Abstract
Resurrection plants could survive severe drought stress, but the underlying mechanism for protecting their photosynthetic apparatus against drought stress is unclear. Cyclic electron flow (CEF) has been documented as a crucial mechanism for photoprotection in Arabidopsis and tobacco. We hypothesized that CEF plays an important role in protecting photosystem I (PSI) and photosystem II (PSII) against drought stress for resurrection plants. To address this hypothesis, the effects of mild drought stress on light energy distribution in PSII and P700 redox state were examined in a resurrection plant Paraboea rufescens. Cyclic electron flow was not activated below the photosynthetic photon flux density (PPFD) of 400 μmol m−2 s−1 in leaves without drought stress. However, CEF was activated under low light in leaves with mild drought stress, and the effective quantum yield of PSII significantly decreased. Meanwhile, non-photochemical quenching (NPQ) was significantly stimulated not only under high light but also under low light. Compared with the control, the fraction of overall P700 that cannot be oxidized in a given state (PSI acceptor side limitation) under high light was maintained at low level of 0.1 in leaves with water deficit, indicating that the over-reduction of the PSI acceptor side was prevented by the significant stimulation of CEF. Furthermore, methyl viologen could significantly increase the PSII photo-inhibition induced by high light compared with chloramphenicol. These results suggested that CEF is an important mechanism for protecting PSI and PSII from drought stress in resurrection plants.
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Abbreviations
- CEF:
-
Cyclic electron flow
- LEF:
-
Linear electron flow
- MV:
-
Methyl viologen
- NPQ:
-
Non-photochemical quenching
- PPFD:
-
Photosynthetic photon flux density
- PS:
-
Photosystem
- ROS:
-
Reactive oxygen species
- Y(I):
-
Effective quantum yield of photosystem I
- Y(II):
-
Effective quantum yield of photosystem II
- Y(NA):
-
Fraction of over P700 that cannot be oxidized in a given state
- Y(ND):
-
Fraction of over P700 that is oxidized in a given state
- Y(NO):
-
Fraction of energy that is passively dissipated in form of heat and fluorescence
- Y(NPQ):
-
Fraction of energy dissipated in form of heat via the regulated non-photochemical quenching mechanism
- Ψleaf :
-
Leaf water potential
References
Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098:275–335
Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639
Burrows PA, Sazanov LA, Svab Z, Maliga P, Nixon PJ (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J 17:868–876
Busch F, Hunter NPA, Ensminger I (2009) Biochemical constrains limit the potential of the photochemical reflectance index as a predictor of effective quantum efficiency of photosynthesis during the winter spring transition in Jack pine seedlings. Funct Plant Biol 36:1016–1026
Chen LS, Cheng L (2003) Both xanthophyll cycle-dependent thermal dissipation and the antioxidant system are up-regulated in grape (Vitis labrusca L. cv. Concord) leaves in response to N limitation. J Exp Bot 54:2165–2175
Chow WS, Aro EM (2005) Photo-inactivation 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
Chow WS, Hope AB (2004) Electron fluxes through photosystem I in cucumber leaf discs probed by far-red light. Photosynth Res 81:77–89
Cooper K, Farrent JM (2002) Recovery of the resurrection plant Craterostigma wilmsii from desiccation: protection versus repair. J Exp Bot 53(375):1805–1813
Cornic G (1994) Drought stress and high light effects on leaf photosynthesis. In: Baker NR (ed) Photoinhibition of photosynthesis: from molecular mechanisms to the field. BIOS, Oxford, pp 297–313
Deng X, Hu Z-A, Wang H-X, Wen X-G, Kuang T-Y (2003) A comparison of photosynthetic apparatus of the detached leaves of the resurrection plant Boea hygrometrica with its non-tolerant relative Chirita heterotrichia in response to dehydration and rehydration. Plant Sci 165(4):851–861
Eickmeier WG (1979) Photosynthetic recovery in the resurrection plant Selaginella lepidophylla after wetting. Oecologia 39:93–106
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
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 94:347–357
Finazzi G, Furia A, Barbagallo RP, Forti G (1999) State transitions, cyclic and linear electron flow transport and photophosphorylation in Chlamydomonas reinhardtii. Biochim Biophys Acta 1413:117–129
Finazzi G, Rappaport F, Furia A, Fleischmann M, Rochaix JD, Zito F, Forti G (2002) Involvement of state transitions in the switch between between linear and cyclic electron flow in Chlamydomonas reinhardtii. EMBO Rep 3:280–285
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
Golding AJ, Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218:107–114
Hakala M, Tuominen I, Keränen M, Tyystjärvi T, Tyystjärvi E (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochim Biophys Acta 1706:68–80
Haldrup A, Jensen PE, Lunde C, Scheller HV (2001) Balance of power: a review of the mechanism of photosynthetic state transitions. Trends Plant Sci 6:301–305
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
Horvath EM, Peter SO, Joet T, Rumeau D, Cournac L, Horvath GV, Kavanagh TA, Schafer C, Peltier G, Medgyesy P (2000) Targeted inactivation of the plastid ndhB gene in tobacco results in an enhanced sensitivity of photosynthesis to moderate stomatal closure. Plant Physiol 123:1337–1349
Huang W, Zhang SB, Cao KF (2011) Cyclic electron flow plays an important role in photoprotection of tropical trees illuminated at temporal chilling temperature. Plant Cell Physiol 52:297–305
Jia H, Oguchi R, Hope AB, Barber J, Chow WS (2008) Differential effects of severe water stress on linear and cyclic electron fluxes through Photosystem I in spinach leaf discs in CO2-enriched air. Planta 228:803–812
Klughammer 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
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
Krieger-Liszkay A, Fufezan C, Trebst A (2008) Single oxygen production in photosystem II and related protection mechanism. Photosynth Res 98:551–564
Lehtimaki N, Lintala M, Allahverdiyeva Y, Aro EM, Mulo P (2010) Drought stress-induced upregulation of components involved in ferredoxin-dependent cyclic electron transfer. J Plant Physiol 167:1018–1022
Miyake C, Shinzaki Y, Miyata M, Tomizawa K (2004) Enhancement of cyclic electron flow around PSI at high light and its contribution to the induction of non-photochemical quenching of chl fluorescence in intact leaves of tobacco plants. Plant Cell Physiol 45:1426–1433
Miyake C, Miyata M, Shinzaki Y, Tomizawa K (2005) CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves: relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of chl fluorescence. Plant Cell Physiol 46:629–737
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
Munekage Y, Genty B, Peltier G (2008) Effect of PGR5 impairment on photosynthesis and growth in Arabidopsis thaliana. Plant Cell Physiol 49:1688–1698
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
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
Nishiyama Y, Allakhverdiev SI, Murata N (2005) Inhibition of the repair of photosystem II by oxidative stress in cyanobacteria. Photosynth Res 84:1–7
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
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
Ortiz-Lopez A, Ort DR, Boyer JS (1991) Photophosphorylation in attached leaves of Helianthus annuus at low water potentials. Plant Physiol 96:1018–1025
Osmond CB (1981) Photorespiration and photoinhibition. Some implications for the energetics of photosynthesis. Biochim Biophys Acta 639:77–98
Oxborough K, Baker NR (1997) Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components–calculation of qP and Fv′/Fm′ without measuring Fo’. Photosynth Res 54:135–142
Rochaix JD (2007) Role of thylakoid protein kinases in photosynthetic acclimation. FEBS Lett 581:2768–2775
Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ 30:1041–1051
Sarvikas P, Hakala M, Pätsikkä E, Tyystjärvi T, Tyystjärvi E (2006) Action spectrum of photoinhibition in leaves of wild type and npq1–2 and npq4–1 mutants of Arabidopsis thaliana. Plant Cell Physiol 47:391–400
Smirnoff N (1993) The role of active oxygen in response of plants to water deficit and desiccation. New Phytol 125:27–58
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, 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
Sun Z-L, Lee H-Y, Matsubara S, Hope AB, Pogson BJ, Hong Y-N, Chow WS (2006) Photoprotection of residual functional photosystem II units that survive illumination in the absence of repair, and their critical role in subsequent recovery. Physiol Plant 128:415–424
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
Tyystjärvi E (2008) Photoinhibition of photosystem II and photodamage of the oxygen evolving manganese cluster. Coord Chem Rev 252:361–376
Tyystjärvi E, Hakala M, Sarvikas P (2005) Mathematical modelling of the light response curve of photoinhibition of photosystem II. Photosynth Res 84:21–27
Vass I (2011) Role of charge recombination processes in photodamage and photoprotection of the photosystem II complex. Physiol Plant 142:6–16
Vener AV, von Kan PJM, Rich PR, Ohad I, Andersson B (1997) Plastoquinol at the quinol oxidation site of reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: Thylakoid protein kinase deactivation by a single-turnover flash. Proc Natl Acad Sci USA 94:1585–1590
von Caemmerer S (2000) Biochemical models of leaf photosynthesis. CSIRO Publishing, Collingwood
Wollman FA (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J 20:3623–3630
Zhang SP, Scheller HV (2004) Photoinhibition of photosystem I at chilling temperature and subsequent recovery in Arabidopsis. Plant Cell Physiol 45:1595–1602
Zhang JL, Meng LZ, Cao KF (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
Zito F, Finazzi G, Delosme R, Nitschke W, Picot D, Wollman FA (1999) The Qo site of cytochrome b 6 f complexes controls the activation of the LHCII kinase. EMBO J 18:2961–2969
Acknowledgments
Xishuangbanna Station for Tropical Rain Forest Ecosystem Studies (XSTRE) provided climatic data. This work was supported by National Natural Science Foundation of China (Grant 30900174 and 30770226) and the Key Laboratory of National Forestry Bureau for Fast-growing Tree Breeding and Cultivation in Central South China (an open project grant).
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Huang, W., Yang, SJ., Zhang, SB. et al. Cyclic electron flow plays an important role in photoprotection for the resurrection plant Paraboea rufescens under drought stress. Planta 235, 819–828 (2012). https://doi.org/10.1007/s00425-011-1544-3
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DOI: https://doi.org/10.1007/s00425-011-1544-3