on photosynthesis in vivo. The inactivation of PSI was done by a series of short light saturation pulses applied by fluorimeter in darkness (every 10 s for 15 min), which led to decrease of both PSI (~60 %) and photosystem II (PSII) (~15 %) photochemical activity. No PSI recovery was observed within 2 days, whereas the PSII was fully recovered. Strongly limited PSI electron transport led to an imbalance between PSII and PSI photochemistry, with a high excitation pressure on PSII acceptor side and low oxidation of the PSI donor side. Low and delayed light-induced NPQ and P700+ rise in inactivated samples indicated a decrease in formation of transthylakoid proton gradient (ΔpH), which was confirmed also by analysis of electrochromic bandshift (ECSt) records. In parallel with photochemical parameters, the CO2 assimilation was also strongly inhibited, more in low light (~70 %) than in high light (~45 %); the decrease was not caused by stomatal closure. PSI electron transport limited the CO2 assimilation at low to moderate light intensities, but it seems not to be directly responsible for a low CO2 assimilation at high light. In this regard, the possible effects of PSI photoinhibition on the redox signaling in chloroplast and its role in downregulation of Calvin cycle activity are discussed.

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Abbreviations

\(A_{{{\text{CO}}_{2} }}\) :

CO2 assimilation rate

CET:

Cyclic electron transport

cyt b 6/f :

Cytochrome b 6/f

ECS:

Electrochromic shift

ETR:

Apparent electron transport rate

F 0 :

Minimum fluorescence from dark-adapted leaf (PSII centers open)

\(F_{0}^{\prime}\) :

Minimum fluorescence from light-adapted leaf

F m, \(F_{\rm m}^{\prime}\) :

Maximum fluorescence from dark- or light-adapted leaf respectively (PS II centers closed)

FNR:

Ferredoxin NADP+ oxidoreductase

F v/F m :

Maximum quantum yield of PSII photochemistry

gH+ :

Transthylakoid proton conductivity

LED:

Light emitting diode

LHC:

Light harvesting complex

NPQ:

Non-photochemical quenching

P :

P700 absorbance at given light intensity

P700:

Primary electron donor of PSI (reduced form)

P700+ :

Primary electron donor of PSI (oxidized form)

PAM:

Pulse-amplitude modulated

PAR:

Photosynthetic active radiation

P m, \(P_{\rm m}^{\prime}\) :

Maximum P700 signal in dark- or light-adapted state

Pmf:

Proton motive force

PS I:

Photosystem I

PS II:

Photosystem II

Q A :

Primary PSII acceptor

Q A /Q A :

Total Redox poise of the primary electron acceptor of PSII (1 − qP)

qE:

PH dependent energy dissipation

qL:

‘Lake’ model photochemical quenching coefficient

qP:

‘Puddle’ model photochemical quenching coefficient

SP:

Saturation light pulse

ΔpH:

Transthylakoid pH gradient

ΔpHpmf :

Osmotic component of proton motive force

Φ NA :

Quantum yield of non-photochemical energy dissipation in PSI due to acceptor side limitation

Φ ND :

Quantum yield of non-photochemical energy dissipation in PSI due to donor side limitation

Φ NO :

Quantum efficiency of non-regulated energy dissipation in PSII

Φ NPQ :

Quantum yield of pH-dependent energy dissipation in PSII

Φ PSI :

Effective quantum yield (efficiency) of PSI photochemistry at given actinic light intensity

Φ PSII :

Actual quantum yield (efficiency) of PSII photochemistry

Δψ :

Transmembrane electric potential

Δψ pmf :

Electric component of proton motive force

References

  • Alboresi A, Ballottari M, Hienerwadel R, Giacometti GM, Morosinotto T (2009) Antenna complexes protect photosystem I from photoinhibition. BMC Plant Biol 9:71

    PubMed Central  Article  PubMed  Google Scholar 

  • 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 1657:23–32

    CAS  Article  PubMed  Google Scholar 

  • Allakhverdiev SI, Murata N (2008) Salt stress inhibits photosystems II and I in cyanobacteria. Photosynth Res 98:529–539

    CAS  Article  PubMed  Google Scholar 

  • Apostol S, Briantais JM, Moise N, Cerovic Z, Moya I (2001) Photoinactivation of the photosynthetic electron transport chain by accumulation of over-saturating light pulses given to dark adapted pea leaves. Photosynth Res 67:215–227

    CAS  Article  PubMed  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    CAS  Article  PubMed  Google Scholar 

  • Barber J, Andersson B (1994) Revealing the blueprint of photosynthesis. Nature 370:31–34

    CAS  Article  Google Scholar 

  • Brestic M, Zivcak M, Olsovska K, Shao HB, Kalaji HM, Allakhverdiev SI (2014) Reduced glutamine synthetase activity plays a role in control of photosynthetic responses to high light in barley leaves. Plant Physiol Biochem 81:74–83

    CAS  Article  PubMed  Google Scholar 

  • Briantais JM, Vernotte C, Picaud M, Krause GH (1979) A quantitive study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochim Biophys Acta 548:128–138

    CAS  Article  PubMed  Google Scholar 

  • Buchanan BB, Schürmann P, Wolosiuk RA, Jacquot JP (2002) The ferredoxin/thioredoxin system: from discovery to molecular structures and beyond. Photosynth Res 73:215–222

    CAS  Article  PubMed  Google Scholar 

  • Bukhov NG, Carpentier R (2003) Measurement of photochemical quenching of absorbed quanta in photosystem I of intact leaves using simultaneous measurements of absorbance changes at 830 nm and thermal dissipation. Planta 216:630–638

    CAS  PubMed  Google Scholar 

  • Bukhov N, Carpentier R (2004) Alternative photosystem I-driven electron transport routes: mechanisms and functions. Photosynth Res 82:17–33

    CAS  Article  PubMed  Google Scholar 

  • Cardol P, Forti G, Finazzi G (2011) Regulation of electron transport in microalgae. Biochim Biophys Acta 1807:912–918

    CAS  Article  PubMed  Google Scholar 

  • Chazdon R (1988) Sunflecks and their importance to forest understory plants. Adv Ecol Res 18:1–63

    Article  Google Scholar 

  • Chibani K, Couturier J, Selles B, Jacquot JP, Rouhier N (2010) The chloroplastic thiol reducing systems: dual functions in the regulation of carbohydrate metabolism and regeneration of antioxidant enzymes, emphasis on the poplar redoxin equipment. Photosyn Res 104:75–99

    CAS  Article  PubMed  Google Scholar 

  • Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24

    CAS  Article  Google Scholar 

  • Dietz KJ, Pfannschmidt T (2011) Novel regulators in photosynthetic redox control of plant metabolism and gene expression. Plant Physiol 155:1477–1485

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Fischer S, Gräber P (1999) Comparison of ΔpH- and Δφ-driven ATP synthesis catalyzed by H + -ATPases from Escherichia coli or chloroplasts reconstituted into liposomes. FEBS Lett 457:327–332

    CAS  Article  PubMed  Google Scholar 

  • Goltsev V, Zaharieva I, Chernev P, Kouzmanova M, Kalaji MH, Yordanov I, Krasteva V, Alexandrov V, Stefanov D, Allakhverdiev SI, Strasser RJ (2012) Drought-induced modifications of photosynthetic electron transport in intact leaves: analysis and use of neural networks as a tool for a rapid non-invasive estimation. Biochim Biophys Acta 1817:1490–1498

    CAS  Article  PubMed  Google Scholar 

  • Grieco M, Tikkanen M, Paakkarinen V, Kangasjärvi S, Aro EM (2012) Steady-state phosphorylation of light-harvesting complex II proteins preserves Photosystem I under fluctuating white light. Plant Physiol 160:1896–1910

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • Ivanov AG, Morgan R, Gray G, Velitchkova M, Huner NP (1998) Temperature/light dependent development of selective resistance to photoinhibition of photosystem I. FEBS Lett 430:288–292

    CAS  Article  PubMed  Google Scholar 

  • Ivanov AG, Krol M, Zeinalov Y, Huner NPA, Sane PV (2008) The lack of LHCII proteins modulates excitation energy partitioning and PSII charge recombination in Chlorina F2 mutant of barley. Physiol Mol Biol Plants 14:205–215

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Joliot P, Johnson GN (2011) Regulation of cyclic and linear electron flow in higher plants. Proc Natl Acad Sci USA 108:13317–13322

    PubMed Central  CAS  Article  PubMed  Google Scholar 

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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Jones HG (1985) Partitioning stomatal and non-stomatal limitations to photosynthesis. Plant Cell Environ 8:95–104

    Article  Google Scholar 

  • Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI et al (2014) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res 122:121–158

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Klughammer C, Schreiber U (1994) Saturation pulse method for assessment of energy conversion in PS I. Planta 192:261–268

    CAS  Article  Google Scholar 

  • Klughammer C, Siebke K, Schreiber U (2013) Continuous ECS-indicated recording of the proton-motive charge flux in leaves. Photosynth Res 117:471–487

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Kono M, Terashima I (2014) Long-term and short-term responses of the photosynthetic electron transport to fluctuating light. J Photochem Photobiol B 137:89–99

    CAS  Article  PubMed  Google Scholar 

  • Kono M, Noguchi K, Terashima I (2014) Roles of the cyclic electron flow around PSI (CEF-PSI) and O2-dependent alternative pathways in regulation of the photosynthetic electron flow in short-term fluctuating light in Arabidopsis thaliana. Plant Cell Physiol 55:990–1004

    CAS  Article  PubMed  Google Scholar 

  • Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155:70–78

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Kramer DM, Cruz JA, Kanazawa A (2003) Balancing the central roles of the thylakoid proton gradient. Trends Plant Sci 8:27–32

    CAS  Article  PubMed  Google Scholar 

  • Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218

    CAS  Article  PubMed  Google Scholar 

  • Kudoh H, Sonoike K (2002) Irreversible damage to photosystem I by chilling in the light: cause of the degradation of chlorophyll after returning to normal growth temperature. Planta 215:541–548

    CAS  Article  PubMed  Google Scholar 

  • Lemaire SD, Michelet L, Zaffagnini M, Massot V, Issakidis-Bourguet E (2007) Thioredoxins in chloroplasts. Curr Genet 51:343–365

    CAS  Article  PubMed  Google Scholar 

  • Li XP, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395

    CAS  Article  PubMed  Google Scholar 

  • Long SP, Drake BG (1991) Effect of the long-term elevation of CO2 concentration in the field on the quantum yield of photosynthesis of the C3 sedge, Scirpus-olneyi. Plant Physiol 96:221–226

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Meyer Y, Belin C, Delorme-Hinoux V, Reichheld JP, Riondet C (2012) Thioredoxin and glutaredoxin systems in plants: molecular mechanisms, crosstalks, and functional significance. Antioxid Redox Signal 17:1124–1160

    CAS  Article  PubMed  Google Scholar 

  • Mitchell P (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol Rev 41:445–502

    CAS  Article  PubMed  Google Scholar 

  • Miyake C (2010) Alternative electron flows (water–water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. Plant Cell Physiol 51:1951–1963

    CAS  Article  PubMed  Google Scholar 

  • Miyake C, Miyata M, Shinzaki Y, Tomizawa KI (2005) CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves—relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of Chl fluorescence. Plant Cell Physiol 46:629–637

    CAS  Article  PubMed  Google Scholar 

  • Munekage Y, Hashimoto M, Miyake C, Tomizawa KI, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582

    CAS  Article  PubMed  Google Scholar 

  • Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421

    CAS  Article  PubMed  Google Scholar 

  • Ögren E, Evans JR (1993) Photosynthetic light-response curves. Planta 189:182–190

    Article  Google Scholar 

  • Okegawa Y, Kagawa Y, Kobayashi Y, Shikanai T (2008) Characterization of factors affecting the activity of photosystem I cyclic electron transport in chloroplasts. Plant Cell Physiol 49:825–834

    CAS  Article  PubMed  Google Scholar 

  • Pearcy RW, Chazdon RL, Gross LJ, Mott KA (1994) Photosynthetic utilization of sunflecks: a temporally patchy resource on a time scale of seconds to minutes. In: Caldwell MM, Pearcy RW (eds) Exploitation of environmental heterogeneity by plants. Academic Press, San Diego, pp 175–208

    Chapter  Google Scholar 

  • Powles SB (1984) Photoinhibition of Photosynthesis Induced by Visible Light. Annu Rev Plant Physiol 35:15–44

    CAS  Article  Google Scholar 

  • Purcell M, Carpentier R (1994) Homogeneous photobleaching of chlorophyll holochromes in a photosystem I reaction center complex. Photochem Photobiol 59:215–218

    CAS  Article  Google Scholar 

  • Rajagopal S, Bukhov NG, Carpentier R (2002) Changes in the structure of chlorophyll-protein complexes and excitation energy transfer during photoinhibitory treatment of isolated photosystem I submembrane particles. J Photochem Photobiol B 62:194–200

    Article  Google Scholar 

  • Rajagopal S, Bukhov NG, Carpentier R (2003) Photoinhibitory light-induced changes in the composition of chlorophyll-protein complexes and photochemical activity in photosystem-I submembrane fractions. Photochem Photobiol 77:284–291

    CAS  Article  PubMed  Google Scholar 

  • Ruban AV, Walters RG, Horton P (1992) The molecular mechanism of the control of excitation energy dissipation in chloroplast membranes inhibition of pH-dependent quenching of chlorophyll fluorescence by dicyclohexylcarbodiimide. FEBS Lett 309:175–179

    CAS  Article  PubMed  Google Scholar 

  • Ruelland E, Miginiac-Maslow M (1999) Regulation of chloroplast enzyme activities by thioredoxins: activation or relief from inhibition? Trends Plant Sci 4:136–141

    Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • Sacksteder CA, Kanazawa A, Jacoby ME, Kramer DM (2000) The proton to electron stoichiometry of steady-state photosynthesis in living plants: a proton-pumping Q-cycle is continuously engaged. Proc Natl Acad Sci USA 97:14283–14288

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Scheller HV, Haldrup A (2005) Photoinhibition of photosystem I. Planta 221:5–8

    CAS  Article  PubMed  Google Scholar 

  • Schürmann P, Buchanan BB (2008) The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxid Redox Signal 10:1235–1274

    Article  PubMed  Google Scholar 

  • Sejima T, Takagi D, Fukayama H, Makino A, Miyake C (2014) Repetitive short-pulse light mainly inactivates photosystem I in sunflower leaves. Plant Cell Physiol. doi:10.1093/pcp/pcu061

    PubMed  Google Scholar 

  • Shen Y-K, Chow WS, Park Y-I, Anderson JM (1996) Photoinactivation of Photosystem II by cumulative exposure to short light pulses during the induction period of photosynthesis. Photosynth Res 47:51–59

    CAS  Article  PubMed  Google Scholar 

  • Shikanai T (2012) Cyclic electron transport around photosystem I; genetic approaches. Annu Rev Plant Biol 58:199–217

    Article  Google Scholar 

  • Shikanai T (2014) Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis. Curr Opin Biotechnol 26:25–30

    CAS  Article  PubMed  Google Scholar 

  • Sonoike K (1996) Photoinhibition of photosystem I: its physiological significance in the chilling sensitivity of plants. Plant Cell Physiol 37:239–247

    CAS  Article  Google Scholar 

  • Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64

    CAS  Article  PubMed  Google Scholar 

  • Sonoike K, Terashima I (1994) Mechanism of photosystem-I photoinhibition in leaves of Cucumis sativus L. Planta 194:287–293

    CAS  Article  Google Scholar 

  • Sonoike K, Kamo M, Hihara Y, Hiyama T, Enami I (1997) The mechanism of the degradation of PsaB gene product, one of the photosynthetic reaction centre subunits of photosystem I, upon photoinhibition. Photosynth Res 53:55–63

    CAS  Article  Google Scholar 

  • Suorsa M, Jarvi S, Grieco M, Nurmi M, Pietrzykowska M, Rantala M, Kangasjarvi S, Paakkarinen V, Tikkanen M, Jansson S, Aro EM (2012) Proton gradient regulation5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. Plant Cell 24:2934–2948

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Szyszka B, Ivanov AG, Huner NP (2007) Psychrophily is associated with differential energy partitioning, photosystem stoichiometry and polypeptide phosphorylation in Chlamydomonas raudensis. Biochim Biophys Acta 1767:789–800

    CAS  Article  PubMed  Google Scholar 

  • Teicher HB, Møller BL, Scheller HV (2000) Photoinhibition of photosystem I in field-grown barley (Hordeum vulgare L.): induction, recovery and acclimation. Photosynth Res 64:53–61

    CAS  Article  Google Scholar 

  • Terashima I, Funayama S, Sonoike K (1994) The site of photoinhibition in leaves of Cucumis sativus L. at low temperatures is photosystem I, not photosystem II. Planta 193:300–306

    CAS  Article  Google Scholar 

  • Thiele A, Winter K, Krause GH (1997) Low inactivation of D1 protein of photosystem II in young canopy leaves of Anacardium excelsum under high-light stress. J Plant Physiol 151:286–292

    CAS  Article  Google Scholar 

  • Tikkanen M, Grieco M, Nurmi M, Rantala M, Suorsa M, Aro EM (2012) Regulation of the photosynthetic apparatus under fluctuating growth light. Philos Trans Roy Soc B 367:3486–3493

    CAS  Article  Google Scholar 

  • Tikkanen M, Mekala NR, Aro EM (2014) Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage. Biochim Biophys Acta 1837:210–215

    CAS  Article  PubMed  Google Scholar 

  • Tjus SE, Møller BL (1998) Scheller HV (1998) Photosystem I is an early target of photoinhibition in barley illuminated at chilling temperatures. Plant Physiol 116:755–764

    CAS  Article  PubMed  Google Scholar 

  • Tjus SE, Møller BL, Scheller HV (1999) Photoinhibition of photosystem I damages both reaction centre proteins PSI-A and PSI-B and acceptor-side located small photosystem I polypeptides. Photosynth Res 60:75–86

    CAS  Article  Google Scholar 

  • Wang LF, Chen YY (2013) Characterization of a wide leaf mutant of rice (Oryza sativa L.) with high yield potential in field. Pak J Bot 45:921–926

    Google Scholar 

  • Wang C, Yamamoto H, Shikanai T (2015) Role of cyclic electron transport around photosystem I in regulating proton motive force. Biochim Biophys Acta. doi:10.1016/j.bbabio.2014.11.013

    Google Scholar 

  • 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. Kluwer, Dordrecht, pp 553–556

    Chapter  Google Scholar 

  • Witt HT (1979) Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods the central role of the electric field. Biochim Biophys Acta 505:355–427

    CAS  Article  PubMed  Google Scholar 

  • Wolosiuk RA, Buchanan BB (1977) Thioredoxin and glutathione regulate photosynthesis in chloroplasts. Nature 266:565–567

    CAS  Article  Google Scholar 

  • Zhang S, Scheller HV (2004) Photoinhibition of photosystem I at chilling temperature and subsequent recovery in Arabidopsis thaliana. Plant Cell Physiol 45:1595–1602

    CAS  Article  PubMed  Google Scholar 

  • Zhang ZS, Jia YJ, Gao HY, Zhang LT, Li HD, Meng QW (2011) Characterization of PSI recovery after chilling-induced photoinhibition in cucumber (Cucumis sativus L.) leaves. Planta 234:883–889

    CAS  Article  PubMed  Google Scholar 

  • Zivcak M, Brestic M, Balatová Z, Drevenaková P, Olsovska K, Kalaji HM, Allakhverdiev SI (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth Res 117:529–546

    CAS  Article  PubMed  Google Scholar 

  • Zivcak M, Brestic M, Kalaji HM, Govindjee (2014a) Photosynthetic responses of sun-and shade-grown barley leaves to high light: is the lower PSII connectivity in shade leaves associated with protection against excess of light? Photosynth Res 119:339–354

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Zivcak M, Kalaji HM, Shao HB, Olšovská K, Brestič M (2014b) Photosynthetic proton and electron transport in wheat leaves under prolonged moderate drought stress. J Photochem Photobiol B 137:107–115

    CAS  Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the European Community under the project no. 26220220180: “Construction of the “AgroBioTech” Research Centre and  project “Center of Excellence for Agrobiodiversity Conservation and Use, ECOVA”.” SIA was supported by Grants from the Russian Foundation for Basic Research (Nos. 14-04-01549, 14-04-92690), and by Molecular and Cell Biology Programs of the Russian Academy of Sciences.

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Correspondence to Marian Brestic or Suleyman I. Allakhverdiev.

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Zivcak, M., Brestic, M., Kunderlikova, K. et al. Repetitive light pulse-induced photoinhibition of photosystem I severely affects CO2 assimilation and photoprotection in wheat leaves. Photosynth Res 126, 449–463 (2015). https://doi.org/10.1007/s11120-015-0121-1

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Keywords

  • PSI photoinactivation
  • Transthylakoid proton gradient
  • Non-photochemical quenching
  • Electrochromic bandshift
  • P700