Survey of ‘d’Anjou’ Pear Metabolic Profile Following Harvest from Different Canopy Positions and Fruit Tissues

in HortScience

Physiological variability within a large canopy ‘d’Anjou’ tree results from agronomic and environmental factors. Fruit diversity within the canopy was surveyed using metabolic profiling to identify metabolism associated variability within the canopy. Different portions of the same fruit were evaluated to determine future precise sampling protocols for metabolic profiling of pear. We expected that the metabolic profile of the peel and cortex would be diverse and these differences would highlight specific metabolic pathways as influenced by these conditions. Another focus of this work was developing an untargeted metabolic profiling protocol tailored for pear using a combination of extractions coupled with GC-MS and LC-MS analysis. ‘d’Anjou’ pear fruit harvested from two different zones of trees trained to an open vase canopy were maintained at room temperature for 24 days to observe any changes in external phenotype and metabolic profile. Fruit harvested from the internal canopy were greener as also indicated by high Index of Absorbance Difference (IAD) and hue angle values. Metabolic profile differences between tree positions were widespread and included metabolites from many pathways beyond those associated with peel color. In addition, peel metabolic profile was different depending upon the tissue position (top vs. bottom) sampled from the pears. Specific pathways altered by tree position included those potentially linked to fruit quality and ripeness, including malic acid and aroma volatile (V) levels, as well as light environment, such as flavonol glycoside levels. Present results warrant further future work targeting these changes over time during storage and alongside fruit quality analyses to validate the impacts on ripening and tree factors. In addition, outcomes indicate tissue sampling strategies require consistency with respect to the region of the pear fruit sampled for metabolomics.

Contributor Notes

This research was supported by PNW Pear Research Committee, project number: PR14-108A—Improving quality and maturity consistency of ‘d’Anjou’.Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the Washington State University and PNW Pear Research Committee.D.R.R., S.S., N.S., J.P.M., and S.M. substantially contributed to the conception, design of the work, to the acquisition, analysis, or interpretation of data for the work; to drafting the work or revising it critically for important intellectual content; to final approval of the version to be published. All authors are in agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Corresponding author. E-mail: stefano.musacchi@wsu.edu.

  • AckermannJ.FischerM.AmadoR.1992Changes in sugars, acids, and amino acids during ripening and storage of apples (cv. Glockenapfel)J. Agr. Food Chem.40711311134

    • Search Google Scholar
    • Export Citation
  • AliK.MalteseF.FortesA.M.PaisM.S.ChoiY.H.VerpoorteR.2011Monitoring biochemical changes during grape berry development in Portuguese cultivars by NMR spectroscopyFood Chem.124417601769

    • Search Google Scholar
    • Export Citation
  • ArgentaL.C.FanX.MattheisJ.P.2003Influence of 1-methylcyclopropene on ripening, storage life, and volatile production by d’Anjou cv. pear fruitJ. Agr. Food Chem.511338583864

    • Search Google Scholar
    • Export Citation
  • AubertC.MilhetC.2007Distribution of the volatile compounds in the different parts of a white-fleshed peach (Prunus persica L. Batsch)Food Chem.1021375384

    • Search Google Scholar
    • Export Citation
  • BréhélinC.KesslerF.2008The plastoglobule: A bag full of lipid biochemistry tricksPhotochem. Photobiol.8413881394

  • BonoraE.StefanelliD.CostaG.2013Nectarine fruit ripening and quality assessed using the index of absorbance differenceIntl. J. Agron.doi:10.1155/2013/242461

    • Search Google Scholar
    • Export Citation
  • CaldanaC.DegenkolbeT.Cuadros-InostrozaA.KlieS.SulpiceR.LeisseA.SteinhauserD.FernieA.R.WillmitzerL.HannahM.A.2011High-density kinetic analysis of the metabolomic and transcriptomic response of Arabidopsis to eight environmental conditionsPlant J.675869884

    • Search Google Scholar
    • Export Citation
  • Carreno-QuinteroN.BouwmeesterH.J.KeurentjesJ.J.2013Genetic analysis of metabolome–phenotype interactions: From model to crop speciesTrends Genet.2914150

    • Search Google Scholar
    • Export Citation
  • ChenL.S.ChengL.2007The sun-exposed peel of apple fruit has a higher photosynthetic capacity than the shaded peelFunct. Plant Biol.341110381048

    • Search Google Scholar
    • Export Citation
  • ChenP.M.MellenthinW.M.1981Effects of harvest date on ripening capacity and postharvest life of ‘d’Anjou’ pearsJ. Amer. Soc. Hort. Sci.1063842

    • Search Google Scholar
    • Export Citation
  • CostaG.NoferiniM.FioriG.TorrigianiP.2009Use of Vis/NIR spectroscopy to assess fruit ripening stage and improve management in post-harvest chainGBS J. Fresh Produce33541

    • Search Google Scholar
    • Export Citation
  • CostaG.NoferiniM.2013Use of non-destructive devices as a decision support system for fruit quality enhancementActa Hort.998103116

  • DoerflingerF.C.MillerW.B.NockJ.F.WatkinsC.B.2015Relationships between starch pattern indices and starch concentrations in four apple cultivarsPostharvest Biol. Technol.1108695

    • Search Google Scholar
    • Export Citation
  • Eccher ZerbiniP.2002The quality of pear fruitActa Hort.596805810

  • FarhoomandM.B.PattersonM.E.ChuC.L.1977The ripening pattern of ‘Delicious’ apples in relation to position on the treeJ. Amer. Soc. Hort. Sci.102771774

    • Search Google Scholar
    • Export Citation
  • FelicettiD.A.SchraderL.E.2009aChanges in pigment concentrations associated with sunburn browning of five apple cultivars. I. Chlorophylls and carotenoidsPlant Sci.1767883

    • Search Google Scholar
    • Export Citation
  • FelicettiD.A.SchraderL.E.2009bChanges in pigment concentrations associated with sunburn browning of five apple cultivars. II. PhenolicsPlant Sci.1768489

    • Search Google Scholar
    • Export Citation
  • FellmanJ.K.RudellD.R.MattinsonD.S.MattheisJ.P.2003Relationship of harvest maturity to flavor regeneration after CA storage of ‘Delicious’ applesPostharvest Biol. Technol.273951

    • Search Google Scholar
    • Export Citation
  • FiehnO.2002Metabolomics–the link between genotypes and phenotypesPlant Mol. Biol.481–2155171

  • FischerT.C.GoschC.PfeifferJ.HalbwirthH.HalleC.StichK.ForkmannG.2007Flavonoid genes of pear (Pyrus communis)Trees (Berl.)215521529

    • Search Google Scholar
    • Export Citation
  • GagliardiF.SerraS.AncaraniV.BucciD.PiccininiL.NoferiniM.MusacchiS.CostaG.2014Preliminary results on CV.‘Abbé Fétel’ productivity and fruit quality in relation to tree architectureActa Hort.1058151158

    • Search Google Scholar
    • Export Citation
  • GomezK.A.GomezA.A.1984Statistical procedures for agricultural research. Wiley New York NY

  • GuadagniD.G.BombenJ.L.HudsonJ.S.1971Factors influencing the development of aroma in apple peelsJ. Sci. Food Agr.22110115

  • HiwasaK.KinugasaY.AmanoS.HashimotoA.NakanoR.InabaA.KuboY.2003Ethylene is required for both the initiation and progression of softening in pear (Pyrus communis L.) fruitJ. Expt. Bot.54383771779

    • Search Google Scholar
    • Export Citation
  • JajoA.RahimM.A.SerraS.GagliardiF.JajoN.K.MusacchiS.CostaG.BonghiC.TrainottiL.2014Impact of tree training system, branch type and position in the canopy on the ripening homogeneity of ‘Abbé Fétel’ pear fruitTree Genet. Genomes10514771488

    • Search Google Scholar
    • Export Citation
  • JenningsW.G.CrevelingR.K.HeinzD.E.1964Volatile esters of Bartlett pear. IV. Esters of trans-2,cis-4-decadienoic acidJ. Food Sci.29730734

    • Search Google Scholar
    • Export Citation
  • KappelF.NeilsenG.H.1994Relationship between light microclimate, fruit growth, fruit quality, specific leaf weight and N and P content of spur leaves of ‘Bartlett’ and ‘Anjou’ pearSci. Hort.593–4187196

    • Search Google Scholar
    • Export Citation
  • KhemiraH.LombardP.B.SugarD.AzarenkoA.N.1993Hedgerow orientation affects canopy exposure, flowering, and fruiting of ‘Anjou’ pear treesHortScience28984987

    • Search Google Scholar
    • Export Citation
  • KingstonC.M.1993Maturity indices for apple and pearHort. Rev.13407439

  • KneeM.1971Anthocyanin, carotenoid, and chlorophyll changes in the peel of Cox’s Orange Pippin apples during ripening on and off the treeJ. Expt. Bot.23184196

    • Search Google Scholar
    • Export Citation
  • LalelH.J.D.SinghZ.TanS.C.2003Distribution of aroma volatile compounds in different parts of mango fruitJ. Hort. Sci. Biotechnol.782131138

    • Search Google Scholar
    • Export Citation
  • LeeJ.MattheisJ.P.RudellD.R.2012aAntioxidant treatment alters metabolism associated with internal browning in ‘Braeburn’ apples during controlled atmosphere storagePostharvest Biol. Technol.683242

    • Search Google Scholar
    • Export Citation
  • LeeJ.RudellD.R.DaviesP.J.WatkinsC.B.2012bMetabolic changes in 1-methylcyclopropene (1-MCP)-treated ‘Empire’ apple fruit during storageMetabolomics8742753

    • Search Google Scholar
    • Export Citation
  • Le LezecM.BelouinA.1994Test de regression de l’amidon des poiresArboriculture Fruitiere4743435

  • LeissoR.S.BuchananD.A.LeeJ.MattheisJ.P.SaterC.HanrahanI.HertogM.L.2015Chilling-related cell damage of apple (Malus ×domestica Borkh.) fruit cortical tissue impacts antioxidant, lipid and phenolic metabolismPhysiol. Plant.1532204220

    • Search Google Scholar
    • Export Citation
  • LeissoR.S.GapperN.E.MattheisJ.P.SullivanN.L.WatkinsC.B.GiovannoniJ.J.SchafferR.J.JohnstonJ.W.HanrahanI.HertogM.L.NicolaïB.M.2016Gene expression and metabolism preceding soft scald, a chilling injury of ‘Honeycrisp’ apple fruitBMC Genomics171798

    • Search Google Scholar
    • Export Citation
  • LombardoV.A.OsorioS.BorsaniJ.LauxmannM.A.BustamanteC.A.BuddeC.O.DrincovichM.F.2011Metabolic profiling during peach fruit development and ripening reveals the metabolic networks that underpin each developmental stagePlant Physiol.157416961710

    • Search Google Scholar
    • Export Citation
  • MaF.ChengL.2003The sun-exposed peel of apple fruit has higher xanthophyll cycle-dependent thermal dissipation and antioxidants of the ascorbate–glutathione pathway than the shaded peelPlant Sci.165819827

    • Search Google Scholar
    • Export Citation
  • McGuireR.1992Reporting of objective color measurementsHortScience2712541255

  • MerzlyakM.N.SolovchenkoA.E.2002Photostability of pigments in ripening apple fruit: A possible photoprotective role of carotenoids during plant senescencePlant Sci.1634881888

    • Search Google Scholar
    • Export Citation
  • MerzlyakM.N.MeløT.B.NaqviK.R.2008Effect of anthocyanins, carotenoids, and flavonols on chlorophyll fluorescence excitation spectra in apple fruit: Signature analysis, assessment, modelling, and relevance to photoprotectionJ. Expt. Bot.59349359

    • Search Google Scholar
    • Export Citation
  • MesaK.SerraS.MasiaA.GagliardiF.BucciD.MusacchiS.2016Seasonal trends of starch and soluble carbohydrates in fruits and leaves of ‘Abbé Fétel’ pear trees and their relationship to fruit quality parametersSci. Hort.2116069

    • Search Google Scholar
    • Export Citation
  • MocoS.BinoR.J.VorstO.VerhoevenH.A.de GrootJ.van BeekT.A.De VosC.R.2006A liquid chromatography-mass spectrometry-based metabolome database for tomatoPlant Physiol.141412051218

    • Search Google Scholar
    • Export Citation
  • NashimaK.ShimizuT.NishitaniC.YamamotoT.TakahashiH.NakazonoM.MatsumotoS.2013Microarray analysis of gene expression patterns during fruit development in European pear (Pyrus communis)Sci. Hort.164466473

    • Search Google Scholar
    • Export Citation
  • NeriD.SaviniG.MassetaniF.GiorgiV.SabbatiniP.2008Pear pruning and training for economically sustainable productionActa Hort.800747754

    • Search Google Scholar
    • Export Citation
  • Núñez-DelicadoE.Serrano-MegíasM.Pérez-LópezA.J.López-NicolásJ.M.2005Polyphenol oxidase from Dominga table grapeJ. Agr. Food Chem.5360876093

    • Search Google Scholar
    • Export Citation
  • OikawaA.OtsukaT.NakabayashiR.JikumaruY.IsuzugawaK.MurayamaH.ShiratakeK.2015Metabolic profiling of developing pear fruits reveals dynamic variation in primary and secondary metabolites, including plant hormonesPLoS One107e0131408

    • Search Google Scholar
    • Export Citation
  • OleszekW.AmiotM.J.AubertS.Y.1994Identification of some phenolics in pear fruitJ. Agr. Food Chem.42612611265

  • Oms-OliuG.Odriozola-SerranoI.Martin-BellosoO.2012Using metabolomics to improve the quality of postharvest fruit p. 207–214. In: D. Hemming (ed.). Plant sciences reviews 2012. CABI UK

  • PalmerJ.W.1988Annual dry matter production and partitioning over the first 5 years of a bed system of Crispin/M. 27 apple trees at four spacingsJ. Appl. Ecol.252569578

    • Search Google Scholar
    • Export Citation
  • PechJ.C.BouzayenM.LatchéA.2014Cellular metabolic and molecular aspects of chromoplast differentiation in ripening fruit p. 28–47. In: P. Nath M. Bouzayen A.K. Mattoo and J.C. Pech (eds.). Fruit ripening: Physiology signaling and genomics. CABI UK

  • PedreschiR.FranckC.LammertynJ.ErbanA.KopkaJ.HertogM.VerlindenB.NicolaïB.2009Metabolic profiling of ‘Conference’ pears under low oxygen stressPostharvest Biol. Technol.512123130

    • Search Google Scholar
    • Export Citation
  • PicchioniG.A.WatadaA.E.ConwayW.S.WhitakerB.D.SamsC.E.1995Phospholipid, galactolipid, and steryl lipid composition of apple fruit cortical tissue following postharvest CaCl2 infiltrationPhytochemistry39763769

    • Search Google Scholar
    • Export Citation
  • PluskalT.CastilloS.Villar-BrionesA.OresicM.2010MZmine 2: Modular frame- work for processing, visualizing, and analyzing mass spectrometry-based molecular profile dataBMC Bioinformatics111395405

    • Search Google Scholar
    • Export Citation
  • RaffoM.D.PonceN.M.SozziG.O.VicenteA.R.StortzC.A.2011Compositional changes in ‘Bartlett’ pear (Pyrus communis L.) cell wall polysaccharides as affected by sunlight conditionsJ. Agr. Food Chem.59221215512162

    • Search Google Scholar
    • Export Citation
  • ReuscherS.IsuzugawaK.KawachiM.OikawaA.ShiratakeK.2014Comprehensive elemental analysis of fruit flesh from European pear ‘La France’ and its giant fruit bud mutant indicates specific roles for B and Ca in fruit developmentSci. Hort.176255260

    • Search Google Scholar
    • Export Citation
  • ReuscherS.FukaoY.MorimotoR.OtagakiS.OikawaA.IsuzugawaK.ShiratakeK.2016Quantitative proteomics based reconstruction and identification of metabolic pathways and membrane transport proteins related to sugar accumulation in developing fruits of pear (Pyrus communis)Plant Cell Physiol.573505518

    • Search Google Scholar
    • Export Citation
  • RobinsonC.MantA.2009Biogenesis of the thylakoid membraneAnnu. Plant Rev.13180331

  • RudellD.R.MattinsonD.S.MattheisJ.P.FellmanJ.K.2000The progression of ethylene production and respiration in the tissues of ripening ‘Fuji’ apple fruitHortScience3513001303

    • Search Google Scholar
    • Export Citation
  • RudellD.R.MattheisJ.P.FellmanJ.K.2005Relationship of superficial scald development and α-farnesene oxidation to reactions of diphenylamine and diphenylamine derivatives in cv. Granny Smith apple peelJ. Agr. Food Chem.5383828389

    • Search Google Scholar
    • Export Citation
  • RudellD.R.MattheisJ.P.CurryE.A.2008Prestorage ultraviolet−white light irradiation alters apple peel metabolomeJ. Agr. Food Chem.56311381147

    • Search Google Scholar
    • Export Citation
  • RudellD.R.MattheisJ.P.2009Superficial scald development and related metabolism is modified by postharvest light irradiationPostharvest Biol. Technol.512174182

    • Search Google Scholar
    • Export Citation
  • RudellD.R.MattheisJ.P.HertogM.L.2009Metabolomic change precedes apple superficial scald symptomsJ. Agr. Food Chem.5784598466

  • RudellD.R.BuchananD.A.LeissoR.S.WhitakerB.D.MattheisJ.P.ZhuY.VaranasiV.2011Ripening, storage temperature, ethylene action, and oxidative stress alter apple peel phytosterol metabolismPhytochemistry7213281340

    • Search Google Scholar
    • Export Citation
  • SchraderL.E.ZhangJ.SunJ.XuJ.ElfvingD.C.KahnC.2009Postharvest changes in internal fruit quality in apples with sunburn browningJ. Amer. Soc. Hort. Sci.1341148155

    • Search Google Scholar
    • Export Citation
  • ShiotaH.1990Changes in the volatile composition of La France pear during maturationJ. Sci. Food Agr.52421429

  • SolovchenkoA.Schmitz-EibergerM.2003Significance of skin flavonoids for UV B-protection in apple fruitsJ. Expt. Bot.5419771984

  • SolovchenkoA.E.AvertchevaO.V.MerzlyakM.N.2006Elevated sunlight promotes ripening-associated pigment changes in apple fruitPostharvest Biol. Technol.40183189

    • Search Google Scholar
    • Export Citation
  • SpanosG.A.WrolstadR.E.1992Phenolics of apple, pear, and white grape juices and their changes with processing and storage. A reviewJ. Agr. Food Chem.40914781487

    • Search Google Scholar
    • Export Citation
  • StewartD.McDougallG.J.SungurtasJ.VerrallS.GrahamJ.MartinussenI.2007Metabolomic approach to identifying bioactive compounds in berries: Advances toward fruit nutritional enhancementMol. Nutr. Food Res.516645651

    • Search Google Scholar
    • Export Citation
  • SunY.QianM.WuR.NiuQ.TengY.ZhangD.2014Postharvest pigmentation in red Chinese sand pears (Pyrus pyrifolia Nakai) in response to optimum light and temperaturePostharvest Biol. Technol.916471

    • Search Google Scholar
    • Export Citation
  • TorresC.A.SepulvedaA.Gonzalez-TaliceJ.YuriJ.A.RazmilicI.2013Fruit water relations and osmoregulation on apples (Malus domestica Borkh.) with different sun exposures and sun-injury levels on the treeSci. Hort.161143152

    • Search Google Scholar
    • Export Citation
  • TreutterD.2005Significance of flavonoids in plant resistance and enhancement of their biosynthesisPlant Biol.76581591

  • WhitakerB.D.1991Growth conditions and ripening influence plastid and microsomal membrane lipid composition in bell pepper fruitJ. Amer. Soc. Hort. Sci.116525533

    • Search Google Scholar
    • Export Citation
  • WoldS.1994PLS for multivariate linear modeling. In: H. Van de Watterbeemd (ed.). QSAR: Chemometric methods in molecular design. Methods and principles in medicinal chemistry. Verlag-Chemie Weinheim Germany

  • WorkmanM.1963Color and pigment changes in Golden Delicious and Grimes Golden applesJ. Amer. Soc. Hort. Sci.83149161

  • WünscheJ.N.LaksoA.N.RobinsonT.L.LenzF.DenningS.S.1996The bases of productivity in apple production systems: The role of light interception by different shoot typesJ. Amer. Soc. Hort. Sci.121886893

    • Search Google Scholar
    • Export Citation
  • ZhangJ.WangX.YuO.TangJ.GuX.WanX.FangC.2010Metabolic profiling of strawberry (Fragaria ×ananassa Duch.) during fruit development and maturationJ. Expt. Bot.623116

    • Search Google Scholar
    • Export Citation
  • ZhangJ.SerraS.LeissoR.S.MusacchiS.2016Effect of light microclimate on the quality of ‘d’Anjou’ pears in mature open-centre tree architectureBiosyst. Eng.141111

    • Search Google Scholar
    • Export Citation
  • ZiosiV.NoferiniM.FioriG.TadielloA.TrainottiL.CasadoroG.CostaG.2008A new index based on vis spectroscopy to characterize the progression of ripening in peach fruitPostharvest Biol. Technol.49319329

    • Search Google Scholar
    • Export Citation
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