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Analysis of the changes of electron transfer and heterogeneity of photosystem II in Deg1-reduced Arabidopsis plants

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Abstract

Deg1 protease functions in protease and chaperone of PSII complex components, but few works were performed to study the effects of Deg1 on electron transport activities on the donor and acceptor side of PSII and its correlation with the photoprotection of PSII during photoinhibition. Therefore, we performed systematic and comprehensive investigations of electron transfers on the donor and acceptor sides of photosystem II (PSII) in the Deg1-reduced transgenic lines deg1-2 and deg1-4. Both the maximal quantum efficiency of PSII photochemistry (Fv/Fm) and the actual PSII efficiency (ΦPSII) decreased significantly in the transgenic plants. Increases in nonphotochemical quenching (NPQ) and the dissipated energy flux per reaction center (DI0/RC) were also shown in the transgenic plants. Along with the decreased D1, CP47, and CP43 content, these results suggested photoinhibition under growth light conditions in transgenic plants. Decreased Deg1 caused inhibition of electron transfer on the PSII reducing side, leading to a decline in the number of QB-reducing centers and accumulation of QB-nonreducing centers. The Tm of the Q band shifted from 5.7 °C in the wild-type plant to 10.4 °C and 14.2 °C in the deg1-2 and deg1-4 plants, respectively, indicating an increase in the stability of S2QA¯ in transgenic plants. PSIIα in the transgenic plants largely reduced, while PSIIβ and PSIIγ increased with the decline in the Deg1 levels in transgenic plants suggesting PSIIα centers gradually converted into PSIIβ and PSIIγ centers in the transgenic plants. Besides, the connectivity of PSIIα and PSIIβ was downregulated in transgenic plants. Our results reveal that downregulation of Deg1 protein levels induced photoinhibition in transgenic plants, leading to loss of PSII activities on both the donor and acceptor sides in transgenic plants. These results give a new insight into the regulation role of Deg1 in PSII electron transport.

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References

  • Allahverdiyeva Y, Deak Z, Szilard A, Diner BA, Nixon PJ, Vass I (2004) The function of D1–H332 in Photosystem II electron transport studied by thermoluminescence and chlorophyll fluorescence in site-directed mutants of Synechocystis 6803. Euro J Biochem 271:3523–3532

    CAS  Google Scholar 

  • Allahverdiyeva Y, Mamedov F, Holmström M, Nurmi M, Lundin B, Styring S, Spetea C, Aro E-M (2009) Comparison of the electron transport properties of the psbo1 and psbo2 mutants of Arabidopsis thaliana. Biochim Biophys Acta 1787:1230–1237

    CAS  PubMed  Google Scholar 

  • Allahverdiyeva Y, Aro E-M (2012) Photosynthetic responses of plants to excess light: mechanisms and conditions for photoinhibition, excess energy dissipation and repair. In: Eaton-Rye JJ, Tripathy BC, Sharkey TD (eds) Photosynthesis: Plastid Biology, Energy Conversion and Carbon Assimilation. Advances in Photosynthesis and Respiration 34, Springer Science+Business Media BV, pp 275–297

    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  PubMed  Google Scholar 

  • Allakhverdiev SI (2020) Optimising photosynthesis for environmental fitness. Funct Plant Biol 47:iii–vii

    PubMed  Google Scholar 

  • Andersson JM, Melis A (1983) Localization of different photosystems in separate regions of chloroplast membranes. Proc Natl Acad Sci USA 80:745–749

    Google Scholar 

  • Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of Photosystem II Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134

    CAS  PubMed  Google Scholar 

  • Barker M, de Vries R, Nield J, Komenda J, Nixon PJ (2006) The deg proteases protect Synechocystis sp PCC 6803 during heat and light stresses but are not essential for removal of damaged D1 protein during the photosystem two repair cycle. J Biol Chem 281:30347–30355

    CAS  PubMed  Google Scholar 

  • Bassi R, Marquardt J, Lavergne J (1995) Biochemical and functional properties of photosystem II in agranal membranes from maize mesophyll and bundle sheath chloroplasts. Eur J Biochem 233:709–719

    CAS  PubMed  Google Scholar 

  • Briantais JM, Ducruet JM, Hodges M, Krause GH (1992) The effects of low temperature acclimation and photoinhibitory treatments on photosystem 2 studied by thermoluminescence and fluorescence decay kinetics. Photosynth Res 31:1–10

    CAS  PubMed  Google Scholar 

  • Bricker TM, Roose JL, Fagerlund RD, Frankel LK, Eaton-Rye JJ (2012) The extrinsic proteins of Photosystem II. Biochim Biophys Acta 1817:121–142

    CAS  PubMed  Google Scholar 

  • Bukhov NG, Carpentier R (2000) Heterogeneity of photosystem II reaction centers as influenced by heat treatment of barley leaves. Physiol Plant 110:279–285

    CAS  Google Scholar 

  • Butenko Y, Lin A, Naveh L, Kupervaser M, Levin Y, Reich Z, Adam Z (2018) Differential roles of the thylakoid lumenal deg protease homologs in chloroplast proteostasis. Plant Physiol 178:1065–1080

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burnap RL, Shen J-R, Jursinic PA, Inoue Y, Sherman LA (1992) Oxygen yield and thermoluminescence characteristics of a cyanobacterium lacking the manganese-stabilizing protein of photosystem II. Biochemistry 31:7404–7410

    CAS  PubMed  Google Scholar 

  • Chassin Y, Kapri-Pardes E, Sinvany G, Arad T, Adam Z (2002) Expression and characterization of the thylakoid lumen protease DegP1 from Arabidopsis. Plant Physiol 130:857–864

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cheregi O, Sicora C, Kos PB, Barker M, Nixon PJ, Vass I (2007) The role of the FtsH and Deg proteases in the repair of UV-B radiation-damaged Photosystem II in the cyanobacterium Synechocystis PCC 6803. Biochim Biophys Acta 1767:820–828

    CAS  PubMed  Google Scholar 

  • Chylla RA, Whitmarsh J (1989) Inactive photosystem II complexes in leaves: Turnover rate and quantitation. Plant Physiol 90:765–772

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clausen T, Kaiser M, Huber R, Ehrmann M (2011) HTRA proteases: regulated proteolysis in protein quality control. Nat Rev Mol Cell Biol 12:152–162

    CAS  PubMed  Google Scholar 

  • Dau H (1994) Molecular mechanisms and quantitative models of variable photosystem II fluorescence. Photochem Photobiol 60:1–23

    CAS  Google Scholar 

  • Ding S, Jiang R, Lu Q, Wen X, Lu C (2016) Glutathione reductase 2 maintains the function of photosystem II in Arabidopsis under excess light Biochim Biophys. Acta 1857:665–677

    CAS  Google Scholar 

  • Ducruet J-M (2003) Chlorophyll thermoluminescence of leaf discs: simple instruments and progress in signal interpretation open the way to new ecophysiological indicators. J Exp Bot 54:2419–2430

    CAS  PubMed  Google Scholar 

  • Duysens LNM, Sweers HE (1963) Mechanisms of two photochemical reactions in algae as studied by means of fluorescence. In: Japanese Society of Plant Physiologists (ed) Studies on microalgae and photosynthetic bacteria. Special Issue of Plant and Cell Physiology. University of Tokyo Press, Tokyo, pp 353–372

    Google Scholar 

  • Falk S, Leverenz JW, Samuelsson G, Öquist G (1992) Changes in Photosystem II fluorescence in Chlamydomonas reinhardtii exposed to increasing levels of irradiance in relationship to the photosynthetic response to light. Photosynth Res 31:31–40

    CAS  PubMed  Google Scholar 

  • Gong H, Tang Y, Wang J, Wen X, Zhang L, Lu C (2008) Characterization of photosystem II in salt-stressed cyanobacterial Spirulina platensis cells. Biochim Biophys Acta 1777:488–495

    CAS  PubMed  Google Scholar 

  • Govindjee (1995) Sixty-three years since Kautsky:chlorophyll a fluorescence. Aust J Plant Physiol 22:131–160

    CAS  Google Scholar 

  • Graan T, Ort DR (1986) Detection of oxygen-evolving Photosystem II centers inactive in plastoquinone reduction. Biochim Biophys Acta 852:320–330

    CAS  Google Scholar 

  • Hankamer B, Barber J, Boekema EJ (1997) Structure and membrane organization of Photosystem II in green plants. Annu Rev Plant Physiol Plant Mol Biol 48:641–671

    CAS  PubMed  Google Scholar 

  • Hansen G, Hilgenfeld R (2013) Architecture and regulation of HtrA-family proteins involved in protein quality control and stress response. Cell Mol Life Sci 70:761–775

    CAS  PubMed  Google Scholar 

  • Haussühl K, Andersson B, Adamska I (2001) A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II. EMBO J 20:713–722

    PubMed  PubMed Central  Google Scholar 

  • Hsu B, Lee J (1991) A study on the fluorescence induction curve of the DCMU-poisoned chloroplast. Biochim Biophys Acta 1056:285–292

    CAS  Google Scholar 

  • Hsu B, Lee J (1995) The Photosystem II heterogeneity of chlorophyll b-deficient mutants of rice: a fluorescence induction study. Aust J Plant Physiol 22:195–200

    Google Scholar 

  • Hsu B, Lee Y, Jang Y (1989) A method for analysis of fluorescence induction curve from DCMU-poisoned chloroplasts. Biochim Biophys Acta 975:44–49

    CAS  Google Scholar 

  • Hubbart S, Ajigboye OO, Horton P, Murchie EH (2012) The photoprotective protein PsbS exerts control over CO2 assimilation rate in fluctuating light in rice. Plant J 71:402–412

    CAS  PubMed  Google Scholar 

  • Huesgen P, Schumann H, Adamska I (2006) Photodamaged D1 protein is degraded in Arabidopsis mutants lacking the Deg2 protease. FEBS Lett 580:6929–6932

    CAS  PubMed  Google Scholar 

  • Itzhaki H, Naveh L, Lindahl M, Cook M, Adam Z (1998) Identification and characterization of DegP, a serine protease associated with the luminal side of the thylakoid membrane. J Biol Chem 273:7094–7098

    CAS  PubMed  Google Scholar 

  • Kato MC, Hikosaka K, Hirose T (2002) Photoinactivation and recovery of photosystem II in Chenopodium album leaves grown at different levels of irradiance and nitrogen availability. Funct Plant Biol 29:787–795

    CAS  PubMed  Google Scholar 

  • Kato Y, Ozawa S, Takahashi Y, Sakamoto W (2015) D1 fragmentation in photosystem II repair caused by photo-damage of a two-step model. Photosynth Res 126:409–416

    CAS  PubMed  Google Scholar 

  • Kapri-Pardes E, Naveh L, Adam Z (2007) The thylakoid lumen protease Deg1 is involved in the repair of Photosystem II from photoinhibition in Arabidopsis. Plant Cell 19:1039–1047

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kieselbacha T, Funk C (2003) The family of Deg/HtrA proteases: from Escherichia coli to Arabidopsis. Physiol Plantarum 119:337–346

    Google Scholar 

  • Kirchhoff H, Borinski M, Lenhert S, Chi L, Büchel C (2004) Transversal and lateral exciton energy transfer in grana thylakoids of spinach. Biochemistry 43:14508–14516

    CAS  PubMed  Google Scholar 

  • Kley J, Schmidt B, Boyanov B, Stolt-Bergner PC, Kirk R, Ehrmann M, Knopf RR, Naveh L, Adam Z, Clausen T (2011) Structural adaptation of the plant protease Deg1 to repair photosystem II during light exposure. Nat Struct Mol Biol 18:728–731

    CAS  PubMed  Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: The basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349

    CAS  Google Scholar 

  • Kulik N, Kutý M, Řeha D (2020) The study of conformational changes in photosystem II during a charge separation. J Mol Model 26:75

    CAS  PubMed  Google Scholar 

  • Lavergne J, Braintais J-M (1996) Photosystem II heterogeneity. In: Ort DR, Yocum CF (eds) Oxygenic photosynthesis: the light reactions. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 265–287

    Google Scholar 

  • Lavergne J, Leci E (1993) Properties of inactive Photosystem II centers. Photosynth Res 38:323–343

    Google Scholar 

  • Lazar D, Tomek P, Ilík P, Naus J (2001) Determination of the antenna heterogeneity of PS II by direct simultaneous fitting of several fluorescence rise curves measured with DCMU at different light intensities. Photosynth Res 68:247–257

    CAS  PubMed  Google Scholar 

  • Li J, Sun XW, Zhang LX (2010) Deg1 is involved in the degradation of the PsbO oxygen-evolving protein of photosystem II in Arabidopsis. Chin Sci Bull 55:3145–3148

    CAS  Google Scholar 

  • Li L, Aro E-M, Millar AH (2018) Mechanisms of photodamage and protein turnover in photoinhibition. Trends Plant Sci 23:667–676

    CAS  PubMed  Google Scholar 

  • Lindahl M, Spetea C, Hundal T, Oppenheim AB, Adam Z, Andersson B (2000) The thylakoid FtsH protease plays a role in the light-induced turnover of the Photosystem II D1 protein. Plant Cell 12:419–431

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Frankel LK, Bricker TM (2007) Functional analysis of photosystem II in a PsbO-1-deficient mutant in Arabidopsis thaliana. Biochemistry-Us 46:7607–7613

    CAS  Google Scholar 

  • Liu H, Blankenship RE (2019) On the interface of light-harvesting antenna complexes and reaction centers in oxygenic photosynthesis. Biochim Biophys Acta 1860:148079

    CAS  Google Scholar 

  • Liu J, Yang H, Lu Q, Wen X, Chen F, Peng L, Zhang L, Lu C (2012) PsbP-domain protein1, a nuclear-encoded thylakoid luminal protein, is essential for photosystem I assembly in Arabidopsis. Plant Cell 24:4992–5006

    CAS  PubMed  PubMed Central  Google Scholar 

  • Long SP, Humphries S (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45:633–662

    CAS  Google Scholar 

  • Mäenpää P, Miranda T, Tyystjarvi E, Tyystjarvi T, Govindjee D-M, Etienne AL, Kirilovsky D (1995) A mutation in the D-de loop of D1 modifies the stability of the S2QA¯ and S2QB¯ states in photosystem II. Plant Physiol 107:187–197

    PubMed  PubMed Central  Google Scholar 

  • Mathur S, Allakhverdiev SI, Jajoo A (2011) Analysis of high temperature stress on the dynamics of antenna size and reducing side heterogeneity of Photosystem II in wheat leaves (Triticum aestivum). Biochim Biophys Acta 1807:22–29

    CAS  PubMed  Google Scholar 

  • de Marchin T, Ghysels B, Nicolay S, Franck F (2014) Analysis of PSII antenna size heterogeneity of Chlamydomonas reinhardtii during state transitions. Biochim Biophys Acta 1837:121–130

    PubMed  Google Scholar 

  • Martínez-García JF, Monte E, Quail PH (1999) A simple, rapid and quantitative method for preparing Arabidopsis protein extracts for immunoblot analysis. Plant J 20:251–257

    PubMed  Google Scholar 

  • Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: What modulates the rate of photodamage in vivo? Trends Plant Sci 4:130–135

    CAS  PubMed  Google Scholar 

  • Melis A, Guenther GE, Morrissey PJ, Ghirardi ML (1988) Photosystem II heterogeneity in chloroplasts. In: Lichtenthaler HK (ed) Applications of chlorophyll fluorescence. Kluwer Acad Press, Springer, Netherlands, pp 33–43

    Google Scholar 

  • Melis A, Homann PH (1975) Kinetic analysis of the fluorescence induction in 3(3,4-dichlorophenyl)-1,1-dimethylurea poisoned chloroplasts. Photochem Photobiol 21:431–437

    CAS  Google Scholar 

  • Meurer J, Meierhoff K, Westhoff P (1996) Isolation of high chlorophyll-fluorescence mutants of Arabidopsis thaliana and their characterization by spectroscopy, immunoblotting and northern hybridization. Planta 198:385–396

    CAS  PubMed  Google Scholar 

  • Michel H, Deisenhofer J (1988) Relevance of the photosynthetic reaction center from purple bacteria to the structure of photosystem-II. Biochemistry 27:1–7

    CAS  Google Scholar 

  • Morrissey PJ, Glick RE, Melis A (1989) Supramolecular assembly and function of subunits associated with the chlorophyll a-b light-harvesting complex II (LHC II) in soybean chloroplasts. Plant Cell Physiol 30:335–344

    CAS  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  PubMed  Google Scholar 

  • Nanba O, Satoh K (1987) Isolation of a photosystem-II reaction center containing D1 and D2 polypeptides and cytochrome b-559. Proc Natl Acad Sci U S A 84:109–112

    CAS  PubMed  PubMed Central  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. Biochim Biophys Acta 1757:742–749

    CAS  PubMed  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol 50:333–339

    CAS  Google Scholar 

  • Niyogi KK, Li X-P, Rosenberg V, Jung H-S (2005) Is PsbS the site of non-photochemical quenching in photosynthesis? J Exp Bot 56:375–382

    CAS  PubMed  Google Scholar 

  • Ohad I, Koike H, Shochat S, Inoue Y (1988) Changes in the properties of reaction centers during the initial stages of photoinhibition as revealed by thermoluminescence measurements. Biochim Biophys Acta 993:288–298

    Google Scholar 

  • Peltier JB, Emanuelsson O, Kalume DE, Ytterberg J, Friso G, Rudella A, Liberles DA, Söderberg L, Roepstorff P, von Heijne G (2002) Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. Plant Cell 14:211–236

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rappaport F, Cuni A, Xiong L, Sayre RT, Lavergne J (2005) Charge recombination and thermoluminescence in photosystem II. Biophys J 88:1948–1958

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rutherford AW, Crofts AR, Inoue Y (1982) Thermoluminescence as a probe of photosystem II photochemistry: the origin of the flash-induced glow peaks. Biochim Biophys Acta 689:457–465

    Google Scholar 

  • Sane PV, Ivanov AG, Hurry V, Huner NPA, Öquist G (2003) Changes in redox potential of primary and secondary electron-accepting quinones in photosystem II confer increased resistance to photoinhibition in low temperature acclimated Arabidopsis. Plant Physiol 132:2144–2151

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schansker G, Tóth SZ, Holzwarth AR, Garab G (2014) Chlorophyll a fluorescence: beyond the limits of the QA-model. Photosynth Res 120:43–58

    CAS  PubMed  Google Scholar 

  • Schuhmann H, Adamska I (2012) Deg proteases and their role in protein quality control and processing in different subcellular compartments of the plant cell. Physiol Plant 145:224–234

    CAS  PubMed  Google Scholar 

  • Schubert M, Petersson UA, Haas BJ, Funk C, Schröder WP, Kieselbach T (2002) Proteome map of the chloroplast lumen of Arabidopsis thaliana. J Biol Chem 277:8354–8365

    CAS  PubMed  Google Scholar 

  • Shen JR, Henmi T, Kamiya N (2008) Structure and function of photosystem II. In: Fromme P (ed) Photosynthetic protein complexes: a structural approach. WILEY-VCH Verlag GmbH & Co KGaA, Weinheim, pp 83–106

    Google Scholar 

  • Spiess C, Beil A, Ehrmann M (1999) A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97:339–347

    CAS  PubMed  Google Scholar 

  • Stirbet A, Govindjee, (2012) Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise. Photosynth Res 113:15–61

    CAS  PubMed  Google Scholar 

  • Strasser RJ, Srivastava A, Govindjee, (1995) Polyphasic chlorophyll a fluorescence transients in plants and cyanobacteria. Photochem Photobiol 61:32–42

    CAS  Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820 nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim Biophys Acta 1797:1313–1326

    CAS  PubMed  Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of chlorophyll a fluorescence transient. In: Papageorgiou G, Govindjee (Eds) Advances in photosynthesis and respiration: chlorophyll a fluorescence: a signature of photosynthesis. Springer Publishers, Dordrecht The Netherlands, pp 321–362

    Google Scholar 

  • Sun X, Fu T, Chen N, Guo J, Ma J, Zou M, Lu C, Zhang L (2010a) The stromal chloroplast Deg7 protease participates in the repair of photosystem II after photoinhibition in Arabidopsis. Plant Physiol 152:1263–1273

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun X, Ouyang M, Guo J, Ma J, Lu C, Adam Z, Zhang L (2010b) The thylakoid protease Deg1 is involved in photosystem-II assembly in Arabidopsis thaliana. Plant J 62:240–249

    CAS  PubMed  Google Scholar 

  • Sun X, Peng LW, Guo JK, Chi W, Ma JF, Lu CM, Zhang LX (2007) Formation of Deg5 and Deg8 complexes and their involvement in the degradation of photodamaged Photosystem II reaction center D1 protein in Arabidopsis thaliana. Plant Cell 19:1347–1361

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vass I, Ono T, Inoue Y (1987) Removal of 33 kDa extrinsic protein specifically stabilizes the charge pair in photosystem II. FEBS Lett 211:71–76

    Google Scholar 

  • Vass I (2012) Molecular mechanisms of photodamage in the Photosystem II complex. Biochim Biophys Acta 1817:209–217

    CAS  PubMed  Google Scholar 

  • Vass I, Govindjee, (1996) Thermoluminescence from the photosynthetic apparatus. Photosynth Res 48:117–126

    CAS  PubMed  Google Scholar 

  • Vass I, Kirilovsky D, Etienne A-L (1999) UV-B radiation-induced donor- and acceptor-side modifications of photosystem II in the cyanobacterium Synechocystis sp PCC 6803. Biochemistry 38:12786–12794

    CAS  PubMed  Google Scholar 

  • Wei X, Su X, Cao P, Liu X, Chang W, Li M, Zhang X, Liu Z (2016) Structure of spinach photosystem II-LHCII supercomplex at 32 Å resolution. Nature 534:69–74

    CAS  PubMed  Google Scholar 

  • Zavafer A, Campbell DA (2021) Fred Chow: the contributions of a quiet giant of photoinhibition and photoprotection. Funct Plant Biol. https://doi.org/10.1071/FP20337

    Article  PubMed  Google Scholar 

  • Zienkiewicz M, Ferenc A, Wasilewska W, Romanowska E (2012) High light stimulates Deg1-dependent cleavage of the minor LHCII antenna proteins CP26 and CP29 and the PsbS protein in Arabidopsis thaliana. Planta 235:279–288

    CAS  PubMed  Google Scholar 

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Acknowledgements

We gratefully thank Prof. Lijin Tian and Prof. Xuwu Sun for giving us valuable suggestions. This study was supported by the National Key Research and Development Program of China (2020YFA0907602), the Ministry of Agriculture of the People’s Republic of China (2016ZX08009-003–005), and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA24010203, XDB17030100). We gratefully thank the editor and reviewers for their constructive comments and critical advice.

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Wen, X., Yang, Z., Ding, S. et al. Analysis of the changes of electron transfer and heterogeneity of photosystem II in Deg1-reduced Arabidopsis plants. Photosynth Res 150, 159–177 (2021). https://doi.org/10.1007/s11120-021-00842-2

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