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In vivo regulation of thylakoid proton motive force in immature leaves

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Abstract

In chloroplast, proton motive force (pmf) is critical for ATP synthesis and photoprotection. To prevent photoinhibition of photosynthetic apparatus, proton gradient (ΔpH) across the thylakoid membranes needs to be built up to minimize the production of reactive oxygen species (ROS) in thylakoid membranes. However, the regulation of thylakoid pmf in immature leaves is little known. In this study, we compared photosynthetic electron sinks, P700 redox state, non-photochemical quenching (NPQ), and electrochromic shift (ECS) signal in immature and mature leaves of a cultivar of Camellia. The immature leaves displayed lower linear electron flow and cyclic electron flow, but higher levels of NPQ and P700 oxidation ratio under high light. Meanwhile, we found that pmf and ΔpH were higher in the immature leaves. Furthermore, the immature leaves showed significantly lower thylakoid proton conductivity than mature leaves. These results strongly indicated that immature leaves can build up enough ΔpH by modulating proton efflux from the lumenal side to the stromal side of thylakoid membranes, which is essential to prevent photoinhibition via thermal energy dissipation and photosynthetic control of electron transfer. This study highlights that the activity of chloroplast ATP synthase is a key safety valve for photoprotection in immature leaves.

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Abbreviations

CEF:

Cyclic electron flow around photosystem I;

ΔpH:

Proton gradient across the thylakoid membranes

g H + :

Thylakoid proton conductivity

LEF:

Linear electron flow

NPQ:

Non-photochemical quenching

pmf:

Proton motive force

qL:

The fraction of open PSII reaction centers based on the “lake model” of PSII antenna pigment organization

Y(I):

Quantum yield of PSI photochemical quenching

Y(II):

Effective quantum yield of PSII photochemistry

Y(NA):

The quantum yield of PSI non-photochemical energy dissipation due to the acceptor-side limitation

Y(ND):

The quantum yield of PSI non-photochemical energy dissipation due to the donor-side limitation

References

  • Allahverdiyeva Y, Mamedov F, Mäenpää P, Vass I, Aro EM (2005) Modulation of photosynthetic electron transport in the absence of terminal electron acceptors: Characterization of the rbcL deletion mutant of tobacco. Biochimica et Biophysica Acta 1709:69–83

    Article  CAS  Google Scholar 

  • Allakhverdiev SI (2011) Recent progress in the studies of structure and function of photosystem II. J Photochem Photobiol B 104:1–8

    Article  CAS  Google Scholar 

  • Allakhverdiev SI, Nishiyama Y, Takahashi S, Miyairi S, Suzuki I, Murata N (2005) Systematic analysis of the relation of electron transport and ATP synthesis to the photodamage and repair of photosystem II in synechocystis. Plant Physiol 137:263–273

    Article  CAS  Google Scholar 

  • Aro EM, Suorsa M, Rokka A, Allahverdiyeva Y, Paakkarinen V, Salee A, Battchikova N, Rintamaki E (2005) Dynamics of photosystem II: proteomic approach to thylakoid protein complexes. J Exp Bot 56:347–356

    Article  CAS  Google Scholar 

  • Avenson TJ, Cruz JA, Kanazawa A, Kramer DM (2005) Regulating the proton budget of higher plant photosynthesis. Proc Natl Acad Sci USA 102:9709–9713

    Article  Google Scholar 

  • Brestic M, Zivcak M, Kunderlikova K, Sytar O, Shao H, Kalaji HM, Allakhverdiev SI (2015) Low PSI content limits the photoprotection of PSI and PSII in early growth stages of chlorophyll b-deficient wheat mutant lines. Photosynth Res 125:151–166

    Article  CAS  Google Scholar 

  • Cruz AJ, Sacksteder CA, Kanazawa A, Kramer DM (2001) Contribution of electric field (∆Ψ) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of pmf parsing into ∆Ψ and ∆pH by ionic strength. Biochemistry 40:1226–1237

    Article  CAS  Google Scholar 

  • Cruz JA, Avenson TJ, Kanazawa A, Takizawa K, Edwards GE, Kramer DM (2005) Plasticity in light reactions of photosynthesis for energy production and photoprotection. J Exp Bot 56:395–406

    Article  CAS  Google Scholar 

  • Ettinger WF, Clear AM, Fanning KJ, Peck ML (1999) Identification of a Ca2+/H+ antiport in the plant chloroplast thylakoid membrane. Plant Physiol 119:1379–1385

    Article  CAS  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochem Biophys Acta 99:87–92

    Article  Google Scholar 

  • He J, Chow WS (2003) The rate coefficient of repair of photosystem II after photoinactivation. Physiol Plant 118:297–304

    Article  CAS  Google Scholar 

  • Horton P, Ruban AV, Wentworth M (2000) Allosteric regulation of the light-harvesting system of photosystem II. Philos Trans R Soc B: Biol Sci 355:1361–1370

    Article  CAS  Google Scholar 

  • Huang W, Zhang SB, Cao KF (2010a) The different effects of chilling stress under moderate illumination on photosystem II compared with photosystem I and subsequent recovery in tropical tree species. Photosynth Res 103:175–182

    Article  CAS  Google Scholar 

  • Huang W, Zhang SB, Cao KF (2010b) Stimulation of cyclic electron flow during recovery after chilling-induced photoinhibition of PSII. Plant Cell Physiol 51:1922–1928

    Article  CAS  Google Scholar 

  • Huang W, Zhang SB, Cao KF (2011) Cyclic electron flow plays an important role in photoprotection of tropical trees illuminated at temporal chilling temperature. Plant Cell Physiol 52:297–305

    Article  CAS  Google Scholar 

  • Huang W, Yang SJ, Zhang SB, Zhang JL, Cao KF (2012) Cyclic electron flow plays an important role in photoprotection for the resurrection plant Paraboea rufescens under drought stress. Planta 235:819–828

    Article  CAS  Google Scholar 

  • Huang W, Zhang SB, Zhang JL, Hu H (2015) Photoinhibition of photosystem I under high light in the shade-established tropical tree species Psychotria rubra. Front Plant Sci 6:801

    PubMed  PubMed Central  Google Scholar 

  • Huang W, Yang YJ, Hu H, Zhang SB, Cao KF (2016a) Evidence for the role of cyclic electron flow in photoprotection for oxygen-evolving complex. J Plant Physiol 194:54–60

    Article  CAS  Google Scholar 

  • Huang W, Yang YJ, Zhang JL, Hu H, Zhang SB (2016b) PSI photoinhibition is more related to electron transfer from PSII to PSI rather than PSI redox state in Psychotria rubra. Photosynth Res 129:85–92

    Article  CAS  Google Scholar 

  • Huang W, Yang YJ, Zhang SB (2017a) Specific roles of cyclic electron flow around photosystem I in photosynthetic regulation in immature and mature leaves. J Plant Physiol 209:76–83

    Article  CAS  Google Scholar 

  • Huang W, Yang YJ, Zhang JL, Hu H, Zhang SB (2017b) Superoxide generated in the chloroplast stroma causes photoinhibition of photosystem I in the shade-establishing tree species Psychotria henryi. Photosynth Res 132:293–303

    Article  CAS  Google Scholar 

  • Hwang HJ, Kim JH, Eu YJ, Moon BY, Cho SH, Lee CH (2004) Photoinhibition of photosystem I is accelerated by dimethyldithiocarbamate, an inhibitor of superoxide dismutase, during light-chilling of spinach leaves. J Photochem Photobiol B 73:79–85

    Article  CAS  Google Scholar 

  • Johnson GN (2011) Physiology of PSI cyclic electron transport in higher plants. Biochem Biophys Acta 1807:384–389

    CAS  PubMed  Google Scholar 

  • Johnson MP, Ruban AV (2014) Rethinking the existence of a steady-state ∆ψ component of the proton motive force across plant thylakoid membranes. Photosynth Res 119:233–242

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Kanazawa A, Ostendorf E, Kohzuma K, Hoh D, Strand DD, Sato-Cruz M, Savage L, Cruz JA, Fisher N, Froehlich JE, Kramer DM (2017) Chloroplast ATP synthase modulation of the thylakoid proton motive force: Implications for photosystem I and photosystem II photoprotection. Front Plant Sci 8:719

    Article  Google Scholar 

  • Kanervo E, Singh M, Suorsa M, Paakkarinen V, Aro E, Battchikova N, Aro EM (2008) Expression of protein complexes and individual proteins upon transition of etioplasts to chloroplasts in pea (Pisumsativum). Plant Cell Physiol 49:396–410

    Article  CAS  Google Scholar 

  • Karlsson PM, Herdean A, Adolfsson L, Beebo A, Nziengui H, Irigoyen S, Unnep R, Zsiros O, Nagy G, Garab G, Aronsson H, Versaw W, Spetea C (2015) The Arabidopsis thylakoid transporter PHT4;1 influences phosphate availability for ATP synthesis and plant growth. Plant J 84:99–110

    Article  CAS  Google Scholar 

  • Klüghammer C, Schreiber U (2008) Saturation pulse method for assessment of energy conversion in PSI. PAM Appl Notes (PAN) 1:11–14

    Google Scholar 

  • Kohzuma K, Cruz JA, Akashi K, Hoshiyasu S, Munekage YN, Yokota A, Kramer DM (2009) The long-term responses of the photosynthetic proton circuit to drought. Plant Cell Environ 32:209–219

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Kou J, Takahashi S, Oguchi R, Fan DY, Badger MR, Chow WS (2013) Estimation of the steady-state cyclic electron flux around PSI in spinach leaf discs in white light, CO2-enriched air and other varied conditions. Funct Plant Biol 40:1018–1028

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Krieger A, Weis E (1993) The role of calcium in the pH-dependent control of photosystem II. Photosynth Res 37:117–130

    Article  CAS  Google Scholar 

  • Krieger-Liszkay A, Kós PB, Hideg É (2011) Superoxide anion radicals generated by methylviologen in photosystem I damage photosystem II. Physiol Plant 142:17–25

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Kuhlgert S, Austic G, Zegarac R, Osei-Bonsu I, Hoh D, Chilvers MI, Roth M, Bi K, TerAvest D, Weebadde P, Kramer DM (2016) MultispeQ Beta: a tool for large-scale plant phenotyping connected to the open PhotosynQ network. R Soc Open Sci 3:160592

    Article  Google Scholar 

  • Li XP, Müller-Moule P, Gilmore AM, Niyogi KK (2002) PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc Natl Acad Sci USA 99:15222–15227

    Google Scholar 

  • Livingston AK, Cruz JA, Kohzuma K, Dhingra A, Kramer DM (2010) An Arabidopsis mutant with high cyclic electron flow around photosystem I (hcef) involving the NDH complex. Plant Cell 22:221–233

    Article  CAS  Google Scholar 

  • Miller AJ, Fan X, Orsel M, Smith SJ, Wells DM (2007) Nitrate transport and signaling. J Exp Bot 58:2297–2306

    Article  CAS  Google Scholar 

  • Miyake C, Horiguchi S, Makino A, Shinzaki Y, Yamamoto H, Tomizawa K (2005) Effects of light intensity on cyclic electron flow around PSI and its relationship to non-photochemical quenching of Chl fluorescence in tobacco leaves. Plant Cell Physiol 46:1819–1830

    Article  CAS  Google Scholar 

  • 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 94:217–224

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  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

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Niinemets U, Garcia-Plazaola JI, Tosens T (2012) Photosynthesis during leaf development and ageing. In: Flexas J, Loreto F, Medrano H (eds) Terrestrial photosynthesis in a changing environment. A molecular, physiological and ecological approach. Cambridge University Press, Cambridge, pp 353–372

    Chapter  Google Scholar 

  • Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A, Murata N (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J 20:5587–5594

    Article  CAS  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochem Biophys Acta 1757:742–749

    CAS  PubMed  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2011) Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II. Physiol Plant 142:35–46

    Article  CAS  Google Scholar 

  • Oguchi R, Jia H, Barber J, Chow WS (2008) Recovery of photoinactivated photosystem II in leaves retardation due to restricted mobility of photosystem I in the thylakoid membrane. Photosynth Res 98:621–629

    Article  CAS  Google Scholar 

  • Oguchi R, Terashima I, Chow WS (2009) The involvement of dual mechanisms of photoinactivation of photosystem II in Capsicum annuum L. plants. Plant Cell Physiol 50:1815–1825

    Article  CAS  Google Scholar 

  • Oguchi R, Douwstra P, Fujita T, Chow WS, Terashima I (2011) Intra-leaf gradients of photoinhibition induced by different color lights: implications for the dual mechanisms of photoinhibition and for the application of conventional chlorophyll fluorometers. New Phytol 191:146–159

    Article  Google Scholar 

  • Oxborough K, Baker NR (1997) Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components—calculation of qP and Fv’/Fm’ without measuring Fo’. Photosynth Res 54:135–142

    Article  CAS  Google Scholar 

  • Rott M, Martins NF, Thiele W, Lein W, Bock R, Kramer DM, Schottler MA (2011) ATP synthase repression in tobacco restricts photosynthetic electron transport, CO2 assimilation, and plant growth by overacidification of the thylakoid lumen. Plant Cell 23:304–321

    Article  CAS  Google Scholar 

  • Ruban AV, Berera R, Ilioaia C, van Stokkum IHM, Kennis JYM, Pascal AA, van Amerongen H, Robert B, Horton P, van Grondelle R (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450:575–578

    Article  CAS  Google Scholar 

  • Sacksteder CA, Kramer DM (2000) Dark interval relaxation kinetics of absorbance changes as a quantitative probe of steady-state electron transfer. Photosynth Res 66:145–158

    Article  CAS  Google Scholar 

  • Sacksteder CA, Jacoby ME, Kramer DM (2001) A portable, non-focusing optics spectrometer (NoFOSpec) for measurements of steady-state absorbance changes in intact plants. Photosynth Res 70:231–240

    Article  CAS  Google Scholar 

  • Sato R, Ohta H, Masuda S (2014) Prediction of respective contribution of linear electron flow and PGR5-dependent cyclic electron flow to non-photochemical quenching induction. Plant Physiol Biochem 81:190–196

    Article  CAS  Google Scholar 

  • Schmitt FJ, Renger G, Friedrich T, Kreslavski VD, Zharmukhamedov SK, Los DA, Kuznetsov VV, Allakhverdiev SI (2014) Reactive oxygen species:re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms. Biochem Biophys Acta 1837:835–848

    CAS  PubMed  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

    Article  CAS  Google Scholar 

  • Shikanai T (2016) Regulatory network of proton motive force: contribution of cyclic electron transport around photosystem I. Photosynth Res 129:253–260

    Article  CAS  Google Scholar 

  • Shikanai T, Yamamoto H (2017) Contribution of cyclic and pseudo-cyclic electron transport to the formation of proton motive force in chloroplasts. Mol Plant 10:20–29

    Article  CAS  Google Scholar 

  • Shubin VV, Terekhova IN, Kirillov BA, Karapetyan NV (2008) Quantum yield of P700+ photodestruction in isolated photosystem I complexes of the cyanobacterium Arthrospira platensis. Photochem Photobiol Sci 7:956–962

    Article  CAS  Google Scholar 

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

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Suorsa M, Rossi F, Tadini L, Labs M, Colombo M, Jahns P, Kater MM, Leister D, Finazzi G, Aro EM, Barbato R, Pesaresi P (2016) PGR5-PGRL1-dependent cyclic electron transport modulates linear electron transport rate in Arabidopsis thaliana. Mol Plant 9:271–288

    Article  CAS  Google Scholar 

  • Takagi D, Takumi S, Hashiguchi M, Sejima T, Miyake C (2016) Superoxide and singlet oxygen produced within the thylakoid membranes both cause photosystem I photoinhibition. Plant Physiol 171:1626–1634

    Article  CAS  Google Scholar 

  • Takagi D, Amako K, Hashiguchi M, Fukaki H, Ishizaki K, Goh T, Fukao Y, Sano R, Kurata T, Demura T, Sawa S, Miyake C (2017) Chloroplastic ATP synthase builds up proton motive force for preventing reactive oxygen species production in photosystem I. Plant J 91:306–324

    Article  CAS  Google Scholar 

  • Takahashi S, Murata N (2005) Interruption of the Calvin cycle inhibits the repair of photosystem II from photodamage. Biochem Biophys Acta 1708:352–361

    CAS  PubMed  Google Scholar 

  • Takahashi S, Bauwe H, Badger MR (2007) Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem II by suppression of repair but not acceleration of damage processes in Arabidopsis. Plant Physiol 144:487–494

    Article  CAS  Google Scholar 

  • Takahashi S, Milward SE, Fan DY, Chow WS, Badger MR (2009) How does cyclic electron flow alleviate photoinhibition in Arabidopsis?. Plant Physiol 149:1560–1567

    Article  CAS  Google Scholar 

  • Takizawa K, Cruz JA, Kanazawa A, Kramer DM (2007) The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf. Biochem Biophys Acta 1767:1233–1244

    CAS  PubMed  Google Scholar 

  • Takizawa K, Kanazawa A, Kramer DM (2008) Depletion of stromal Pi induces high ‘energy-dependent’ antenna exciton quenching (qE) by decreasing proton conductivity at CFO-CF1 ATP synthase. Plant Cell Environ 31:235–243

    Article  CAS  Google Scholar 

  • Tikkanen M, Aro EM (2014) Integrative regulatory network of plant thylakoid energy transduction. Trends Plant Sci 19:10–17

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Tikkanen M, Rantala S, Aro EM (2015) Electron flow from PSII to PSI under high light is controlled by PGR5 but not by PSBS. Front Plant Sci 6:521

    Article  Google Scholar 

  • Tiwari A, Mamedov F, Grieco M, Suorsa M, Jajoo A, Styring S, Tikkanen M, Aro EM (2016) Photodamage of iron-sulphur clusters in photosystem I induces non-photochemical energy dissipation. Nat Plants 21:16035

    Article  Google Scholar 

  • Vass I (2011) Role of charge recombination processes in photodamage and photoprotection of the photosystem II complex. Physiol Plant 142:6–16

    Article  CAS  Google Scholar 

  • Wang C, Yamamoto H, Shikanai T (2015) Role of cyclic electron transport around photosystem I in regulating proton motive force. Biochem Biophys Acta 1847:931–938

    CAS  PubMed  Google Scholar 

  • Yamamoto H, Kato H, Shinzaki Y (2006) Ferredoxin limits cyclic electron flow around PSI (CEF-PSI) in higher plants—stimulation of CEF-PSI enhances non-photochemical quenching of fluorescence in transplastomic tobacco. Plant Cell Physiol 47:1355–1371

    Article  CAS  Google Scholar 

  • Yamamoto H, Takahashi S, Badger MR, Shikanai T (2016) Artificial remodeling of alternative electron flow by flavodiiron proteins in Arabidopsis. Nat Plants 2:16012

    Article  CAS  Google Scholar 

  • Yamori W, Shikanai T (2016) Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annu Rev Plant Biol 67:81–106

    Article  CAS  Google Scholar 

  • Yamori W, Makino A, Shikanai T (2016) A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice. Sci Rep 6:20147

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Zivcak M, Brestic M, Kunderlikova K, Sytar O, Allakhverdiev SI (2015) Repetitive light pulse-induced photoinhibition of photosystem I severely affects CO2 assimilation and photoprotection in wheat leaves. Photosynth Res 126:449–463

    Article  CAS  Google Scholar 

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Acknowledgements

This work is supported by National Natural Science Foundation of China (Grant No. 31670343) and Youth Innovation Promotion Association of the Chinese Academy of Sciences (Grant No. 2016347).

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  1. Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, Yunnan, China

    Wei Huang & Shi-Bao Zhang

  2. University of Turku, 20014, Turku, Finland

    Marjaana Suorsa

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Huang, W., Suorsa, M. & Zhang, SB. In vivo regulation of thylakoid proton motive force in immature leaves. Photosynth Res 138, 207–218 (2018). https://doi.org/10.1007/s11120-018-0565-1

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