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Insusceptibility of oxygen-evolving complex to high light in Betula platyphylla

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Abstract

High mountain plants growing at high altitude have to regularly cope with high light and high UV radiation that can lead to photodamage of oxygen-evolving complex (OEC). However, the underlying mechanism of photoprotection for OEC in high mountain plants is unclear. Sun leaves of Betula platyphylla were used to examine whether cyclic electron flow (CEF) around photosystem I (PSI) plays an important role in photoprotection for OEC. Our results indicated that the value of ETRI/ETRII ratio significantly increased under high light. With increasing light intensity, non-photochemical quenching (NPQ) gradually increased, and the fraction of P700 that is oxidized in a given state gradually increased. These results indicated that CEF was significantly activated under high light. After treatment with a high light of 1600 μmol photons m−2 s−1 for 8 h, the OEC activity did not decline, but the maximum quantum yield of PSII (F v /F m ) ratio significantly decreased. These results suggested that CEF-dependent generation of proton gradient across thylakoid membrane protected OEC activity against high light. Furthermore, the stability of PSI activity during exposure to high light suggested that the high CEF activity in B. platyphylla played an important role in photoprotection for PSI activity.

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References

  • Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Ann Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  CAS  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chow WS, Aro EM (2005) Photoinactivation and mechanisms of recovery. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light-driven water: plastoquinone oxidoreductase advances in photosynthesis and respiration. Springer, Dordrecht, pp 627–648

    Google Scholar 

  • Dasgupta J, Ananyev GM, Dismukes GC (2008) Photoassembly of the water-oxidizing complex in photosystem II. Coord Chem Rev 252:347–360

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • De Ronde JA, Cress WA, Kruger GHJ, Strasser RJ, Van Staden J (2004) Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene, during heat and drought stress. J Plant Physiol 161:1211–1224

    Article  PubMed  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  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hakala M, Tuominen I, Keranen M, Tyystjarvi T, Tyystjarvi E (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochim Biophys Acta 1706:68–80

    Article  CAS  PubMed  Google Scholar 

  • Hendrickson L, Furbank RT, Chow WS (2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynth Res 82:73–81

    Article  CAS  PubMed  Google Scholar 

  • Huang W, Zhang S-B, Cao K-F (2010a) Stimulation of cyclic electron flow during recovery after chilling-induced photoinhibition of PSII. Plant Cell Physiol 51:1922–1928

    Article  CAS  PubMed  Google Scholar 

  • Huang W, Zhang S-B, Cao K-F (2010b) 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  PubMed  Google Scholar 

  • Huang W, Yang S-J, Zhang S-B, Zhang J-L, Cao K-F (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  PubMed  Google Scholar 

  • Huang W, Fu P-L, Jiang Y-J, Zhang J-L, Zhang S-B, Hu H, Cao K-F (2013) Differences in the responses of photosystem I and photosystem II of three tree species Cleistanthus sumatranus, Celtis philippensis and Pistacia weinmannifolia submitted to a prolonged drought in a tropical limestone forest. Tree Physiol 33:211–220

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  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 

  • Kou JC, 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, 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

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Laureau C, De Paepe R, Latouche G, Moreno-Chacon M, Finazzi G, Kunz M, Cornic G, Streb P (2013) Plastid terminal oxidase (PTOX) has the potential to act as a safety valve for excess excitation energy in the alpine plant species Ranunculus glacialis L. Plant Cell Environ 36:1296–1310

    Article  CAS  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li P-M, Cheng L-L, Gao H-Y, Jiang C-D, Peng T (2009) Heterogeneous behavior of PSII in soybean (Glycine max) leaves with identical PSII photochemistry efficiency under different high temperature treatments. J Plant Physiol 166:1607–1615

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Miller AF, Brudvig GW (1989) Manganese and calcium requirements for reconstitution of oxygen-evolution activity in manganese-depleted photosystem II membranes. Biochemistry 28:8181–8190

    Article  CAS  PubMed  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  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

    Article  CAS  PubMed  Google Scholar 

  • Nandha B, Finazzi G, Joliot P, Hald S, Johnson GN (2007) The role of PGR5 in the redox poising of photosynthetic electron transport. Biochim Biophys Acta 1767:1252–1259

    Article  CAS  PubMed  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  PubMed Central  CAS  PubMed  Google Scholar 

  • Niyogi KK, BjoÈrkman O, Grossman AR (1997) Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell 9:1369–1380

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Niyogi KK, Grossman AR, Bjorkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in regulation of photosynthetic energy conversion. Plant Cell 10:1121–1134

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Niyogi KK, Shih C, Chow WS, Pogson BJ, DellaPenna D, Bjorkman O (2001) Photoprotection in a zeaxanthin and lutein deficient double mutant of Arabidopsis. Photosynth Res 67:139–145

    Article  CAS  PubMed  Google Scholar 

  • Nuijs AM, Shuvalov A, van Gorkom HJ, Plijter JJ, Duysens LNM (1986) Picosecond absorbance difference spectroscopy on the primary reactions and the antenna-excited states in photosystem I particles. Biochim Biophys Acta 850:310–318

    Article  CAS  Google Scholar 

  • Ohnishi N, Allakhverdiev SI, Takahashi S, Higashi S, Watanabe M, Nishiyama Y, Murata N (2005) Two-step mechanism of photodamage to photosystem II: step one occurs at the oxygen-evolving complex and step two occurs at the photochemical reaction center. Biochemistry 44:8494–8499

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Peltier G, Cournac L (2002) Chlororespiration. Annu Rev Plant Biol 53:523–550

    Article  CAS  PubMed  Google Scholar 

  • Shikanai T, Endo T, Hashimoto T, Yamada Y, Asada K, Yokota A (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc Natl Acad Sci 95:9705–9709

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Strasser BJ (1997) Donor side capacity of photosystem II probed by chlorophyll a fluorescence transients. Photosynth Res 52:147–155

    Article  CAS  Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing Photosynthesis: Mechanism, Regulation and Adaptation, chapter 25. Taylor and Francis Press, London, pp 445–483

    Google Scholar 

  • Strasser RJ, Tsimill-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou G, Govindjee (eds) Advances in Photosynthesis and Respiration, chapter 12. KAP Press, Netherlands, pp 1–47

  • Streb P, Josse E-M, Gallouët E, Baptist F, Kuntz M, Cornic G (2005) Evidence for alternative electron sinks to photosynthetic carbon assimilation in the high mountain plant species Ranunculus glacialis. Plant Cell Environ 28:1123–1135

    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  PubMed Central  CAS  PubMed  Google Scholar 

  • Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trend Plant Sci 13:178–182

    Article  CAS  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  PubMed Central  CAS  PubMed  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  PubMed Central  CAS  PubMed  Google Scholar 

  • Takahashi S, Milward SE, Yamori W, Evans JR, Hillier W, Badger MR (2010) The solar action spectrum of photosystem II damage. Plant Physiol 153:988–993

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang P, Duan W, Takabayashi A, Endo T, Shikanai T, Ye JY, Mi HL (2006) Chloroplastic NAD(P)H dehydrogenase in tobacco leaves functions in alleviation of oxidative damage caused by temperature stress. Plant Physiol 141:465–474

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yamori W, Sakata N, Suzuki Y, Shikanai T, Maniko A (2011) Cyclic electron flow around photosystem I via chloroplast NAD(P)H dehydrogenase (NDH) complex performs a significant physiological role during photosynthesis and plant growth at low temperature in rice. Plant J 68:966–976

    Article  CAS  PubMed  Google Scholar 

  • Zhang J-L, Meng L-Z, Cao K-F (2009) Sustained diurnal photosynthetic depression in uppermost-canopy leaves of four dipterocarp species in the rainy and dry seasons: does photorespiration play a role in photoprotection? Tree Physiol 29:217–228

    Article  PubMed  Google Scholar 

  • Zhang W, Huang W, Yang Q-Y, Zhang S-B, Hu H (2013) Effect of growth temperature on the electron flow for photorespiration in leaves of tobacco grown in the field. Physiol Plant 149:141–150

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study is supported by China Postdoctoral Science Foundation to Wei Huang (2013M531994) and National Natural Science Foundation of China (grant 31300332). We are grateful to Ying-Jie Yang and Wei Zhang for critical reading of the manuscript.

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The authors declare that they have no conflict of interest.

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Correspondence to Wei Huang.

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Huang, W., Zhang, SB. & Hu, H. Insusceptibility of oxygen-evolving complex to high light in Betula platyphylla . J Plant Res 128, 307–315 (2015). https://doi.org/10.1007/s10265-014-0684-5

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