Adaptive strategies of Zostera japonica photosynthetic electron transport in response to thermal stress

Abstract

Seawater warming is emerging as a result of increasing global temperature. In this study, Zostera japonica (Ascherson and Graebner) collected from the intertidal zones of Changdao (37°N, 120°E) were used to investigate the responses of photosynthetic electron transport to thermal exposure in April 2016. As seawater temperature rose from 20 to 32 °C, increases of the relative variable fluorescence at the K-step to the amplitude of F JF o (W k) and the maximum photochemical efficiency (F v/F m) indicated inhibition of the oxygen-evolving complex (OEC) and photosystem II (PSII) reaction centers, respectively. When exposed to 32 °C for 4 h, both OEC and PSII reaction centers suffered irreversible damage, confirming that 32 °C is the upper critical seawater temperature for Z. japonica photosynthetic electron transport. As a thermal inhibition indicator, PIabs exhibited a time-dependent linear decrease, with irreversible damage of the PSII reaction center occurring once the value of PIabs dropped below 10.60. Based on results of the photosynthetic performance, thermal response strategies were summarized as: (1) an enhancement in the efficiency of the active PSII reaction centers; (2) an increase in the activity of the PSII electron acceptor side; (3) an enhancement in the activities of both PSI and the cyclic electron transport around PSI; (4) the alternation between PSII and PSI. Such adaptive strategies may balance the redox state of electron transport and regulate the distribution of excitation energy between the two photosystems, thereby protecting Z. japonica from ocean warming.

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References

  1. Abe, M., Yokota, K., Kurashima, A., Maegawa, M. (2009a) High water temperature tolerance in photosynthetic activity of Zostera japonica Ascherson & Graebner seedlings from Ago Bay, Mie Prefecture, central Japan. Fish Sci 75(5):1117–1123

  2. Abe, M., Yokota, K., Kurashima, A., Maegawa, M. (2009b) Temperature characteristics in seed germination and growth of Zostera japonica Ascherson & Graebner from Ago Bay, Mie Prefecture, central Japan. Fish Sci 75(4):921–927

  3. Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosyn Res 98(1–3):541–550

    CAS  Article  Google Scholar 

  4. Briantais JM, Dacosta J, Goulas Y, Ducruet JM, Moya I (1996) Heat stress induces in leaves an increase of the minimum level of chlorophyll fluorescence, Fo: a time-resolved analysis. Photosyn Res 48(1–2):189–196

    CAS  Article  Google Scholar 

  5. Bukhov NG, Wiese C, Neimanis S, Heber U (1999) Heat sensitivity of chloroplasts and leaves: leakage of protons from thylakoids and reversible activation of cyclic electron transport. Photosyn Res 59(1):81–93

    CAS  Article  Google Scholar 

  6. Burnap RL (2004) D1 protein processing and Mn cluster assembly in light of the emerging photosystem II structure. Phys Chem Chem Phys 6(20):4803–4809

    CAS  Article  Google Scholar 

  7. Campbell SJ, McKenzie LJ, Kerville SP (2006) Photosynthetic responses of seven tropical seagrasses to elevated seawater temperature. J Exp Mar Biol Ecol 330(2):455–468

    CAS  Article  Google Scholar 

  8. Ceppi MG, Oukarroum A, Çiçek N, Strasser RJ, Schansker G (2012) The IP amplitude of the fluorescence rise OJIP is sensitive to changes in the photosystem I content of leaves: a study on plants exposed to magnesium and sulfate deficiencies, drought stress and salt stress. Physiol Plant 144(3):277–288

    CAS  Article  Google Scholar 

  9. Chen HX, Li WJ, An SZ, Gao HY (2004) Characterization of PSII photochemistry and thermostability in salt-treated Rumex leaves. J Plant Physiol 161(3):257–264

    CAS  Article  Google Scholar 

  10. Duan Y, Zhang M, Gao J, Li P, Goltsev V, Ma F (2015) Thermotolerance of apple tree leaves probed by chlorophyll a fluorescence and modulated 820 nm reflection during seasonal shift. J Photochem Photobiol B 152:347–356

    CAS  Article  Google Scholar 

  11. Duarte CM (2002) The future of seagrass meadows. Environ conserv 29(02):192–206

    Article  Google Scholar 

  12. Egorova EA, Bukhov NG (2002) Effect of elevated temperatures on the activity of alternative pathways of photosynthetic electron transport in intact barley and maize leaves. Russ J Plant Physiol 49(5):575–584

    CAS  Article  Google Scholar 

  13. Enami I, Kamo M, Ohta H, Takahashi S, Miura T, Kusayanagi M, Tanabe S, Kamei A, Motoki A, Hirano M, Tomo T, Satoh K (1998) Intramolecular cross-linking of the extrinsic 33-kDa protein leads to loss of oxygen evolution but not its ability of binding to photosystem II and stabilization of the manganese cluster. J Biol Chem 273(8):4629–4634

    CAS  Article  Google Scholar 

  14. Eullaffroy P, Frankart C, Aziz A, Couderchet M, Blaise C (2009) Energy fluxes and driving forces for photosynthesis in Lemna minor exposed to herbicides. Aquat Bot 90(2):172–178

    CAS  Article  Google Scholar 

  15. Fan DY, Nie Q, Hope AB, Hillier W, Pogson BJ, Chow WS (2007) Quantification of cyclic electron flow around Photosystem I in spinach leaves during photosynthetic induction. Photosynth Res 94(2–3):347–357

    CAS  Article  Google Scholar 

  16. Fan DY, Fitzpatrick D, Oguchi R, Ma W, Kou J, Chow WS (2016). Obstacles in the quantification of the cyclic electron flux around Photosystem I in leaves of C3 plants. Photosynth Res, 1–13

  17. Gao J, Li P, Ma F, Goltsev V (2014) Photosynthetic performance during leaf expansion in Malus micromalus probed by chlorophyll a fluorescence and modulated 820 nm reflection. J Photochem Photobiol B 137:144–150

    CAS  Article  Google Scholar 

  18. Gao F, Zhao J, Wang X, Qin S, Wei L, Ma W (2016) NdhV is a subunit of NADPH dehydrogenase essential for cyclic electron transport in Synechocystis sp. strain PCC 6803. Plant Physiol 170(2):752–760

    CAS  Article  Google Scholar 

  19. Goltsev V, Zaharieva I, Chernev P, Strasser RJ (2009) Delayed fluorescence in photosynthesis. Photosynth Res 101(2–3):217–232

    CAS  Article  Google Scholar 

  20. Hall TD, Chastain DR, Horn PJ, Chapman KD, Choinski JS (2014) Changes during leaf expansion of ΦPSII temperature optima in Gossypium hirsutum are associated with the degree of fatty acid lipid saturation. J Plant Physiol 171(6):411–420

    CAS  Article  Google Scholar 

  21. Havaux M, Tardy F (1996) Temperature-dependent adjustment of the thermal stability of photosystem II in vivo: possible involvement of xanthophyll-cycle pigments. Planta 198(3):324–333

    CAS  Article  Google Scholar 

  22. Holmer M, Wirachwong P, Thomsen MS (2011) Negative effects of stress-resistant drift algae and high temperature on a small ephemeral seagrass species. Mar Biol 158(2):297–309

    Article  Google Scholar 

  23. Joliot P, Johnson GN (2011) Regulation of cyclic and linear electron flow in higher plants. P Natl Acad Sci USA 108(32):13317–13322

    CAS  Article  Google Scholar 

  24. Joliot P, Joliot A, Johnson G (2006). Cyclic electron transfer around photosystem I. In Photosystem I. Springer, The Netherlands, pp 639–656

    Google Scholar 

  25. Kaldy JE, Shafer DJ, Magoun AD (2015) Duration of temperature exposure controls growth of Zostera japonica: implications for zonation and colonization. J Exp Mar Biol Ecol 464:68–74

    Article  Google Scholar 

  26. Lee HY, Hong YN, Chow WS (2001) Photoinactivation of photosystem II complexes and photoprotection by non-functional neighbours in Capsicum annuum L. leaves. Planta 212(3):332–342

    CAS  Article  Google Scholar 

  27. Lee SY, Oh JH, Choi CI, Suh Y, Mukai H (2005) Leaf growth and population dynamics of intertidal Zostera japonica on the western coast of Korea. Aquat Bot 83(4):263–280

    Article  Google Scholar 

  28. Li XM, Zhang QS, Tang YZ, Yu YQ, Liu HL, Li LX (2014) Highly efficient photoprotective responses to high light stress in Sargassum thunbergii germlings, a representative brown macroalga of intertidal zone. J Sea Res 85:491–498

    Article  Google Scholar 

  29. Morita T, Miyamatsu A, Fujii M, Kokubu H, Abe M, Kurashima A, Maegawa M (2011) Germination in Zostera japonica is determined by cold stratification, tidal elevation and sediment type. Aquat Bot 95(3):234–241

    Article  Google Scholar 

  30. Orth RJ, Carruthers, T. J. B., Dennison WC, Duarte CM, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy JW, Olyarnik S, Short FT, Waycott M, Williams SL (2006) A global crisis for seagrass ecosystems. Bioscience 56(12):987–996

    Article  Google Scholar 

  31. Oukarroum A, Goltsev V, Strasser RJ (2013) Temperature effects on pea plants probed by simultaneous measurements of the kinetics of prompt fluorescence, delayed fluorescence and modulated 820 nm reflection. PloS One 8(3):e59433

    CAS  Article  Google Scholar 

  32. Perron MC, Juneau P (2011) Effect of endocrine disrupters on photosystem II energy fluxes of green algae and cyanobacteria. Environ Res 111(4):520–529

    CAS  Article  Google Scholar 

  33. Pettai H, Oja V, Freiberg A, Laisk A (2005) The long-wavelength limit of plant photosynthesis. Febs Lett 579(18):4017–4019

    CAS  Article  Google Scholar 

  34. Quiles MJ (2006) Stimulation of chlororespiration by heat and high light intensity in oat plants. Plant Cell Environ 29(8):1463–1470

    CAS  Article  Google Scholar 

  35. Ralph PJ, Polk SM, Moore KA, Orth RJ, Smith WO (2002) Operation of the xanthophyll cycle in the seagrass Zostera marina in response to variable irradiance. J Exp Mar Biol Ecol 271(2):189–207

    CAS  Article  Google Scholar 

  36. Salvatori E, Fusaro L, Gottardini E, Pollastrini M, Goltsev V, Strasser RJ, Bussotti F (2014) Plant stress analysis: application of prompt, delayed chlorophyll fluorescence and 820 nm modulated reflectance. Insights from independent experiments. Plant Physiol Bioch 85:105–113

    CAS  Article  Google Scholar 

  37. Schansker G, Srivastava A, Strasser RJ (2003) Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Funct Plant Biol 30(7):785–796

    CAS  Article  Google Scholar 

  38. Shafer DJ, Kaldy JE, Gaeckle JL (2014) Science and management of the introduced seagrass Zostera japonica in North America. Environ Manage 53(1):147–162

    Article  Google Scholar 

  39. Sharkey TD, Zhang R (2010) High temperature effects on electron and proton circuits of photosynthesis. J Integr Plant Biol 52(8):712–722

    CAS  Article  Google Scholar 

  40. Shi Y, Fan H, Cui X, Pan L, Li S, Song X (2010) Overview on seagrasses and related research in China. Chin J Oceanol Limnol 28:329–339

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  42. Stirbet, Govindjee A (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B 104(1):236–257

    CAS  Article  Google Scholar 

  43. Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In Chlorophyll a Fluorescence. Springer, The Netherlands, pp 321–362

    Book  Google Scholar 

  44. 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(6):1313–1326

    CAS  Article  Google Scholar 

  45. Tóth SZ, Nagy V, Puthur JT, Kovács L, Garab G (2011) The physiological role of ascorbate as photosystem II electron donor: protection against photoinactivation in heat-stressed leaves. Plant Physiol 156(1):382–392

    Article  Google Scholar 

  46. Waycott M, Duarte CM, Carruthers TJ, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean JW, Heck KL, Hughs RA, Kendrick GA, Kenworthy JW, Short FT, Williams SL (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Natl Acad Sci 106(30):12377–12381

    CAS  Article  Google Scholar 

  47. 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

    CAS  Article  Google Scholar 

  48. Yoshioka M, Uchida S, Mori H, Komayama K, Ohira S, Morita N, Yamamoto Y (2006) Quality control of photosystem II cleavage of reaction center D1 protein in spinach thylakoids by FtsH protease under moderate heat stress. J Biol Chem 281(31):21660–21669

    CAS  Article  Google Scholar 

  49. Zhang R, Sharkey TD (2009) Photosynthetic electron transport and proton flux under moderate heat stress. Photosynth Res 100(1):29–43

    CAS  Article  Google Scholar 

  50. Zhang Z, Jia Y, Gao H, Zhang L, Li H, Meng Q (2011) Characterization of PSI recovery after chilling-induced photoinhibition in cucumber (Cucumis sativus L.) leaves. Planta 234(5):883–889

    CAS  Article  Google Scholar 

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Acknowledgements

This study was financially supported by the National Natural Science Foundation of China (No. 41376154).

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Correspondence to Quan Sheng Zhang.

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Zhang, D., Zhang, Q.S. & Yang, X.Q. Adaptive strategies of Zostera japonica photosynthetic electron transport in response to thermal stress. Mar Biol 164, 35 (2017). https://doi.org/10.1007/s00227-016-3064-y

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Keywords

  • Seawater Temperature
  • Photosynthetic Electron Transport
  • Thermal Exposure
  • PSII Reaction Center
  • Acceptor Side