Skip to main content
Log in

Glycine betaine application in grain filling wheat plants alleviates heat and high light-induced photoinhibition by enhancing the psbA transcription and stomatal conductance

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  CAS  PubMed  Google Scholar 

  • Chen TH, Murata N (2008) Glycinebetaine: an effective protectant against abiotic stress in plants. Trends Plant Sci 13:499–505

    Article  CAS  PubMed  Google Scholar 

  • Chen TH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Edelman M, Mattoo AK (2008) D1 protein dynamics in photosystem II: the lingering enigma. Photosynth Res 98:609–620

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Mulo P, Sicora C, Aro EM (2009) Cyanobacterial psbA gene family: optimization of oxygenic photosynthesis. Cell Mol Life Sci 66:3697–3710

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Roelfsema MRG, Hedrich R (2005) In the light of stomatal opening: new insights into ‘the Watergate’. New Phytol 167:665–691

    Article  CAS  PubMed  Google Scholar 

  • Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410:327–330

    Article  CAS  PubMed  Google Scholar 

  • Shah N, Paulsen G (2003) Interaction of drought and high temperature on photosynthesis and grain-filling of wheat. Plant Soil 257:219–226

    Article  CAS  Google Scholar 

  • Tyystjärvi E (2013) Photoinhibition of photosystem II. Int Rev Cell Mol Biol 300:243–303

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Vass I (2012) Molecular mechanisms of photodamage in the photosystem II complex. Biochim Biophys Acta 1817:209–217

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ 33:510–525

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto Y (2001) Quality control of photosystem II. Plant Cell Physiol 42:121–128

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Yuexia Wang or Huijie Zhao.

Additional information

Communicated by Z. Miszalski.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-014-1596-7

Keywords

Navigation