Changes of Antioxidant Defense System and Fatty Acid Composition in Bermudagrass under Chilling Stress

in Journal of the American Society for Horticultural Science

Bermudagrass (Cynodon dactylon) is a typical and widely used warm-season turfgrass. Low temperature is one of the key environmental stress limiting its utility. However, little information is available about the differences of cold response between bermudagrass genotypes. Here, we analyzed antioxidant defense system and fatty acid composition in cold-resistant genotype WBD128 and cold-sensitive genotype WBDg17 exposed to chilling stress. Low temperature (4 °C) significantly decreased the relative water content, whereas increased the H2O2 and O2 contents, more profoundly for WBDg17. Under chilling condition, WBD128 had higher anti O2 activity than WBDg17. Besides, the contents of total glutathione, reduced glutathione (GSH) and its oxidized form (GSSG) were markedly increased by low temperature in both genotypes, whereas WBD128 had significantly higher values of GSH, total glutathione, and GSH/GSSG ratio than WBDg17. Moreover, chilling stress increased saturated fatty acids (SFAs) percentage (palmitic acid and stearic acid) in WBDg17. After chilling treatment, the proportion of linoleic acid decreased in both genotypes, particularly in WBDg17. As for unsaturated fatty acids (UFAs), the percentage of linolenic acid was increased in WBD128. In addition, chilling treatment decreased the values of double bond index (DBI), UFA/SFA ratio as well as degree of unsaturation in WBDg17. Finally, chilling stress altered the expression patterns of the genes, which encode one kind of late embryogenesis abundant proteins (LEA), superoxide dismutase (Cu/Zn SOD) C-repeat-binding factor/DRE-binding factor (CBF1), and peroxidase (POD-2). Collectively, our results revealed that natural variation of chilling tolerance in bermudagrass genotypes may be largely associated with the alterations of antioxidant defense system and fatty acid composition.

Contributor Notes

This work was funded by the China National Science Foundation (NSFC) (grant nos. 31272194, 31401915, and 31428021). We would like to thank Qian Liu for collecting the documents.

Corresponding authors. E-mail: jfu@wbgcas.cn or chenliang1034@126.com.

  • AllenR.D.1995Dissection of oxidative stress tolerance using transgenic plantsPlant Physiol.1071049(abstr.)

  • AlscherR.G.ErturkN.HeathL.S.2002Role of superoxide dismutases (SODs) in controlling oxidative stress in plantsJ. Expt. Bot.5313311341

    • Search Google Scholar
    • Export Citation
  • ApelK.HirtH.2004Reactive oxygen species: Metabolism, oxidative stress, and signal transductionAnnu. Rev. Plant Biol.55373399

  • AroraA.SairamR.K.SrivastavaG.C.2002Oxidative stress and antioxidative system in plantsCurr. Sci.8212271238

  • BaekK.H.SkinnerD.Z.2003Alteration of antioxidant enzyme gene expression during cold acclimation of near-isogenic wheat linesPlant Sci.16512211227

    • Search Google Scholar
    • Export Citation
  • BarrsH.WeatherleyP.1962A re-examination of the relative turgidity technique for estimating water deficits in leavesAustral. J. Biol. Sci.15413428

    • Search Google Scholar
    • Export Citation
  • BurkeM.J.GustaL.V.QuammeH.A.WeiserC.J.LiP.H.1976Freezing and injury in plantsAnnu. Rev. Plant Physiol.27507528

  • CataláR.López-CobolloR.CastellanoM.M.AngostoT.AlonsoJ.M.EckerJ.R.SalinasJ.2014The Arabidopsis 14-3-3 protein RARE COLD INDUCIBLE 1A links low-temperature response and ethylene biosynthesis to regulate freezing tolerance and cold acclimationPlant Cell2633263342

    • Search Google Scholar
    • Export Citation
  • ChenL.RenF.ZhongH.JiangW.LiX.2010Identification and expression analysis of genes in response to high-salinity and drought stresses in Brassica napusActa Biochim. Biophys. Sin. (Shanghai)42154164

    • Search Google Scholar
    • Export Citation
  • CyrilJ.PowellG.L.DuncanR.R.BairdW.V.2002Changes in membrane polar lipid fatty acids of seashore paspalum in response to low temperature exposureCrop Sci.4220312037

    • Search Google Scholar
    • Export Citation
  • FagernessM.J.YelvertonF.H.LivingstonD.P.RuftyT.W.2002Temperature and trinexapac-ethyl effects on bermudagrass growth, dormancy, and freezing toleranceCrop Sci.42853858

    • Search Google Scholar
    • Export Citation
  • FanJ.RenJ.ZhuW.AmomboE.FuJ.ChenL.2014Antioxidant responses and gene expression in bermudagrass under cold stressJ. Amer. Soc. Hort. Sci.139699705

    • Search Google Scholar
    • Export Citation
  • FoyerC.H.Lopez-DelgadoH.DatJ.F.ScottI.M.1997Hydrogen peroxide and glutathione associated mechanisms of acclamatory stress tolerance and signalingPhysiol. Plant.100241254

    • Search Google Scholar
    • Export Citation
  • HalliwellB.GutteridgeJ.M.2015Free radicals in biology and medicine. Oxford Univ. Press Oxford UK

  • HoaglandD.R.ArnonD.I.1950The water-culture method for growing plants without soil. California Agr. Expt. Sta. Circ. 347

  • HoekstraF.A.GolovinaE.A.BuitinkJ.2001Mechanisms of plant desiccation toleranceTrends Plant Sci.6431438

  • HuZ.FanJ.ChenK.AmomboE.ChenL.FuJ.2016aEffects of ethylene on photosystem II and antioxidant enzyme activity in bermuda grass under low temperaturePhotosynth. Res.1285972

    • Search Google Scholar
    • Export Citation
  • HuZ.FanJ.XieY.AmomboE.LiuA.MukamiM.G.ChenL.FuJ.2016bComparative photosynthetic and metabolic analyses reveal mechanism of improved cold stress tolerance in bermudagrass by exogenous melatoninPlant Physiol. Biochem.10094104

    • Search Google Scholar
    • Export Citation
  • HuY.JiangL.WangF.YuD.2013Jasmonate regulates the inducer of CBF expression–c-repeat binding factor/DRE binding factor1 cascade and freezing tolerance in ArabidopsisPlant Cell2529072924

    • Search Google Scholar
    • Export Citation
  • IswariS.PaltaJ.P.1989Plasma membrane ATPase activity following reversible and irreversible freezing injuryPlant Physiol.9010881095

  • JeonJ.KimN.Y.KimS.KangN.Y.NovákO.KuS.J.ChoC.LeeD.J.LeeE.J.StrnadM.KimJ.2010A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in ArabidopsisJ. Biol. Chem.2852337123386

    • Search Google Scholar
    • Export Citation
  • KocsyG.GalibaG.BrunoldC.2001Role of glutathione in adaptation and signalling during chilling and cold acclimation in plantsPhysiol. Plant.113158164

    • Search Google Scholar
    • Export Citation
  • KumariP.BijoA.J.MantriV.A.ReddyC.R.K.JhaB.2013Fatty acid profiling of tropical marine macroalgae: An analysis from chemotaxonomic and nutritional perspectivesPhytochemistry864456

    • Search Google Scholar
    • Export Citation
  • LarkindaleJ.HuangB.2004Changes of lipid composition and saturation level in leaves and roots for heat-stressed and heat acclimated creeping bentgrass (Agrostis stolonifera)Environ. Exp. Bot.515767

    • Search Google Scholar
    • Export Citation
  • LehningerA.L.1977Biochemistry. 2nd ed. Worth Publ. New York NY

  • LuoL.SunT.JiniY.1997Accumulation of superoxide radical in wheat leaves under cadmium stressActa Scientiae Circumstantiae18495499

  • LyonsJ.M.1973Chilling injury in plantsAnnu. Rev. Plant Physiol.24445466

  • MauchF.DudlerR.1993Differential induction of distinct glutathione S-transferases of wheat by xenobiotics and pathogen attackPlant Physiol.10211931201

    • Search Google Scholar
    • Export Citation
  • McKersieB.D.BowleyS.R.1997Active oxygen and freezing tolerance in transgenic plants p. 203–214. In: P.H. Li and T.H.H. Chen (eds.). Plant cold hardiness. Springer New York NY

  • MishraA.PatelM.K.JhaB.2015Non-targeted metabolomics and scavenging activity of reactive oxygen species reveal the potential of Salicornia brachiata as a functional foodJ. Funct. Foods132131

    • Search Google Scholar
    • Export Citation
  • MittlerR.2002Oxidative stress, antioxidants and stress toleranceTrends Plant Sci.7405410

  • NoctorG.ArisiA.C.M.JouaninL.KunertK.J.RennenbergH.FoyerC.H.1998Glutathione: Biosynthesis, metabolism and relationship to stress tolerance explored in transformed plantsJ. Expt. Bot.49623647

    • Search Google Scholar
    • Export Citation
  • PearceR.S.WillisonJ.H.M.1985Wheat tissues freeze-etched during exposure to extracellular freezing: Distribution of icePlanta163295303

  • RachmilevitchS.DaCostaM.HuangB.2006Physiological and biochemical indicators for abiotic stress tolerance p. 321–356. In: B. Huang (ed.). Plant-environment interactions. CRC Press Boca Raton FL

  • RennenbergH.BrunoldC.1994Significance of glutathione metabolism in plants under stressProg. Bot.55144156

  • ŞahinE.GümüşlüS.2004Cold-stress-induced modulation of antioxidant defence: Role of stressed conditions in tissue injury followed by protein oxidation and lipid peroxidationIntl. J. Biometeorol.48165171

    • Search Google Scholar
    • Export Citation
  • ShiY.TianS.HouL.HuangX.ZhangX.GuoH.YangS.2012Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in ArabidopsisPlant Cell2425782595

    • Search Google Scholar
    • Export Citation
  • ShiH.YeT.ChanZ.2013Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in bermudagrass (Cynodon dactylon (L). Pers.)Plant Physiol. Biochem.71226234

    • Search Google Scholar
    • Export Citation
  • ShiH.YeT.ZhongB.LiuX.ChanZ.2014Comparative proteomic and metabolomic analyses reveal mechanisms of improved cold stress tolerance in bermudagrass (Cynodon dactylon (L.) Pers.) by exogenous calciumJ. Integr. Plant Biol.5610641079

    • Search Google Scholar
    • Export Citation
  • SteponkusP.L.1984Role of the plasma membrane in freezing injury and cold acclimationAnnu. Rev. Plant Physiol.35543584

  • ThomashowM.F.1999Plant cold acclimation: Freezing tolerance genes and regulatory mechanismsJ. Integr. Plant Biol.50571599

  • TunnacliffeA.WiseM.J.2007The continuing conundrum of the LEA proteinsNaturwissenschaften94791812

  • VighL.MarescaB.HarwoodJ.L.1998Does the membrane’s physical state control the expression of heat shock and other genes?Trends Biochem. Sci.23369374

    • Search Google Scholar
    • Export Citation
  • WalkerM.A.MckersieB.D.1993Role of the ascorbate-glutathione antioxidant system in chilling resistance of tomatoJ. Plant Physiol.141234239

    • Search Google Scholar
    • Export Citation
  • WeiserC.J.1970Cold resistance and injury in woody plants knowledge of hardy plant adaptations to freezing stress may help us to reduce winter damageScience16912691278

    • Search Google Scholar
    • Export Citation
  • YangP.LiX.LiangY.JingY.ShenS.KuangT.2006Proteomic analysis of the response of Liangyoupeijiu (super high-yield hybrid rice) seedlings to cold stressJ. Integr. Plant Biol.48945951

    • Search Google Scholar
    • Export Citation
  • ZhangX.ErvinE.WaltzC.MurphyT.2011aMetabolic changes during cold acclimation and deacclimation in five bermudagrass varieties: II. Cytokinin and abscisic acid metabolismCrop Sci.51847853

    • Search Google Scholar
    • Export Citation
  • ZhangX.WangK.ErvinE.H.2008Bermudagrass freezing tolerance associated with abscisic acid metabolism and dehydrin expression during cold acclimationJ. Amer. Soc. Hort. Sci.133542550

    • Search Google Scholar
    • Export Citation
  • ZhangX.WangK.ErvinE.WaltzC.MurphyT.2011bMetabolic changes during cold acclimation and deacclimation in five bermudagrass varieties. I. Proline, total amino acid, protein, and dehydrin expressionCrop Sci.51838846

    • Search Google Scholar
    • Export Citation
  • ZhongD.DuH.WangZ.HuangB.2011Genotypic variation in fatty acid composition and unsaturation levels in bermudagrass associated with leaf dehydration toleranceJ. Amer. Soc. Hort. Sci.1363540

    • Search Google Scholar
    • Export Citation
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