Abstract
The photosynthetic responses of wheat (Triticum aestivum L.) leaves to different levels of drought stress were analyzed in potted plants cultivated in growth chamber under moderate light. Low-to-medium drought stress was induced by limiting irrigation, maintaining 20 % of soil water holding capacity for 14 days followed by 3 days without water supply to induce severe stress. Measurements of CO2 exchange and photosystem II (PSII) yield (by chlorophyll fluorescence) were followed by simultaneous measurements of yield of PSI (by P700 absorbance changes) and that of PSII. Drought stress gradually decreased PSII electron transport, but the capacity for nonphotochemical quenching increased more slowly until there was a large decrease in leaf relative water content (where the photosynthetic rate had decreased by half or more). We identified a substantial part of PSII electron transport, which was not used by carbon assimilation or by photorespiration, which clearly indicates activities of alternative electron sinks. Decreasing the fraction of light absorbed by PSII and increasing the fraction absorbed by PSI with increasing drought stress (rather than assuming equal absorption by the two photosystems) support a proposed function of PSI cyclic electron flow to generate a proton-motive force to activate nonphotochemical dissipation of energy, and it is consistent with the observed accumulation of oxidized P700 which causes a decrease in PSI electron acceptors. Our results support the roles of alternative electron sinks (either from PSII or PSI) and cyclic electron flow in photoprotection of PSII and PSI in drought stress conditions. In future studies on plant stress, analyses of the partitioning of absorbed energy between photosystems are needed for interpreting flux through linear electron flow, PSI cyclic electron flow, along with alternative electron sinks.
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Abbreviations
- \( A_{{{\text{CO}}_{ 2} }} \) :
-
CO2 assimilation rate
- Cyt b6/f :
-
Cytochrome b6/f
- g m :
-
Mesophyll conductance
- g s :
-
Stomatal conductance
- LED:
-
Light emitting diode
- LHC:
-
Light harvesting complex
- NPQ:
-
Nonphotochemical quenching
- P700:
-
Primary electron donor of PSI (reduced form)
- P700+ :
-
Primary electron donor of PSI (oxidized form)
- PAR:
-
Photosynthetic active radiation
- PQ:
-
Plastoquinone
- PSI:
-
Photosystem I
- PSII:
-
Photosystem II
- Q A :
-
Primary PSII acceptor
- qE:
-
pH-dependent energy dissipation
- RuBP:
-
Ribulose 1,5-bisphosphate
- RWC:
-
Relative water content
- ΔpH:
-
Transthylakoid pH gradient
- Ψ W :
-
Water potential
References
Aluru MR, Rodermel SR (2004) Control of chloroplast redox by the IMMUTANS terminal oxidase. Physiol Plant 120:4–11
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
Bailey S, Walters RG, Jansson S, Horton P (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213:794–801
Balaguer L, Punaire FI, Martínez-Ferri E, Armas C, Valladares F, Manrique E (2002) Ecophysiological significance of chlorophyll loss and reduced photochemical efficiency under extreme aridity in Stipa tenacissima L. Plant Soil 240:343–352
Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25:173–185
Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plant of diverse origins. Planta 170:489–504
Björkman O, Powles SB (1984) Inhibition of photosynthetic reactions under water stress: interaction with light level. Planta 161:490–504
Bonjean AP, Angus WJ (2001) The world wheat book—a history of wheat breeding. Lavoisier Publishing, Paris
Brestic M, Cornic G, Fryer MJ, Baker NR (1995) Does photorespiration protect the photosynthetic apparatus in French bean leaves from photoinhibition during drought stress? Planta 196:450–457
Brestic M, Zivcak M, Olsovska K, Repkova J (2008) Functional study of PS II and PSI energy use and dissipation mechanisms in barley wild type and chlorina mutants under high light conditions. In: Allen JF, Gantt E, Goldbeck JH, Osmond B (eds) Photosynthesis. Energy from the sun: 14th International congress on photosynthesis, Springer, Dordrecht, pp 1407–1411
Brestic M, Zivcak M, Kalaji HM, Allakhverdiev SI, Carpentier R (2012) Photosystem II thermostability in situ: environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L. Plant Physiol Biochem 57:93–105
Buermann W, Lintner BR, Koven CD, Angert A, Pinzon JE, Tucker CJ et al (2007) The changing carbon cycle at Mauna Loa Observatory. Proc Natl Acad Sci USA 104:4249–4254
Cardol P, Bailleul B, Rappaport F, Derelle E, Béal D, Breyton C, Bailey S, Wollman FA, Grossman A, Moreau H, Finazzi G (2008) An original adaptation of photosynthesis in the marine green alga Ostreococcus. Proc Natl Acad Sci USA 105:7881–7886
Chaves MM (1991) Effects of water deficits on carbon assimilation. J Exp Bot 42:1–16
Chaves MM, Oliveira MM (2004) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. J Exp Bot 55:2365–2384
Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CP, Osorio ML, Carvalho I, Faria T, Pinheiro C (2002) How plants cope with water stress in the field. Photosynthesis and growth. Ann Bot 89:907–916
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560
Chen YE, Zhang ZI, Zhang HY, Zeng YX, Yuan S (2013) The significance of CP29 reversible phosphorylation in thylakoids of higher plants under environmental stresses. J Exp Bot 64:1167–1178
Ciais P, Reichstein M, Viovy N, Granier A, Ogee J, Allard V et al (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437:529–533
Clarke JE, Johnson GN (2001) In vivo temperature dependence of cyclic and pseudocyclic electron transport in barley. Planta 212:808–816
Cornic G, Massacci A (1996) Leaf photosynthesis under drought stress. In: Baker NR (ed) Photosynthesis and the environment. Kluwer Academic Publishers, Dordrecht
Cournac L, Redding K, Ravenel J, Rumeau D, Josse E-M, Kuntz M, Peltier G (2000) Electron flow between photosystem II and oxygen in chloroplasts of photosystem I-deficient algae is mediated by a quinol oxidase involved in chlororespiration. J Biol Chem 275:17256–17262
Cruz JA, Avenson TJ, Kanazawa A, Takizawa K, Edwards GE, Kramer DM (2005) Plasticity in light reactions of photosynthesis for energy production and photoprotection. J Exp Bot 56:395–406
Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24
Diaz M, De Haro V, Munoz R, Quiles MJ (2007) Chlororespiration is involved in the adaptation of Brassica plants to heat and high light intensity. Plant Cell Environ 30:1578–1585
Dietzel L, Bräutigam K, Pfannschmidt T (2008) Photosynthetic acclimation: state transitions and adjustment of photosystem stoichiometry–functional relationships between short-term and long-term light quality acclimation in plants. FEBS J 275:1080–1088
Eichelmann H, Laisk A (2000) Cooperation of photosystems II and I in leaves as analysed by simultaneous measurements of chlorophyll fluorescence and transmittance at 800 nm. Plant Cell Physiol 41:138–147
Eichelmann H, Oja V, Peterson RB, Laisk A (2011) The rate of nitrite reduction in leaves as indicated by O2 and CO2 exchange during photosynthesis. J Exp Bot 62:2205–2215
Engelbrecht BMJ, Comita LS, Condit R, Kursar TA, Tyree MT, Turner BL et al (2007) Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447:80–82
Epron D, Godard G, Cornic G, Genty B (1995) Limitation of net CO2 assimilation rate by internal resistances to CO2 transfer in the leaves of two tree species (Fagus sylvatica and Castanea sativa Mill.). Plant Cell Environ 18:43–51
Flexas J, Medrano H (2002) Energy dissipation in C3 plants under drought. Funct Plant Biol 29:1209–1215
Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biol 6:269–279
Flexas J, Barbour MM, Brendel O, Cabrera HM, Carriquí M, Díaz-Espejo A et al (2012) Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Sci 193–194:70–84
Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905
Fristedt R, Vener AV (2011) High light induced disassembly of photosystem II supercomplexes in Arabidopsis requires STN7-dependent phosphorylation of CP29. PLoS ONE 6:e24565
Galmes J, Medrano H, Jaume F (2006) Acclimation of Rubisco specificity factor to drought in tobacco: discrepancies between in vitro and in vivo estimations. J Exp Bot 57:3659–3667
Genty B, Briantais JM, Baker NR (1989) The relationship between 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
Golding AJ, Finazzi G, Johnson GN (2004) Reduction of the thylakoid electron transport chain by stromal reductants: evidence for activation of cyclic electron transport upon dark adaptation or under drought. Planta 202:356–363
Goltsev V, Zaharieva I, Chernev P, Kouzmanova M, Kalaji MH, Yordanov I, Krasteva V, Alexandrov V, Stefanov D, Allakhverdiev SI, Strasser RJ (2012) Drought-induced modifications of photosynthetic electron transport in intact leaves: analysis and use of neural networks as a tool for a rapid non-invasive estimation. Biochim Biophys Acta 1817:1490–1498
Gray GR, Savitch LV, Ivanov AC, Huner NPA (1996) Photosystem II excitation pressure and development of resistance to photoinhibition. 2. Adjustment of photosynthetic capacity in winter wheat and winter rye. Plant Physiol 110:61–71
Harley PC, Loreto F, Di Marco G, Sharkey TD (1992) Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiol 98:1429–1436
Härtel H, Lokstein H (1995) Relationship between quenching of maximum and dark-level chlorophyll fluorescence in vivo: dependence on photosystem II antenna size. Biochim Biophys Acta 1228:91–94
Heber U, Walker D (1992) Concerning a dual function of coupled cyclic electron-transport in leaves. Plant Physiol 100:1621–1626
Holaday AS, Martindale W, Alred R, Brooks AL, Leegood RC (1992) Changes in activities of enzymes of carbon metabolism in leaves during exposure of plants to low temperature. Plant Physiol 98:1105–1114
Huang W, Zhang SB, Cao KF (2010) 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
Ivanov AG, Sane PV, Hurry V, Öquist G, Huner NPA (2008) Photosystem II reaction center quenching: mechanisms and physiological role. Photosynth Res 98:565–574
Ivanov AG, Rosso D, Savitch LV, Stachula P, Rosembert M, Oquist G et al (2012) Implications of alternative electron sinks in increased resistance of PSII and PSI photochemistry to high light stress in cold-acclimated Arabidopsis thaliana. Photosynth Res 113:191–206
Joët T, Genty B, Josse E-M, Kuntz M, Cournac L, Peltier G (2002) Involvement of a plastid terminal oxidase in plastoquinone oxidation as evidenced by expression of the Arabidopsis thaliana enzyme in tobacco. J Biol Chem 277:31623–31630
Johnson GN (2005) Cyclic electron transport in C3 plants: fact or artefact? J Exp Bot 56:407–416
Johnson GN (2011) Physiology of PSI cyclic electron transport in higher plants. Biochim Biophys Acta 1807:384–389
Josse E-M, Alcaraz J-P, Labouré A-M, Kuntz M (2003) In vitro characterization of a plastid terminal oxidase (PTOX). Eur J Biochem 270:3787–3794
Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376:105–115
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
Kohzuma K, Cruz JA, Akashi K, Hoshiyasu S, Munekage YN, Yokota A, Kramer DM (2009) The long-term responses of the photosynthetic proton circuit to drought. Plant Cell Environ 32:209–219
Kozaki A, Takeba G (1996) Photorespiration protects C3 plants from photooxidation. Nature 384:557–560
Krall JP, Edwards GE (1992) Relationship between photosystem II activity and CO2 fixation in leaves. Physiol Plant 86:180–187
Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155:70–78
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
Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Ann Rev Plant Physiol Plant Mol Biol 42:313–349
Laisk A, Loreto F (1996) Determining photosynthetic parameters from leaf CO2 exchange and chlorophyll fluorescence: ribulose-1,5-bisphosphate carboxylase oxygenase specificity factor, dark respiration in the light, excitation distribution between photosystems, alternative electron transport rate, and mesophyll diffusion resistance. Plant Physiol 110:903–912
Laisk A, Eichelmann H, Oja V, Talts E, Scheibe R (2007) Rates and roles of cyclic and alternative electron flow in potato leaves. Plant Cell Physiol 48:1575–1588
Laisk A, Talts E, Oja V, Eichelmann H, Peterson R (2010) Fast cyclic electron transport around photosystem I in leaves under far-red light: a proton-uncoupled pathway? Photosynth Res 103:79–95
Lal A, Ku MSB, Edwards GE (1996) Analysis of inhibition of photosynthesis due to water-stress in the C3 species Hordeum vulgare and Vicia faba—electron-transport, CO2 fixation and carboxylation capacity. Photosynth Res 49:57–69
Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ 25:275–294
Lehtimäki 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
Li XP, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395
Liu WJ, Chen YE, Tian WJ, Du JB, Zhang ZW, Xu F, Zhang F, Yuan S, Lin HH (2009) Dephosphorylation of photosystem II proteins and phosphorylation of CP29 in barley photosynthetic membranes as a response to water stress. Biochim Biophys Acta 1787:1238–1245
Livingston AK, Cruz JA, Kohzuma K, Dhingra A, Kramer DM (2010) An Arabidopsis mutant with high cyclic electron flow around photosystem I (hcef) involving the NADPH dehydrogenase complex. Plant Cell 22:221–233
Maroco JP, Rodrigues ML, Lopes C, Chaves MM (2002) Limitations to leaf photosynthesis in grapevine under drought: metabolic and modelling approaches. Funct Plant Biol 29:1–9
Mathur S, Allakhverdiev SI, Jajoo A (2011) Analysis of high temperature stress on the dynamics of antenna size and reducing side heterogeneity of photosystem II in wheat leaves (Triticum aestivum). Biochim Biophys Acta Bioenerg 1807:22–29
McDonald AE, Ivanov AG, Bode R, Maxwell DP, Rodermel SR, Hüner NPA (2011) Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminal oxidase (PTOX). Biochim Biophys Acta 1807:954–967
Mehta P, Allakhverdiev SI, Jajoo A (2010) Characterization of photosystem II heterogeneity in response to high salt stress in wheat leaves (Triticum aestivum). Photosynth Res 105:249–255
Miyake C (2010) Alternative electron flows (water–water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. Plant Cell Physiol 51:1951–1963
Muller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566
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
Niyogi KK, Li X-P, Rosenberg V, Jung H-S (2005) Is PsbS the site of non-photochemical quenching in photosynthesis? J Exp Bot 56:375–382
Ogren WL (1984) Photorespiration: pathways, regulation, and modification. Annu Rev Plant Physiol 35:415–442
Ort DR (2001) When there is too much light. Plant Physiol 125:29–32
Ortiz-Lopez A, Ort DR, Boyer JS (1991) Photophosphorylation in attached leaves of Helianthus annuus at low water potentials. Plant Physiol 96:1018–1025
Parry M, Andraloje PJ, Khan S, Lea PJ, Keys A (2002) Rubisco activity: effect of drought stress. Ann Bot 89:833–839
Passioura J (2007) The drought environment: physical, biological and agricultural perspectives. J Exp Bot 58:113–117
Pfundel EE (1998) Estimating the contribution of photosystem I to total leaf chlorophyll fluorescence. Photosynth Res 56:185–195
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
Ruuska SA, Badger MR, Andrews TJ, von Caemmerer S (2000) Photosynthetic electron sinks in transgenic tobacco with reduced amounts of Rubisco: little evidence for significant Mehler reaction. J Exp Bot 51:357–368
Savitch LV, Ivanov AG, Krol M, Sprott DP, Öquist G, Huner NPA (2010) Regulation of energy partitioning and alternative electron transport pathways during cold acclimation of lodgepole pine is oxygen dependent. Plant Cell Physiol 51:1555–1570
Schreiber U (1986) Detection of rapid induction kinetics with a new type of high frequency modulated chlorophyll fluorescence. Photosynth Res 9:261–272
Schreiber U, Bilger W, Klughammer C, Neubauer C (1988) Application of the PAM fluorometer in stress detection. In: Lichtenthaler HK (ed) Applications of chlorophyll fluorescence. Kluwer, Dordrecht, pp 151–155
Schreiber U, Hormann H, Neubauer C, Klughammer C (1995) Assessment of photosystem II photochemical quantum yield by chlorophyll fluorescence quenching analysis. Aust J Plant Physiol 22:209–220
Stepien P, Johnson GN (2009) Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis thaliana and the halophyte Tellungiella halophila. Role of the plastid terminal oxidase as an alternative electron sink. Plant Physiol 149:1154–1165
Tezara W, Mitchell VJ, Driscoll SD, Lawlor DW (1999) Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401:914–917
Tikkanen M, Piippo M, Suorsa M, Sirpio S, Mulo P, Vainonen J, Vener AV, Allahverdiyeva Y, Aro EM (2006) State transitions revisited—a buffering system for dynamic low light acclimation of Arabidopsis. Plant Mol Biol 62:779–79371
Turner NC (1981) Techniques and experimental approaches for the measurement of plant water status. Plant Soil 58:339–366
Valentini R, Epron D, De Angelis P, Matteucci G, Dreyer E (1995) In situ estimation of net CO2 assimilation, photosynthetic electron flow and photorespiration in Turkey oak (Q. cerris L.) leaves: diurnal cycles under different levels of water supply. Plant Cell Environ 18:631–640
Van den Berg M, Driessen PM, Rabbinge R (2002) Water uptake in crop growth models for land use systems analysis: II. Comparison of three simple approaches. Ecol Model 148:233–250
Vassileva V, Demirevska K, Simova-Stoilova L, Petrova T, Tsenov N, Feller U (2012) Long-term field drought affects leaf protein pattern and chloroplast ultrastructure of winter wheat in a cultivar-specific manner. J Agron Crop Sci 198:104–117
Walters R, Horton GP (1991) Resolution of components of non-photochemical chlorophyll fluorescence quenching in barley leaves. Photosynth Res 27:121–133
Wingler A, Quick WP, Bungard RA, Bailey KJ, Lea PJ, Leegood RC (1999) The role of photorespiration during drought stress: an analysis utilizing barley mutants with reduced activities of photorespiratory enzymes. Plant Cell Environ 22:361–373
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
Yin X, Struik PC, Romero P, Harbinson J, Evers JB, Van der Putten PEL, Vos J (2009) Using combined measurements of gas exchange and chlorophyll fluorescence to estimate parameters of a biochemical C3 photosynthesis model: a critical appraisal and a new integrated approach applied to leaves in a wheat (Triticum aestivum) canopy. Plant Cell Environ 32:448–464
Yuan S, Liu WJ, Zhang NH, Wang MB, Liang HG, Lin HH (2005) Effects of water stress on major PSII gene expression and protein metabolism in barley leaves. Physiol Plant 125:464–473
Zadraznik T, Hollung K, Egge-Jacobsen W, Meglic V, Sustar-Vozlic J (2013) Differential proteomic analysis of drought stress response in leaves of common bean (Phaseolus vulgaris L.). J Proteomics 78:254–272
Zivcak M, Brestic M, Olsovska K, Slamka P (2008) Performance index as a sensitive indicator of water stress in Triticum aestivum. Plant Soil Environ 54:133–139
Acknowledgments
The authors thank Dr Richard J. Ladle (School of Geography and the Environment, Oxford University, UK, and Institute of Biological and Health Sciences, Federal University of Alagoas, Praça Afrânio Jorge, s/n, Prado, Maceió, AL, Brazil) for reviewing and improving the English of the manuscript. The research described here has been supported by grant APVV-0197-10 and APVV-0661-10. This study was also supported by grants from the Russian Foundation for Basic Research and Molecular and Cell Biology Programs of the Russian Academy of Sciences to SIA.
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See Table 1 for other symbols representing chlorophyll fluorescence and P700 parameters apart from the abbreviations listed.
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Zivcak, M., Brestic, M., Balatova, Z. et al. Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth Res 117, 529–546 (2013). https://doi.org/10.1007/s11120-013-9885-3
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DOI: https://doi.org/10.1007/s11120-013-9885-3