Abstract
Although it has been believed that wild-type plants are capable of protecting photosystem I (PSI) under high light, our previous study indicates that PSI is sensitive to high light in the shade-established tree species Psychotria rubra. However, the underlying physiological mechanisms are unclear. In this study, we examined the roles of electron transfer from PSII to PSI and PSI redox state in PSI photoinhibition in P. rubra by treatments with lincomycin (Lin), diuron (DCMU), and methyl viologen (MV). After exposure to 2000 μmol photons m−2 s−1 for 2 h, PSI activity decreased by 35, 29, 3, and 49 % in samples treated with H2O, Lin, DCMU, and MV, respectively. Meanwhile, the MV-treated samples showed higher P700 oxidation ratio than the H2O-treated samples, suggesting the PSI photoinhibition under high light was accompanied by high levels of P700 oxidation ratio. PSI photoinhibition was alleviated in the DCMU-treated samples but was accelerated in the MV-treated samples, suggesting that PSI photoinhibition in P. rubra was mainly controlled by electron transfer from PSII to PSI. Taking together, PSI photoinhibition is more related to electron transfer from PSII to PSI rather than PSI redox state in P. rubra, which is different from the mechanisms of PSI photoinhibition in Arabidopsis thaliana and cucumber.
Similar content being viewed by others
References
Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134
Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Ann Rev Plant Biol 50:601–639
Barber J, Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17:61–66
Barth C, Krause GH (1999) Inhibition of photosystem I and II in chilling-sensitive and chilling-tolerant plants under light and low-temperature stress. Z Naturforsch 54c:645–657
Barth C, Krause GH, Winter K (2001) Responses of photosystem I compared with photosystem II to high-light stress in tropical shade and sun leaves. Plant, Cell Environ 24:163–176
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 99:87–92
Havaux M, Davaud A (1994) Photoinhibition of photosynthesis in chilled potato leaves is not correlated with a loss of photosystem II activity—preferential inactivation of photosystem I. Photosynth Res 40:75–92
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
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
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
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
Huang W, Fu PL, Jiang YJ, Zhang JL, Zhang SB, Hu H, Cao KF (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
Huang W, Zhang SB, Zhang JL, Hu H (2015a) Photoinhibition of photosystem I under high light in the shade-established tropical tree species Psychotria rubra. Front Plant Sci 6:801
Huang W, Yang YJ, Hu H, Zhang SB (2015b) Different roles of cyclic electron flow around photosystem I under sub-saturating and saturating light intensities in tobacco leaves. Front Plant Sci 6:923
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 Biol 73:79–85
Johnson GN (2011) Physiology of PSI cyclic electron transport in higher plants. Biochim Biophys Acta 1807:384–389
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
Klüghammer C, Schreiber U (2008) Saturation pulse method for assessment of energy conversion in PSI. PAM Appl Notes (PAN). 1:11–14
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
Kou J, Takahashi S, Fan DY, Badger MR, Chow WS (2015) Partially dissecting the steady-state electron fluxes in Photosystem I in wild-type and pgr5 and ndh mutants of Arabidopsis. Front Plant Sci 6:758
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
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
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
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
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421
Nishikawa Y, Yamamoto H, Okegawa Y, Wada S, Sato N, Taira Y, Sugimoto K, Makino A, Shikanai T (2012) PGR5-dependent cyclic electron transport around PSI contributes to the redox homeostasis in chloroplasts rather than CO2 fixation and biomass production in rice. Plant Cell Physiol 53:2117–2126
Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35:15–44
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 USA 95:9705–9709
Sonoike K (1995) Selective photoinhibition of photosystem I in isolated thylakoid membranes from cucumber and spinach. Plant Cell Physiol 36:825–830
Sonoike K (1996) Degradation of psaB gene product, the reaction center subunit of photosystem I, is caused during photoinhibition of photosystem I: possible involvement of active oxygen species. Plant Sci 115:157–164
Sonoike K (2006) Photoinhibition and protection of photosystem I. In: Golbeck JH (ed) Photosystem I: the light-driven plastocyanin: ferredoxin oxidoreductase, series advances in photosynthesis and respiration. Springer, Dordrecht, pp 657–668
Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64
Sonoike K, Terashima I, Iwaki M, Itoh S (1995) Destruction of photosystem I iron-sulfur centers in leaves of Cucumis sativus L. by weak illumination at chilling temperatures. FEBS Lett 362:235–238
Sonoike K, Kamo M, Hihara Y, Hiyama T, Enami I (1997) The mechanism of the degradation of psaB gene product, one of the photosynthetic reaction center subunits of photosystem I, upon photoinhibition. Photosynth Res 53:55–63
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
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
Terashima I, Funayama S, Sonoike K (1994) The site of photoinhibition in leaves of Cucumis-sativus L. at low temperatures is photosystem I, not photosystem II. Planta 193:300–306
Tikkanen M, Aro EM (2014) Integrative regulatory network of plant thylakoid energy transduction. Trends Plant Sci 19:10–17
Tikkanen M, Mekala NR, Aro EM (2014) Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage. Biochim Biophys Acta 1837:210–215
Yamori W, Sakata N, Suzuki Y, Shikanai T, Makino 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
Zhang SP, Scheller HV (2004) Photoinhibition of photosystem I at chilling temperature and subsequent recovery in Arabidopsis. Plant Cell Physiol 45:1595–1602
Acknowledgments
This work was supported by National Natural Science Foundation of China (Grant 31300332), China Postdoctoral Science Foundation to Wei Huang (2014T70892), and an open fund from Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences.
Author information
Authors and Affiliations
Corresponding author
Additional information
Wei Huang and Ying-Jie Yang have contributed equally to this study.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Huang, W., Yang, YJ., Zhang, JL. et al. 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 (2016). https://doi.org/10.1007/s11120-016-0275-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-016-0275-5