Transcriptomic Study of Early Responses to the Bud Dormancy-breaking Agent Hydrogen Cyanamide in ‘TropicBeauty’ Peach

in Journal of the American Society for Horticultural Science

To determine how the dormancy-breaking agent hydrogen cyanamide (HC) advances budbreak in peach (Prunus persica), this study compared the transcriptome of buds of low-chill ‘TropicBeauty’ peach trees treated with 1% (v/v) HC and that of nontreated trees at 3 and 7 days after treatment (DAT), respectively, using an RNA sequencing analysis. The peak of total budbreak occurred 6 weeks earlier in the HC-treated trees (at 32 DAT) than the nontreated trees (at 74 DAT). There were 1312 and 1095 differentially expressed genes (DEGs) at 3 and 7 DAT, respectively. At 3 DAT, DEGs related to oxidative stress, including the response to hypoxia, lipid oxidation, and reactive oxygen species (ROS) metabolic process, were upregulated in HC-treated buds. Additionally, DEGs encoding enzymes for ROS scavenging and the pentose phosphate pathway were upregulated at 3 DAT but they were not differently expressed at 7 DAT, indicating a temporary demand for defense mechanisms against HC-triggered oxidative stress. Upregulation of DEGs for cell division and development at 7 DAT, which were downregulated at 3 DAT, suggests that cell activity was initially suppressed but was enhanced within 7 DAT. At 7 DAT, DEGs related to cell wall degradation and modification were upregulated, which was possibly responsible for the burst of buds. The results of this study strongly suggest that HC induces transient oxidative stress shortly after application, leading to the release of bud dormancy and, subsequently, causing an increase in cell activity and cell wall loosening, thereby accelerating budbreak in peach.

Contributor Notes

Corresponding author. E-mail: tvashisth@ufl.edu.

Article Sections

Article Figures

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    Budbreak rate expressed as the number of swollen (about to open) or open flower and vegetative buds for nontreated ‘TropicBeauty’ peach control trees and ‘TropicBeauty’ peach trees treated with 1% (v/v) hydrogen cyanimide (HC) 21 to 81 d after treatment (DAT) and 21 to 60 DAT, respectively, and the accumulation of chill hours (Weinberger, 1950) in Citra, FL, since 1 Oct. 2015. Data are means ± se of four biological replicates. *Significant differences based on Student’s t test for total budbreak rate between control and HC-treated trees on the same day.

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    Overview of hydrogen cyanide-related metabolic pathways in which enzymes were encoded by the differentially expressed genes (DEGs), with red and blue indicating upregulated and downregulated DEGs, respectively, in buds of ‘TropicBeauty’ peach trees treated with 1% (v/v) hydrogen cyanamide compared with nontreated control trees at 3 d after treatment (DAT) (A). A list of these enzymes, DEGs, putative Arabidopsis thaliana orthologs, and log2 fold change (LFC) at 3 DAT (B) is provided.

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    Overview of glycolysis (highlighted in orange), tricarboxylic acid cycle (highlighted in yellow), and pentose phosphate pathway (highlighted in green) in which enzymes were encoded by the differentially expressed genes (DEGs), with red and blue indicating upregulated and downregulated DEGs, respectively, in buds of ‘TropicBeauty’ peach trees treated with 1% (v/v) hydrogen cyanamide compared with nontreated control trees at 3 d after treatment (DAT) (A) and 7 DAT (B). A list of these enzymes, DEGs, putative Arabidopsis thaliana orthologs, and log2 fold change (LFC) at 3 and 7 DAT (C) is provided.

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    Significant gene ontology (GO) terms of upregulated and downregulated differentially expressed genes (DEGs), indicated by red and blue, respectively, in buds of ‘TropicBeauty’ peach trees treated with 1% (v/v) hydrogen cyanamide compared with nontreated control trees at 3 and 7 d after treatment (DAT) for the biological process (A), molecular function (B), and cellular component (C). The intensity of the color indicates the enrichment values [absolute values of the logarithm (to the base of 10) of false discovery rate–corrected P values based on Fisher’s exact test for GO enrichment analysis] of individual GO terms.

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    Relative expressions of formate dehydrogenase (FDH), manganese superoxide dismutase1 (MSD1), glutathione s-transferase tau8 (GSTU8), glutathione s-transferase tau19 (GSTU19), peptide methionine sulfoxide reductase1 (PMSR1), and nadph:quinone oxidoreductase (NQR) in buds of nontreated control ‘TropicBeauty’ peach trees (solid lines with white circles) and trees treated with 1% (v/v) hydrogen cyanamide [HC (broken lines with black circles)] at 0, 1, 3, and 7 d after treatment (DAT) analyzed using real-time quantitative polymerase chain reaction (qPCR); data are means ± se of four biological replicates; asterisks indicate significant differences based on Student’s t test between control and HC-treated trees on the same day; ns = no significant difference.

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    Relative expression of dormancy-associated MADS-box 1 (DAM1), DAM5, and DAM6, apetala1 (AP1), pistillata (PI), agamous (AG), and floral binding protein9 (FBP9) in buds of nontreated control ‘TropicBeauty’ peach trees (solid lines with white circles) and trees treated with 1% (v/v) hydrogen cyanamide [HC (broken lines with black circles)] at 0, 1, 3, and 7 d after treatment (DAT) analyzed using real-time quantitative polymerase chain reaction (qPCR); data are means ± se of four biological replicates; ns = no significant difference based on Student’s t test between control and HC-treated trees on the same day.

Article References

  • AntoniniE.BrunoriM.GreenwoodC.MalmströmB.G.RotilioG.C.1971The interaction of cyanide with cytochrome oxidaseEur. J. Biochem.23396400

    • Search Google Scholar
    • Export Citation
  • BabithaK.C.RamuS.V.PruthviV.MaheshP.NatarajaK.N.UdayakumarM.2013Co-expression of AtbHLH17 and AtWRKY28 confers resistance to abiotic stress in ArabidopsisTransgenic Res.22327341

    • Search Google Scholar
    • Export Citation
  • BaiS.SaitoT.SakamotoD.ItoA.FujiiH.MoriguchiT.2013Transcriptome analysis of japanese pear (Pyrus pyrifolia Nakai) flower buds transitioning through endodormancyPlant Cell Physiol.5411321151

    • Search Google Scholar
    • Export Citation
  • BakshiM.OelmüllerR.2014WRKY transcription factorsPlant Signal. Behav.9e27700

  • BarrettT.WilhiteS.E.LedouxP.EvangelistaC.KimI.F.TomashevskyM.MarshallK.A.PhillippyK.H.ShermanP.M.HolkoM.YefanovA.LeeH.ZhangN.RobertsonC.L.SerovaN.DavisS.SobolevaA.2013NCBI GEO: Archive for functional genomics data sets–updateNucleic Acids Res.41D991D995

    • Search Google Scholar
    • Export Citation
  • BaxterC.J.RedestigH.SchauerN.RepsilberD.PatilK.R.NielsenJ.SelbigJ.LiuA.FernieA.R.SweetloveL.J.2007The metabolic response of heterotrophic Arabidopsis cells to oxidative stressPlant Physiol.143312325

    • Search Google Scholar
    • Export Citation
  • BeauvieuxR.WendenB.DirlewangerE.2018Bud dormancy in perennial fruit tree species: A pivotal role for oxidative cuesFront. Plant Sci.9657

    • Search Google Scholar
    • Export Citation
  • BendallD.S.BonnerW.D.1971Cyanide-insensitive respiration in plant mitochondriaPlant Physiol.47236245

  • BielenbergD.G.WangY.LiZ.ZhebentyayevaT.FanS.ReighardG.L.ScorzaR.AbbottA.G.2008Sequencing and annotation of the ever-growing locus in peach [Prunus persica (L.) Batsch] reveals a cluster of six MADS-box transcription factors as candidate genes for regulation of terminal bud formationTree Genet. Genomes4495507

    • Search Google Scholar
    • Export Citation
  • BlokhinaO.FagerstedtK.V.2010Oxidative metabolism, ROS and NO under oxygen deprivationPlant Physiol. Biochem.48359373

  • BoadaJ.RoigT.PerezX.GamezA.BartronsR.CascanteM.BermúdezJ.2000Cells overexpressing fructose-2,6-bisphosphatase showed enhanced pentose phosphate pathway flux and resistance to oxidative stressFEBS Lett.480261264

    • Search Google Scholar
    • Export Citation
  • BonhommeM.RageauR.GendraudM.2000Influence of temperature on the dynamics of ATP, ADP and non-adenylic triphosphate nucleotides in vegetative and floral peach buds during dormancyTree Physiol.20615621

    • Search Google Scholar
    • Export Citation
  • BoundS.A.JonesK.M.2004Hydrogen cyanamide impacts on flowering, crop load, and fruit quality of red ‘Fuji’ apple (Malus domestica)N. Z. J. Crop Hort. Sci.32227234

    • Search Google Scholar
    • Export Citation
  • ChenL.SongY.LiS.ZhangL.ZouC.YuD.2012The role of WRKY transcription factors in plant abiotic stressesBiochim. Biophys. Acta1819120128

    • Search Google Scholar
    • Export Citation
  • ChoiD.S.KimN.H.HwangB.K.2014Pepper mitochondrial FORMATE DEHYDROGENASE1 regulates cell death and defense responses against bacterial pathogensPlant Physiol.16612981311

    • Search Google Scholar
    • Export Citation
  • ConsidineM.J.ConsidineJ.A.2016On the language and physiology of dormancy and quiescence in plantsJ. Expt. Bot.6731893203

  • CooperC.E.BrownG.C.2008The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: Chemical mechanism and physiological significanceJ. Bioenerg. Biomembr.40533

    • Search Google Scholar
    • Export Citation
  • CosgroveD.J.2000Expansive growth of plant cell wallsPlant Physiol. Biochem.38109124

  • CouéeI.SulmonC.GouesbetG.El AmraniA.2006Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plantsJ. Expt. Bot.57449459

    • Search Google Scholar
    • Export Citation
  • DemidchikV.StraltsovaD.MedvedevS.S.PozhvanovG.A.SokolikA.YurinV.2014Stress-induced electrolyte leakage: The role of K+-permeable channels and involvement in programmed cell death and metabolic adjustmentJ. Expt. Bot.6512591270

    • Search Google Scholar
    • Export Citation
  • DemidchikV.2015Mechanisms of oxidative stress in plants: From classical chemistry to cell biologyEnviron. Exp. Bot.109212228

  • DennisF.G.2003Problems in standardizing methods for evaluating the chilling requirements for the breaking of dormancy in buds of woody plantsHortScience38347350

    • Search Google Scholar
    • Export Citation
  • EdgarR.DomrachevM.LashA.E.2002Gene expression omnibus: NCBI gene expression and hybridization array data repositoryNucleic Acids Res.30207210

    • Search Google Scholar
    • Export Citation
  • FarmerE.E.MuellerM.J.2013ROS-mediated lipid peroxidation and RES-activated signalingAnnu. Rev. Plant Biol.64429450

  • GeorgeA.P.LloydJ.NissenR.J.1992Effects of hydrogen cyanamide, paclobutrazol and pruning date on dormancy release of the low chill peach cultivar Flordaprince in subtropical AustraliaAustral. J. Expt. Agr.328995

    • Search Google Scholar
    • Export Citation
  • GleadowR.M.MøllerB.L.2014Cyanogenic glycosides: Synthesis, physiology, and phenotypic plasticityAnnu. Rev. Plant Biol.65155185

  • GodiniA.PalascianoM.FerraraG.CamposeoS.PacificoA.2008On the advancement of bud break and fruit ripening induced by hydrogen cyanamide (Dormex®) in sweet cherry: A three-year studyActa Hort.795469478

    • Search Google Scholar
    • Export Citation
  • GookinT.E.HunterD.A.ReidM.S.2003Temporal analysis of alpha and beta-expansin expression during floral opening and senescencePlant Sci.164769781

    • Search Google Scholar
    • Export Citation
  • HalalyT.PangX.BatikoffT.CraneO.KerenA.VenkateswariJ.OgrodovitchA.SadkaA.LaveeS.OrE.2008Similar mechanisms might be triggered by alternative external stimuli that induce dormancy release in grape budsPlanta2287988

    • Search Google Scholar
    • Export Citation
  • HellemansJ.MortierG.De PaepeA.SpelemanF.VandesompeleJ.2007qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR dataGenome Biol.8R19

    • Search Google Scholar
    • Export Citation
  • HenzellR.F.BriscoeM.R.GravettI.1992Improving kiwifruit vine productivity with plant growth regulatorsActa Hort.297345350

  • HuangD.W.ShermanB.T.LempickiR.A.2009Systematic and integrative analysis of large gene lists using DAVID bioinformatics resourcesNat. Protoc.44457

    • Search Google Scholar
    • Export Citation
  • IonescuI.A.MøllerB.L.Sánchez-PérezR.2017aChemical control of flowering timeJ. Expt. Bot.68369382

  • IonescuI.A.López-OrtegaG.BurowM.Bayo-CanhaA.JungeA.GerickeO.MøllerB.L.Sánchez-PérezR.2017bTranscriptome and metabolite changes during hydrogen cyanamide-induced floral bud break in sweet cherryFront. Plant Sci.81233

    • Search Google Scholar
    • Export Citation
  • JacksonJ.E.BepeteM.1995The effect of hydrogen cyanamide (Dormex) on flowering and cropping of different apple cultivars under tropical conditions of sub-optimal winter chillingScientia Hort.60293304

    • Search Google Scholar
    • Export Citation
  • JiménezS.ReighardG.L.BielenbergD.G.2010Gene expression of DAM5 and DAM6 is suppressed by chilling temperatures and inversely correlated with bud break ratePlant Mol. Biol.73157167

    • Search Google Scholar
    • Export Citation
  • JooJ.H.BaeY.S.LeeJ.S.2001Role of auxin-induced reactive oxygen species in root gravitropismPlant Physiol.12610551060

  • KanehisaM.FurumichiM.TanabeM.SatoY.MorishimaK.2017KEGG: New perspectives on genomes, pathways, diseases and drugsNucleic Acids Res.45D353D361

    • Search Google Scholar
    • Export Citation
  • KeilinT.PangX.VenkateswariJ.HalalyT.CraneO.KerenA.OgrodovitchA.OphirR.VolpinH.GalbraithD.OrE.2007Digital expression profiling of a grape-bud EST collection leads to new insight into molecular events during grape-bud dormancy releasePlant Sci.173446457

    • Search Google Scholar
    • Export Citation
  • KobayashiM.OhuraI.KawakitaK.YokotaN.FujiwaraM.ShimamotoK.DokeN.YoshiokaH.2007Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH OxidasePlant Cell1910651080

    • Search Google Scholar
    • Export Citation
  • KurodaH.SugiuraT.ItoD.2002Changes in hydrogen peroxide content in flower buds of japanese pear (Pyrus pyrifolia Nakai) in relation to breaking of endodormancyJ. Jpn. Soc. Hort. Sci.71610616

    • Search Google Scholar
    • Export Citation
  • LangG.A.EarlyJ.D.MartinG.C.DarnellR.L.1987Endo-, para-, and ecodormancy: Physiological terminology and classification for dormancy researchHortScience22371377

    • Search Google Scholar
    • Export Citation
  • LiR.Bonham-SmithP.C.KingJ.2001Molecular characterization and regulation of formate dehydrogenase in Arabidopsis thalianaCan. J. Bot.79796804

    • Search Google Scholar
    • Export Citation
  • LiB.DeweyC.N.2011RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genomeBMC Bioinformatics12323

  • LiszkayA.van der ZalmE.SchopferP.2004Production of reactive oxygen intermediates (O2˙, H2O2, and ˙ OH) by maize roots and their role in wall loosening and elongation growthPlant Physiol.13631143123

    • Search Google Scholar
    • Export Citation
  • MayM.J.VernouxT.LeaverC.MontaguN.V.InzéD.1998Glutathione homeostasis in plants: Implications for environmental sensing and plant developmentJ. Expt. Bot.49649667

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

  • MittlerR.VanderauweraS.GolleryM.Van BreusegemF.2004Reactive oxygen gene network of plantsTrends Plant Sci.9490498

  • MittlerR.VanderauweraS.SuzukiN.MillerG.TognettiV.B.VandepoeleK.GolleryM.ShulaevV.Van BreusegemF.2011ROS signaling: The new wave?Trends Plant Sci.16300309

    • Search Google Scholar
    • Export Citation
  • MittlerR.2017ROS are goodTrends Plant Sci.221119

  • MorantA.V.JørgensenK.JørgensenC.PaquetteS.M.Sánchez-PérezR.MøllerB.L.BakS.2008β-Glucosidases as detonators of plant chemical defensePhytochemistry6917951813

    • Search Google Scholar
    • Export Citation
  • MorganK.OlmsteadM.2013Peach orchard establishment and production planning budgets for FloridaProc. Florida State Hort. Soc.1263542

  • MüllerK.LinkiesA.VreeburgR.A.M.FryS.C.Krieger-LiszkayA.Leubner-MetzgerG.2009In vivo cell wall loosening by hydroxyl radicals during cress seed germination and elongation growthPlant Physiol.15018551865

    • Search Google Scholar
    • Export Citation
  • National Center for Biotechnology Information2018A tool for finding specific primers. 1 Dec. 2018. <http://www.ncbi.nlm.nih.gov/tools/primer-blast/index.cgi?LINK_LOC=BlastHome>

  • NirG.ShulmanY.FanbersteinL.LaveeS.1986Changes in the activity of catalase (EC 1.11.1.6) in relation to the dormancy of grapevine (Vitis vinifera L.) budsPlant Physiol.8111401142

    • Search Google Scholar
    • Export Citation
  • OgasawaraY.KayaH.HiraokaG.YumotoF.KimuraS.KadotaY.HishinumaH.SenzakiE.YamagoeS.NagataK.NaraM.SuzukiK.TanokuraM.KuchitsuK.2008Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylationJ. Biol. Chem.28388858892

    • Search Google Scholar
    • Export Citation
  • OkieW.R.1998Handbook of peach and nectarine varieties: Performance in the southeastern United States and index of names. U.S. Dept. Agr. Washington DC

  • OlmsteadM.ChaparroJ.AndersenP.WilliamsonJ.FergusonJ.2016Florida peach and nectarine varieties. Univ. Florida/Inst. Food Agr. Sci. Ext. Digital Info. Source MG374

  • OlmsteadM.2014Application of hydrogen cyanamide to increase bloom uniformity in low-chill peaches: A preliminary reportProc. Florida State Hort. Soc.1271820

    • Search Google Scholar
    • Export Citation
  • OrE.ViloznyI.EyalY.OgrodovitchA.2000The transduction of the signal for grape bud dormancy breaking induced by hydrogen cyanamide may involve the SNF-like protein kinase GDBRPKPlant Mol. Biol.43483494

    • Search Google Scholar
    • Export Citation
  • OrE.ViloznyI.FennellA.EyalY.OgrodovitchA.2002Dormancy in grape buds: Isolation and characterization of catalase cDNA and analysis of its expression following chemical induction of bud dormancy releasePlant Sci.162121130

    • Search Google Scholar
    • Export Citation
  • PandolfiP.P.SonatiF.RiviR.MasonP.GrosveldF.LuzzattoL.1995Targeted disruption of the housekeeping gene encoding glucose 6-phosphate dehydrogenase (G6PD): G6PD is dispensable for pentose synthesis but essential for defense against oxidative stressEMBO J.1452095215

    • Search Google Scholar
    • Export Citation
  • PerataP.AlpiA.1993Plant responses to anaerobiosisPlant Sci.93117

  • PérezF.J.VergaraR.OrE.2009On the mechanism of dormancy release in grapevine buds: A comparative study between hydrogen cyanamide and sodium azidePlant Growth Regulat.59145152

    • Search Google Scholar
    • Export Citation
  • PfafflM.W.2001A new mathematical model for relative quantification in real-time RT–PCRNucleic Acids Res.29e45

  • PiotrowskiM.SchönfelderS.WeilerE.W.2001The Arabidopsis thaliana isogene NIT4 and its orthologs in tobacco encode β-cyano-L-alanine hydratase/nitrilaseJ. Biol. Chem.27626162621

    • Search Google Scholar
    • Export Citation
  • ReczekC.R.ChandelN.S.2015ROS-dependent signal transductionCurr. Opin. Cell Biol.33813

  • RioD.C.2015Denaturation and electrophoresis of RNA with formaldehydeCold Spring Harb. Protoc.2015306313

  • Rodriguez-AJ.ShermanW.B.ScorzaR.WisniewskiM.OkieW.R.1994‘Evergreen’ peach, its inheritance and dormant behaviorJ. Amer. Soc. Hort. Sci.119789792

    • Search Google Scholar
    • Export Citation
  • RohdeA.BhaleraoR.P.2007Plant dormancy in the perennial contextTrends Plant Sci.12217223

  • RouhierN.2010Plant glutaredoxins: Pivotal players in redox biology and iron–sulphur centre assemblyNew Phytol.186365372

  • SalveminiF.FranzéA.IervolinoA.FilosaS.SalzanoS.UrsiniM.V.1999Enhanced glutathione levels and oxidoresistance mediated by increased glucose-6-phosphate dehydrogenase expressionJ. Biol. Chem.27427502757

    • Search Google Scholar
    • Export Citation
  • ScalabrelliG.VitiR.CinelliF.1991Change in catalase activity and dormancy of apricot buds in response to chillingActa Hort.293267274

  • ScarpeciT.E.ZanorM.I.CarrilloN.Mueller-RoeberB.ValleE.M.2008Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: A focus on rapidly induced genesPlant Mol. Biol.66361378

    • Search Google Scholar
    • Export Citation
  • ShirotaF.N.DemasterE.G.NagasawaH.T.1987Cyanide is a product of the catalase-mediated oxidation of the alcohol deterrent agent, cyanamideToxicol. Lett.37712

    • Search Google Scholar
    • Export Citation
  • ShulmanY.NirG.LaveeS.1986Oxidative processes in bud dormancy and the use of hydrogen cyanamide in breaking dormancyActa Hort.179141148

    • Search Google Scholar
    • Export Citation
  • SiegieńI.BogatekR.2006Cyanide action in plants — From toxic to regulatoryActa Physiol. Plant.28483497

  • SingermanA.Burani-AroucaM.OlmsteadM.2017Establishment and production costs for peach orchards in Florida: Enterprise budget and profitability analysis. Univ. Florida/Inst. Food Agr. Sci. Ext. Digital Info. Source FE1016

  • SudawanB.ChangC.-S.ChaoH.KuM.S.B.YenY.2016Hydrogen cyanamide breaks grapevine bud dormancy in the summer through transient activation of gene expression and accumulation of reactive oxygen and nitrogen speciesBMC Plant Biol.16202

    • Search Google Scholar
    • Export Citation
  • SupekF.BošnjakM.ŠkuncaN.ŠmucT.2011REVIGO summarizes and visualizes long lists of gene ontology termsPLoS One6e21800

  • TaniE.PolidorosA.N.FlemetakisE.StedelC.KalloniatiC.DemetriouK.KatinakisP.TsaftarisA.S.2009Characterization and expression analysis of AGAMOUS-like SEEDSTICK-like and SEPALLATA-like MADS-box genes in peach (Prunus persica) fruitPlant Physiol. Biochem.47690700

    • Search Google Scholar
    • Export Citation
  • ThimmO.BläsingO.GibonY.NagelA.MeyerS.KrügerP.SelbigJ.MüllerL.A.RheeS.Y.StittM.2004MAPMAN: A user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processesPlant J.37914939

    • Search Google Scholar
    • Export Citation
  • TianT.LiuY.YanH.YouQ.YiX.DuZ.XuW.SuZ.2017AgriGO v2.0: A GO analysis toolkit for the agricultural community 2017 updateNucleic Acids Res.45W122W129

    • Search Google Scholar
    • Export Citation
  • TongZ.GaoZ.WangF.ZhouJ.ZhangZ.2009Selection of reliable reference genes for gene expression studies in peach using real-time PCRBMC Mol. Biol.1071

    • Search Google Scholar
    • Export Citation
  • TurrensJ.F.2003Mitochondrial formation of reactive oxygen speciesJ. Physiol.552335344

  • UsadelB.NagelA.ThimmO.RedestigH.BlaesingO.E.Palacios-RojasN.SelbigJ.HannemannJ.PiquesM.C.SteinhauserD.ScheibleW.-R.GibonY.MorcuendeR.WeichtD.MeyerS.StittM.2005Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of corresponding genes, and comparison with known responsesPlant Physiol.13811951204

    • Search Google Scholar
    • Export Citation
  • VanlerbergheG.C.McIntoshL.1997Alternative oxidase: From gene to functionAnnu. Rev. Plant Biol.48703734

  • VerdeI.JenkinsJ.DondiniL.MicaliS.PagliaraniG.VendraminE.ParisR.AraminiV.GazzaL.RossiniL.BassiD.TroggioM.ShuS.GrimwoodJ.TartariniS.DettoriM.T.SchmutzJ.2017The peach v2.0 release: High-resolution linkage mapping and deep resequencing improve chromosome-scale assembly and contiguityBMC Genomics18225

    • Search Google Scholar
    • Export Citation
  • VitiR.BartoliniS.ZanolG.C.2012Biological changes and active oxygen-scavenging enzymes activities in apricot (Prunus armeniaca L.) flower buds during dormancy transitionsActa Hort.940331339

    • Search Google Scholar
    • Export Citation
  • WeinbergerJ.H.1950Chilling requirements of peach varietiesProc. Amer. Soc. Hort. Sci.56122128

  • WilliamsonJ.F.KrewerG.MaustB.E.MillerE.P.2002Hydrogen cyanamide accelerates vegetative budbreak and shortens fruit development period of blueberryHortScience37539542

    • Search Google Scholar
    • Export Citation
  • YamadaK.TakahashiR.FujitaniC.MishimaK.YoshidaM.JoyceD.C.YamakiS.2009Cell wall extensibility and effect of cell-wall-loosening proteins during rose flower openingJ. Jpn. Soc. Hort. Sci.78242251

    • Search Google Scholar
    • Export Citation
  • YamaneH.OokaT.JotatsuH.HosakaY.SasakiR.TaoR.2011Expressional regulation of PpDAM5 and PpDAM6, peach (Prunus persica) dormancy-associated MADS-box genes, by low temperature and dormancy-breaking reagent treatmentJ. Expt. Bot.6234813488

    • Search Google Scholar
    • Export Citation
  • ZhangL.XuY.MaR.2008Molecular cloning, identification, and chromosomal localization of two MADS box genes in peach (Prunus persica)J. Genet. Genomics35365372

    • Search Google Scholar
    • Export Citation
  • ZhuangW.GaoZ.WangL.ZhongW.NiZ.ZhangZ.2013Comparative proteomic and transcriptomic approaches to address the active role of GA4 in japanese apricot flower bud dormancy releaseJ. Expt. Bot.6449534966

    • Search Google Scholar
    • Export Citation

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