Abstract
Wheat (Triticum aestivum) plants often suffer from heat stress combined with high irradiance during the grain filling stage. Glycine betaine (GB) is a compatible solute that accumulates rapidly to enhance stress tolerance in wheat under abiotic stress. In this study, the effect of foliar application of GB on photosystem II (PSII) photochemistry in wheat leaves under the heat and high light stresses were investigated. The results showed that GB-supplemented wheat plants maintained higher chlorophyll content, photochemical activity of PSII and net photosynthetic rate (P n) than stressed only plants. Moreover, GB-treated plants could retard the decrease of psbA gene transcription and accelerate the endogenous accumulation of GB in leaves. The results suggested that the increasing stress tolerance by GB accumulation was associated with an improvement in D1 protein synthesis, which accelerated the repair of PSII following stress-enhanced photoinhibition. Moreover, the accumulation of abscisic acid under the heat and high light stresses was retarded by foliar application of GB, and the decrease of stomatal conductance was inhibited as well. The results suggested that GB accumulation in vivo was involved in the regulation of stomatal conductance. Further work is required to elucidate the mechanism of GB-induced stomatal movement and PSII photoprotection.
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Abbreviations
- ABA:
-
Abscisic acid
- ANOVA:
-
One-way analysis of variance
- C t :
-
Cycle threshold
- ddH2O:
-
Double distilled H2O
- ELISA:
-
Enzyme-linked immuno sorbent
- F m :
-
Maximal fluorescence
- F v :
-
Variable fluorescence in dark-adapted leaves
- F v/F m :
-
Maximal efficiency of PSII
- GB:
-
Glycine betaine
- g s :
-
Stomatal conductance
- HPLC:
-
High-performance liquid chromatography
- P n :
-
Net photosynthetic rate
- PPFD:
-
Photosynthetic photon flux density
- PSII:
-
Photosystem II
- ROS:
-
Reactive oxygen species
- SA:
-
Salicylic acid
References
Allakhverdiev SI, Hayashi H, Nishiyama Y, Ivanov AG, Aliev JA, Klimov VV, Murata N, Carpentier R (2003) Glycinebetaine protects the D1/D2/Cytb559 complex of photosystem II against photo-induced and heat-induced inactivation. J Plant Physiol 160:41–49
Allakhverdiev SI, Los DA, Mohanty P, Nishiyama Y, Murata N (2007) Glycinebetaine alleviates the inhibitory effect of moderate heat stress on the repair of photosystem II during photoinhibition. Biochim Biophys Acta 1767:1363–1371
Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550
Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113
Chen TH, Murata N (2008) Glycinebetaine: an effective protectant against abiotic stress in plants. Trends Plant Sci 13:499–505
Chen TH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20
Chen L, Jia H, Tian Q, Du L, Gao Y, Miao X, Liu Y (2012) Protecting effect of phosphorylation on oxidative damage of D1 protein by down-regulating the production of superoxide anion in photosystem II membranes under high light. Photosynth Res 112:141–148
Csiszár J, Gallé Á, Horváth E, Dancsó P, Gombos M, Váry Z, Erdei L, Györgyey J, Tari I (2012) Different peroxidase activities and expression of abiotic stress-related peroxidases in apical root segments of wheat genotypes with different drought stress tolerance under osmotic stress. Plant Physiol Biochem 52:119–129
Dall’Osto L, Lico C, Alric J, Giuliano G, Havaux M, Bassi R (2006) Lutein is needed for efficient chlorophyll triplet quenching in the major LHCII antenna complex of higher plants and effective photoprotection in vivo under strong light. BMC Plant Biol 6:32
Edelman M, Mattoo AK (2008) D1 protein dynamics in photosystem II: the lingering enigma. Photosynth Res 98:609–620
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil, Circular California Agricultural Experiment Station, vol 347
Kopka J, Provart NJ, Müller-Röber B (1997) Potato guard cells respond to drying soil by a complex change in the expression of genes related to carbon metabolism and turgor regulation. Plant J 11:871–882
Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695
Li M, Li Z, Li S, Guo S, Meng Q, Li G, Yang X (2014) Genetic engineering of glycine betaine biosynthesis reduces heat-enhanced photoinhibition by enhancing antioxidative defense and alleviating lipid peroxidation in tomato. Plant Mol Biol Rep 32:42–51
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408
Ma QQ, Wang W, Li YH, Li DQ, Zou Q (2006) Alleviation of photoinhibition in drought-stressed wheat (Triticum aestivum) by foliar-applied glycinebetaine. J Plant Physiol 163:165–175
Mahouachi J, Argamasilla R, Gómez-Cadenas A (2012) Influence of exogenous glycine betaine and abscisic acid on papaya in responses to water-deficit stress. J Plant Growth Regul 31:1–10
Mäkelä P, Peltonen-Sainio P, Jokinen K, Pehu E, Setälä H, Hinkkanen R, Somersalo S (1996) Uptake and translocation of foliar-applied glycinebetaine in crop plants. Plant Sci 121:221–230
Marutani Y, Yamauchi Y, Kimura Y, Mizutani M, Sugimoto Y (2012) Damage to photosystem II due to heat stress without light-driven electron flow: involvement of enhanced introduction of reducing power into thylakoid membranes. Planta 236:753–761
Miura K, Okamoto H, Okuma E, Shiba H, Kamada H, Hasegawa PM, Murata Y (2013) SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis. Plant J 73:91–104
Mulo P, Sicora C, Aro EM (2009) Cyanobacterial psbA gene family: optimization of oxygenic photosynthesis. Cell Mol Life Sci 66:3697–3710
Mulo P, Sakurai I, Aro EM (2012) Strategies for psbA gene expression in cyanobacteria, green algae and higher plants: from transcription to PSII repair. Biochim Biophys Acta 1817:247–257
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421
Ortiz R, Sayre KD, Govaerts B, Gupta R, Subbarao G, Ban T, Hodson D, Dixon JM, Iván OM (2008) Climate change: can wheat beat the heat? Agri Ecosys Environ 126:46–58
Roelfsema MRG, Hedrich R (2005) In the light of stomatal opening: new insights into ‘the Watergate’. New Phytol 167:665–691
Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410:327–330
Shah N, Paulsen G (2003) Interaction of drought and high temperature on photosynthesis and grain-filling of wheat. Plant Soil 257:219–226
Tyystjärvi E (2013) Photoinhibition of photosystem II. Int Rev Cell Mol Biol 300:243–303
Vaseva II, Grigorova BS, Simova-Stoilova LP, Demirevska KN, Feller U (2010) Abscisic acid and late embryogenesis abundant protein profile changes in winter wheat under progressive drought stress. Plant Biol 12:698–707
Vass I (2012) Molecular mechanisms of photodamage in the photosystem II complex. Biochim Biophys Acta 1817:209–217
Wang GP, Li F, Zhang J, Zhao MR, Hui Z, Wang W (2010a) Overaccumulation of glycine betaine enhances tolerance of the photosynthetic apparatus to drought and heat stress in wheat. Photosynthetica 48:30–41
Wang GP, Zhang XY, Li F, Luo Y, Wang W (2010b) Overaccumulation of glycine betaine enhances tolerance to drought and heat stress in wheat leaves in the protection of photosynthesis. Photosynthetica 48:117–126
Wang YX, Suo B, Zhao TF, Qu XF, Yuan LG, Zhao XJ, Zhao HJ (2011) Effect of nitric oxide treatment on antioxidant responses and psbA gene expression in two wheat cultivars during grain filling stage under drought stress and rewatering. Acta Physiol Plant 33:1923–1932
Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ 33:510–525
Yamamoto Y (2001) Quality control of photosystem II. Plant Cell Physiol 42:121–128
Yamamoto Y, Aminaka R, Yoshioka M, Khatoon M, Komayama K, Takenaka D, Yamashita A, Nijo N, Inagawa K, Morita N, Sasaki T (2008) Quality control of photosystem II: impact of light and heat stresses. Photosynth Res 98:589–608
Yang X, Lu C (2006) Effects of exogenous glycinebetaine on growth, CO2 assimilation, and photosystem II photochemistry of maize plants. Physiol Plant 127:593–602
Yang X, Wen X, Gong H, Lu Q, Yang Z, Tang Y, Liang Z, Lu C (2007) Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants. Planta 225:719–733
Zhao HJ, Zhao XJ, Ma PF, Wang YX, Hu WW, Li LH, Zhao YD (2011) Effect of salicylic acid on protein kinase activity and chloroplast D1 protein degradation in wheat leaves subjected to heat and high light stress. Acta Ecol Sin 31:259–263
Acknowledgments
This research was supported by the National Natural Science Foundation of China (Grant No. 31000688) and the Education Department of Henan Province (Grant No. 13A210487).
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Communicated by Z. Miszalski.
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Wang, Y., Liu, S., Zhang, H. et al. Glycine betaine application in grain filling wheat plants alleviates heat and high light-induced photoinhibition by enhancing the psbA transcription and stomatal conductance. Acta Physiol Plant 36, 2195–2202 (2014). https://doi.org/10.1007/s11738-014-1596-7
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DOI: https://doi.org/10.1007/s11738-014-1596-7