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Journal of Plant Research

, Volume 128, Issue 2, pp 307–315 | Cite as

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

  • Wei HuangEmail author
  • Shi-Bao Zhang
  • Hong Hu
Regular Paper

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.

Keywords

High mountain plants Cyclic electron flow Oxygen-evolving complex Photoprotection Photosystem II 

Notes

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.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 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 50:601–639CrossRefGoogle Scholar
  2. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396CrossRefPubMedCentralPubMedGoogle Scholar
  3. 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 627–648Google Scholar
  4. Dasgupta J, Ananyev GM, Dismukes GC (2008) Photoassembly of the water-oxidizing complex in photosystem II. Coord Chem Rev 252:347–360CrossRefPubMedCentralPubMedGoogle Scholar
  5. 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 161:1211–1224CrossRefPubMedGoogle Scholar
  6. Ettinger WF, Clear AM, Fanning KJ, Peck ML (1999) Identification of a Ca2+/H+ antiport in the plant chloroplast thylakoid membrane. Plant Physiol 119:1379–1385CrossRefPubMedCentralPubMedGoogle Scholar
  7. 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 990:87–92CrossRefGoogle Scholar
  8. 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 1706:68–80CrossRefPubMedGoogle Scholar
  9. Hendrickson L, Furbank RT, Chow WS (2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynth Res 82:73–81CrossRefPubMedGoogle Scholar
  10. 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 51:1922–1928CrossRefPubMedGoogle Scholar
  11. 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 103:175–182CrossRefPubMedGoogle Scholar
  12. 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 235:819–828CrossRefPubMedGoogle Scholar
  13. 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 33:211–220CrossRefPubMedGoogle Scholar
  14. Johnson GN (2011) Physiology of PSI cyclic electron transport in higher plants. Biochim Biophys Acta 1807:384–389CrossRefPubMedGoogle Scholar
  15. 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 192:261–268CrossRefGoogle Scholar
  16. Klüghammer C, Schreiber U (2008) Saturation pulse method for assessment of energy conversion in PSI. PAM Appl Notes (PAN) 1:11–14Google Scholar
  17. 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 40:1018–1028CrossRefGoogle Scholar
  18. 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 79:209–218CrossRefPubMedGoogle Scholar
  19. Krieger A, Weis E (1993) The role of calcium in the pH-dependent control of Photosystem II. Photosynth Res 37:117–130CrossRefPubMedGoogle Scholar
  20. 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 36:1296–1310CrossRefGoogle Scholar
  21. 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 99:15222–15227CrossRefPubMedCentralPubMedGoogle Scholar
  22. 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 166:1607–1615CrossRefPubMedGoogle Scholar
  23. Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Ann Rev Plant Physiol Plant Mol Biol 45:633–662CrossRefGoogle Scholar
  24. Miller AF, Brudvig GW (1989) Manganese and calcium requirements for reconstitution of oxygen-evolution activity in manganese-depleted photosystem II membranes. Biochemistry 28:8181–8190CrossRefPubMedGoogle Scholar
  25. 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 110:361–371CrossRefPubMedGoogle Scholar
  26. 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 429:579–582CrossRefPubMedGoogle Scholar
  27. 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 1767:1252–1259CrossRefPubMedGoogle Scholar
  28. 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 20:5587–5594CrossRefPubMedCentralPubMedGoogle Scholar
  29. Niyogi KK, BjoÈrkman O, Grossman AR (1997) Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell 9:1369–1380CrossRefPubMedCentralPubMedGoogle Scholar
  30. 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 10:1121–1134CrossRefPubMedCentralPubMedGoogle Scholar
  31. 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 67:139–145CrossRefPubMedGoogle Scholar
  32. 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 850:310–318CrossRefGoogle Scholar
  33. 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 44:8494–8499CrossRefPubMedGoogle Scholar
  34. 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 49:825–834CrossRefPubMedGoogle Scholar
  35. Peltier G, Cournac L (2002) Chlororespiration. Annu Rev Plant Biol 53:523–550CrossRefPubMedGoogle Scholar
  36. 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 95:9705–9709CrossRefPubMedCentralPubMedGoogle Scholar
  37. Strasser BJ (1997) Donor side capacity of photosystem II probed by chlorophyll a fluorescence transients. Photosynth Res 52:147–155CrossRefGoogle Scholar
  38. 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 445–483Google Scholar
  39. 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 1–47Google Scholar
  40. 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 28:1123–1135CrossRefGoogle Scholar
  41. 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 24:2934–2948CrossRefPubMedCentralPubMedGoogle Scholar
  42. Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trend Plant Sci 13:178–182CrossRefGoogle Scholar
  43. 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 144:487–494CrossRefPubMedCentralPubMedGoogle Scholar
  44. Takahashi S, Milward SE, Fan DY, Chow WS, Badger MR (2009) How does cyclic electron flow alleviate photoinhibition in Arabidopsis? Plant Physiol 149:1560–1567CrossRefPubMedCentralPubMedGoogle Scholar
  45. Takahashi S, Milward SE, Yamori W, Evans JR, Hillier W, Badger MR (2010) The solar action spectrum of photosystem II damage. Plant Physiol 153:988–993CrossRefPubMedCentralPubMedGoogle Scholar
  46. 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 141:465–474CrossRefPubMedCentralPubMedGoogle Scholar
  47. 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 68:966–976CrossRefPubMedGoogle Scholar
  48. 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 29:217–228CrossRefPubMedGoogle Scholar
  49. 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 149:141–150CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2015

Authors and Affiliations

  1. 1.Kunming Institute of BotanyChinese Academy of SciencesKunmingChina

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