Involvement of phenolic compounds in the susceptibility of ... · PDF filediseases, namely...

BASE Biotechnol. Agron. Soc. Environ.201216(3),393-404 Focus on:

Involvementofphenoliccompoundsinthesusceptibilityofbananastocrownrot.AreviewCécileAnnieEwané(1,3,4),PhilippeLepoivre(1),LucdeLapeyredeBellaire(2),LudivineLassois(1)(1)Univ.Liege-GemblouxAgro-BioTech.PlantPathologyUnit.AvenueMaréchalJuin,13.B-5030Gembloux(Belgium).E-mail:[email protected](2)CIRAD.ResearchUnitBanana,PlantainandPineappleCroppingSystems.TAB-26/PS4(Bur.108).BoulevarddelaLironde.F-34398MontpellierCedex5(France).(3)CARBAP.AfricanResearchCenteronBananasandPlantains.PlantPathologyUnit.P.O.Box832.CAM-Douala(Cameroon).(4)UniversityofYaoundeI.FacultyofSciences.DepartmentofBiochemistry.P.O.Box812.CAM-Yaounde(Cameroon).

ReceivedonJune22,2011;acceptedonMarch6,2012.

Crownrotofbananas,causedbyafungalparasiticcomplex,isoneofthemainqualitydefectsofexportedbananas.Majorvariationsinthesusceptibilityofbananastocrownrothavebeenobservedindifferentproductionzones.Thephysiologicalstateofthebananafruitatharvestissaidtoinfluenceitsresponsetopathogenicattackandthustomodulateitssusceptibilitytocrownrot.Thesusceptibilityofbananastothisdisease,however,appearstobeinfluencedbymanypre-harvestfactors,althoughtheunderlyingdefensemechanismshavenotbeenclearlyidentified.Arecentreportbasedonmolecularanalysessuggeststhatphenoliccompoundsmightbeinvolvedinthedifferentvariationsinthesusceptibilityofbananastocrownrot.Resultsofotherearlierstudiespointtoaninvolvementofphenoliccompoundsinthedefensivereactionsofbananaplantsagainstvariouspathogens.Thepresentpaperreviewsthecurrentstateofknowledgeonthevariationsinthesusceptibilityofbananastocrownrotandtakesstockofwhatisknownaboutphenoliccompoundsinrelationtotheirpotentialinvolvementinthedefensemechanismsofthebananaplant.Keywords.Bananas,fruitsusceptibility,crown,rots,defensemechanisms,phenoliccompounds.

Implication des composés phénoliques dans la sensibilité des bananes à la pourriture de couronne (synthèse bibliographique). La pourriture de couronne des bananes provoquée par un complexe parasitaire fongique est l’un desprincipauxdéfautsdequalitédesbananesd’exportation.Desvariationsdesensibilitéimportantesdesbananesàlapourrituredecouronneontétéobservéesdansdifférenteszonesdeproduction.Ilaétésuggéréquel’étatphysiologiquedufruità larécolte influence la réponse des bananes à l’attaque desmicro-organismes pathogènes etmodule ainsi sa sensibilité à lapourrituredecouronne.Lasensibilitédesbananesàlapourrituredecouronneestinfluencéeparplusieursfacteurspré-récolte,bienquelesmécanismesdedéfensesous-jacentsn’aientpasétéclairementidentifiés.Récemment,uneétudebaséesurdesanalysesmoléculairesasuggéréquelescomposésphénoliquespouvaientêtrepotentiellementimpliquésdanslesvariationsdesensibilitésdesbananesauxpourrituresdecouronne.D’autresétudesantérieuresavaientdéjàsuggéré l’implicationdecomposés phénoliques dans les réactions de défense du bananier contre diverses attaques de pathogènes. Cette étude seproposedefairel’étatdel’artsurlesvariationsdesensibilitédesbananesàlapourrituredecouronne,etdefairelepointsurlescomposésphénoliquesetleurimplicationpotentielledanslesmécanismesdedéfensedubananier.Mots-clés.Banane,sensibilitédufruit,pourrituredecouronne,mécanismededéfense,composésphénoliques.

1. INTRODUCTION

Banana iscultivated inmore than120countriesoverabout10millionhectares.Itranksfirstinglobalfruitproduction with just over 106million tons being

produced annually worldwide. Cropping systemsaround the world are diverse and production targetsincludesubsistence,saleinlocalornationalmarkets,and international export. Some bananas, such asplantains, can be cooked, while others are classified

394 Biotechnol. Agron. Soc. Environ. 201216(3),393-404 EwanéC.A.,LepoivrePh.etal.

as “dessert” bananas. Dessert bananas for exportbelongexclusivelytotheCavendishsubgroupandaresubjectedtoanimportantinternationaltrade(Loeillet,2005). Banana is currently, in terms of volume, thefirstexportedfruitandrankssecondaftercitrusfruitsin terms of value. Total world exports of banana in2006accountedfor16.8milliontons(FAOSTATdata,2006).Thusthebananaindustryisofvitalimportancetobanana-producingcountries.

Banana trees and fruits are susceptible to attackby several diseases, including twomain post-harvestdiseases,namelybananaanthracnoseandcrownrot.InCameroon,themainqualitydefectthataffectsexportedbananaiscrownrot.Thisdiseaseiscausedbyabroadunspecificandopportunisticfungalparasiticcomplex.Fruit contamination can occurwithin the field but itmostlyoccursinthewashingtanksatthepackingstationwhereprocessingfavorsthepenetrationofpathogensinto the crown tissues. The banana crowns, whichwere healthy at harvest, will then develop a fungalinfection after a fewdays of shipping.Upon arrival,the quality of the banana fruits does not allow themtohaveagoodposition in theEuropeanmarket,andthissometimesconstitutesablowtoexports.Theuseofsyntheticfungicidestocontrolbananatreediseasesand post-harvest diseases is systematic. However,this approach is not satisfactory and is increasinglybeing criticized for the amounts of chemicals used,which couldbeharmful to humans aswell as to theenvironment. Consequently, several approaches havebeendevelopedinrecentyears tofindalternatives tochemicalcontrol.

Variations have been noticed in the developmentof crown rot disease partly related to environmentalconditionsduringgrowth.Theoccurrenceofcrownrotthereforedependsfirstly,onthelevelofsusceptibilityofthebananafruittobeinginfluencedphysiologicallybyenvironmentalconditionsduringgrowthandsecondly,onthelevelofcontamination.Occurrenceofcrownrotalsodependson theamountofdefensivecompounds(phenolics)accumulatedinfruittissuesfromfloweringto harvest to fight pathogenic infections. Indeed,plant defense strategies involve the combinationof several structural and biochemical mechanisms,including accumulated phenolic compounds andlignin-likepolymers.However,with thecurrent stateof knowledge, it is extremely difficult to determinethe mechanism responsible for the variability in thesusceptibilityofthefruittocrownrot.

Up-to-date information will be presented belowboth on pre-harvest factors that influence thesusceptibility of bananas to crown rot (especiallybioticandabiotic factors)andon the involvementofphenolic compounds inplantdefensemechanisms inrelation to environmental conditions that support theplant’sgrowth.

2. BANANA CROWN ROT

Exportedbananasaresubjectedtovariousphytosanitaryconstraints throughout the production chain andthese alter fruit marketability. Crown rot disease inparticular causesmajordamageandeconomic lossesin most banana-producing countries (Krauss et al.,2000).Lossesofmore than86%havebeen reportedfornon-chemically-treatedbananasexportedfromthePhilippines(Alvindiaetal.,2000).

2.1. Crown rot disease

Crown rot is a disease of the tissue uniting thepeduncles.Itoccurswhenbananahandsaredetachedfromtheircentralaxis,calledthestalk.Bananahandsarecutinclustersof5-7fruits,causingtheexposureofwoundedcrowntissuestofungalinfection(Muirheadet al.,2000).Fungalcolonizationof thecrownstartsafterwards,andthedegenerationofthefruitsdoesnotrequirehighlyspecializedparasites.Indeed,crownrotisacomplexinfection,whichresultsfromtheactivityof several microorganisms, of whichColletotrichum musae is themost pathogenic species (Finlay et al.,1993; Krauss et al., 2000; Muirhead et al., 2000;Lassoiset al.,2010a).The infection is,however,notvisible when the bananas are placed in commercialboxesandthefirstsymptomsdonotappearuntilaftera fewdays of shipping.The disease evolves quicklyduringripening.Therotisinitiallysuperficialandlaterprogressesintothetissues.Insomecases,itcaninvadethepedunclesandlaterthefruits(Figure 1).Themaineffectsonfruitqualityareseeninrotteningandintheinduction of early ripening during shipping becauseof the ethylene that is released, either by stressedtissues and necrosed fruits or by fungal mycelium.Whencrownrotisfrequentlyobservedinbananasofaspecificorigin,productionofbananasfromthisoriginmaybeexcludedfromthemarket.

Crown rot disease is currently controlled by thesystematic use of post-harvest fungicidal treatments.Thisapproach,however,hasseveraldrawbacks:– theeffectivenessoffungicidesdependsonthetime ofyearthattheyareappliedandontheproduction area;– the frequent appearance of fungicide-resistant strainspreventscompletediseasecontrol;– the fungicidal slurries rejected around packing stations after post-harvest treatment of banana crownsmaycauseenvironmentalpollution.

Inaddition,thesepost-harvestchemicalsanitationtreatments may have wider-reaching effects, withchemical exposure affecting workers at the packingstations,andevenconsumers.Evidenceofthepossibleeffect on consumers can be seen in the fungicidal

Phenoliccompoundsandbananacrownrotsusceptibility 395

residues regularly detected on banana peel and alsoin the pulp. These drawbacks have led to researchfocusingonalternativecontrolmethods.

2.2. Susceptibility of bananas to crown rot

Variations in disease incidence. Geographical andseasonalvariationshavebeenobservedintheincidenceofcrownrotdisease(Lukezicetal.,1967;Shillingford,1978;Kraussetal.,2000;Lassoisetal.,2008).InastudyconductedinHonduras,Lukezicetal.(1967)showedthattheincidenceofthediseasevariedinthecourseoftheyear,beinghigherinsummerandlowerduringthecolderperiod.Theyalsofound thesevariations tobeunrelatedtovariationsintheparasiticcomplexisolatedfrombananacrowns.Similarly,inJamaica,highlevelsof disease incidence were found to correlate withperiodsofhightemperature(Shillingford,1978).Ithasbeenhypothesizedthatsuchspatiotemporalfluctuationsin disease incidence could reflect the variations inthequalitypotentialof thefruit,acquiredin thefield(Lassois et al., 2010a). This quality potential wouldinclude two components, which would themselvesdependontheagrotechnicalandpedoclimaticfactorsprevailing during the growth phase of the bananaplant. The first of these components is parasitic andthesecond isphysiological.Theparasiticcomponentreflectsthelevelofcrowncontaminationbythefungalcomplex and the pathogenicity of this complex.Thephysiological component, for its part, reflects thefruit’sresponsetopathogenicattack,whichisrelatedto the physiological state of the fruit at harvest, andthisstatemodulatesthefruit’ssusceptibilitytocrownrot.

Variations in the level of fruit susceptibility. Recently, it has been shown that several pre-harvestfactorsinfluencethesusceptibilityofbananastocrownrot. These factors are: geographical and seasonalvariations; bunch age; source-sink ratio; and bioticstressfactors.

Geographical variation. A multilocal study carriedoutinCameroonoverayearshowedlessercrownrotdevelopmentathigheraltitude(500m) thanat loweraltitude(80m)(Ewané,personalcommunication).

Seasonal variation.Intheirstudy,Lassoisetal.(2008)showed that the levelof fruit susceptibility to crownrotdiseasewasvariableovera10-weekperiodinthesamebananaplotinGuadeloupe.ThemultilocalstudycarriedoutinCameroonsuggestedthatfruitsharvestedduringtherainyseasonmightbemoresusceptibletocrownrot thanthoseharvestedduringthedryseason(Ewané,personalcommunication).

Bunch age and source-sink (So-Si) ratio.Awithin-bunchgradientoffruitissusceptibletocrownrot.Thefirsthands to initiatearemoresusceptible than thosethat initiate last (Lassois et al., 2010a).On theotherhand, the So-Si ratio of the banana tree during itsgrowthphasealsohasasignificant influenceonfruitsusceptibility (handsbeing regardedas the sinksandleavesasthesources).Whenthetotalsinkisdecreasedby the removal of banana hands from the bunch,the fruit’s susceptibility to crown rot also decreases.Moreover, a linear relationship between fruit ageand fruit susceptibility to crown rot has also beendemonstratedinGuadeloupe,theoldestfruitsbeingthemostsusceptible(Forret,2008).

Biotic stress factors.TheincidenceofMycosphaerellaleaf spot disease also has an influence on crownrot disease, which is generated by host-pathogeninteraction(Ewané,personalcommunication).

Among the great diversity of reactions andproductsinvolvedinplantdefenseresponses,phenoliccompoundshavebeenrepeatedlyproposedaspotentialparticipants in banana tree defense mechanisms(Beverragi et al., 1995; El Hadrami, 1997; Valetteetal.,1998;Collingbornetal.,2000;Kanazawaetal.,2000;Someyaetal.,2002;deAscensaoetal.,2003;Wuytsetal.,2007;Kavinoetal.,2009).Arecentreport

Figure 1.Bananacrownrot—La pourriture de couronne des bananes.

a:necrosedfruitclusters—bouquets de fruits nécrosés;b:internalnecrosis—nécrose interne;c:necrosisspreadtopedunclesandfingers—progression de la nécrose sur les pédoncules et les doigts.

a b c


suggested that thesecompoundsmight contribute todeterminingthestrengthoftheresponseofbananastocrownrot(Lassoisetal.,2011).

3. PHENOLIC COMPOUNDS

Phenoliccompoundsarethemoststudiedsecondarymetabolitesbecauseoftheirconsiderableinvolvementinplant-environmentinteractions.Theyaremoleculesbelongingtoverydiversechemicalfamilieshavingincommonanaromaticringbearingatleastonephenolhydroxyl substituent. Some phenolic compoundshaveseveralhydroxylgroupsubstituents,whichcanundergo esterification,methylation, etherification orglycosylationreactions(Ravenetal.,2003;Macheixet al., 2005; Lattanzio et al., 2006). The molecularweight of phenolic compounds is variable, beinglower in simple compounds, higher in those withcomplex structures, and higher still in polymerizedtannins.

3.1. Classes of phenolic compounds

Phenoliccompoundsareclassifiedaccordingto:– the nature and complexity of the carbonaceous skeleton;– the degree of skeletal modification (degree of oxidation,hydroxylation,methylation,etc.);– thelinkbetweenthebaseunitandothermolecules suchascarbohydrates, lipids,proteins,orthelink toothersecondarymetabolites,possiblypolyphenols (Macheixetal.,2005).

The phenolic compounds of plants include thesimplestforms(hydroxybenzoicandhydroxycinnamicacids),condensedforms(tannins),andformsrelatedto non-phenolic macromolecules (certain glucidiccomponents of the pecto-cellulosic wall, cutin andsuberin). Only two groups of phenolic compoundsare mainly related to the plant walls: firstly, low-molecular-weight hydroxycinnamic acids related tovarious cellwall compounds, and secondly, lignins,which are polymers of monolignol units bound byoxidativecoupling(Figure 2).

Simple phenols (C6). Thesearecompoundswithone(monophenol-likecatechin)orseveralphenolicgroups(di, tri- and oligophenols): phenol, benzoquinone,pyrogallol,pyrocathecol,etc.(Lattanzioetal.,2006).

Phenolic acids (C6-C1 or C6-C3).Thesearebenzoicorhydroxybenzoicacids (gallicacid,ellagicacid),andcinnamic or hydroxycinnamic acids such as caffeic,coumaric, ferulic, and chlorogenic acid (Manachet al., 2004; Macheix et al., 2005; Lattanzio et al.,

2006).Agroupofsmallphenolicmoleculesisderivedfrom the subclass of hydroxycinnamic acids and iscalledphenylpropenes.

Flavonoids (C6-C3-C6). These are present in plantvacuoles, where they are sometimes water-solubleor sometimes act as pigments (Raven et al., 2003).Flavonoidsarethemostabundantphenoliccompoundsinnatureandareclassifiedaccordingtothedegreeofoxidation and unsaturation of their heterocyclic ring(Scalbertetal.,2000).Twoclassesofflavonoidscanbedistinguished:4-oxoflavonoidsandanthocyanidins(Manachetal.,2004).

Lignins (C6-C3)n. These are extremely complexphenolic polymers.Of the biopolymers, lignins ranksecond in abundance after cellulose. The synthesisof thesecompoundsresults froma three-dimensionalpolymerization of three basic phenolic molecules(called monolignols): coumarylic, coniferylic andsinapylic alcohol, corresponding respectively top-coumaric, ferulic and sinapic acid (Macheix et al.,2005). The complexity of lignins results from thepotentialassociationoftheseunitsviavariouschemicalbonds,inamannerthatisneitherorderednorrepetitive,soastogenerateanamorphous,hydrophobicpolymer.

Tannins (C6-C3-C6)n. These are found in severalformswithdifferent typesofchemical reactivityandcomposition:water-solubletannins,condensedtannins,catechic tannins and proanthocyanidins (Macheixetal.,2005).Proanthocyanidinshaveahighmolecularweightandareagroupofcondensed(chaindimersoroligomers)flavan-3-olsoftenrelatedtocellwalls.

The variability of phenolic compound classesin plants is farmore complex than presented above.Thisisonlyintendedtofamiliarizethereaderwiththeclassesofcompoundsrelevanttotheresearchtopic.

3.2. Biosynthesis of phenolic compounds

The biosynthesis pathway of phenolic compounds iswell characterized (Figure 2). Phenolic compoundsare formed via the well-known shikimate pathwayfromsimplesugarsresultingfromprimarymetabolism.Synthesisofphenylalaninebeginswithcarbohydratestransforming into erythrose-4-phosphate (pentosephosphate pathway) and phosphoenolpyruvate(glycolysis), which enter into the shikimic acidmetabolic pathway. Phenylalanine deamination byphenylalanineammonia-lyase(PAL)isthefirstcrucialstage in the biosynthesis of the large majority ofphenoliccompounds(Macheixetal.,2005).Inadditionto its involvement in the production of phenoliccompounds,phenylalanineoxidationalsoleadstotheformationoftyrosine,theprecursorofcatecholamines


(dopamineandderivatives)(Kulmaetal.,2007),whichareabundantcompounds in thebanana treeandfruit(Muirheadetal.,1984;Kanazawaetal.,2000;Wuytsetal.,2007).

In plants, the phenolic composition variesconsiderably both qualitatively and quantitativelybetweenspeciesandbetweenindividualsofthesamespecies. Some phenolic compounds are ubiquitousin plants (e.g. hydroxycinnamic acids), some arecommon (e.g. anthocyanins) and others are specificto certain families or species (e.g. isoflavonoids andstilbenes).Besidesplantvariety,awiderangeofbioticandabioticstresses(physical,chemicalandbiologicalfactors) both external and endogenous can influencethelevelofplantphenoliccontentbothbeforeandafterharvest.Changesinthelevelofplantphenoliccontentare effected through modulation of the phenolicsmetabolism: light (visible and UV), temperature,osmotic potential, plant nutrition, growth regulators,biotic elicitors, the fruit maturation state at harvest,

the photoperiod, moisture, processing, and storage(Manachetal.,2004;Kalt,2005;Macheixetal.,2005;Lattanzio et al., 2006;Ksouri et al., 2008;Xuet al.,2008;Heetal.,2010;Treutter,2010).Thisleadstoanalterationofaverybroadpaletteoffunctions,includingthereleaseorsynthesisofstressmetabolitesinvolvingpolyphenols.Forexample,environmentalstressescanaffect photosynthesis and the assimilation of carbonrequiredforgrowth,developmentanddefense,leadingtoaninfluenceonthefinalphenolicsconcentrationinplant tissues. In the following sections, the influenceofbioticandabioticfactorsonphenolicssynthesisisfullydiscussed.

Influence of biotic factors. Plantsfacedailyparasiticattacksbypathogenicmicroorganisms,herbivoresandinsects. Parasites have developed different strategiesfor colonizing plants, since they need regulationmechanisms to effectively adapt to changes in theirenvironment. Development of a pathogen within

Figure 2. Simplified pathway of phenolic compound synthesis (adapted fromRolandDouce, 2005)—Voie de synthèse simplifiée des composés phénoliques (d’après Roland Douce, 2005).


a host plant occurs only under certain conditions.These conditions relate to the environmental factorsinfluencing the host plant’s physiological state, theparasite’scapacitytoattackandcolonizeitshost,andthe host’s capacity to establish mechanisms capableofstoppingcolonizationby theparasite.Plantshave,however, developed preformed and induced defensemechanismseffectiveagainstpathogenicinfections.

Followingpenetrationbypathogensofthephysicaland chemical constitutive barriers of a susceptibleor a resistant plant, induced structural and chemicalbarriersareactivatedinordertopreventthepathogen’sprogression. This results in a multitude of defenseresponses. For instance, the defense response of thetomatotissueisseeninanincreaseinsolublephenol(Zhu et al., 2004), and/or the deposit of lignin andlignin polymers (Mandal et al., 2007; Panina et al.,2007).Whenaplantcellencountersapathogen, thisalsoprovokesotherreactionssuchasthehypersensitiveresponse(HR),whichmayconfinethepathogenatthepenetration point (Lepoivre, 2003; Lattanzio et al.,2006; Van Loon et al., 2006; Ferreira et al., 2007).However,phenoliccompoundshavedifferentratesofaccumulation depending on whether plant-pathogeninteractioniscompatibleorincompatible.

TheHR triggers a general resistancemechanism,rendering uninfected parts of the plant less sensitivetofurtherattackbypathogens(Lattanzioetal.,2006).Resistantreactionsinvolvingphenoliccompoundsareinducedintheadjacentcellssurroundingtheinfectedzone,formingalocalizedacquiredresistance(LAR).Indistaltissuecells,asystemicacquiredresistance(SAR)isestablished (Lepoivre,2003;Macheixetal.,2005;Lattanzioetal.,2006;VanLoonetal.,2006;Ferreiraet al., 2007). Stilbene phytoalexines (resveratrol),for example, are accumulated in grapewine berriesfollowingfungalinfectionbyBotrytis cinerea,butalsoinhealthygrapesonthesameclusterornearinfectedgrapeclusters(Adrianetal.,2000).Inthecaseofthebananatree,thepresenceofMycosphaerellaleafspotdiseases during growth influences the susceptibilityofbananas topost-harvestdiseases (Ewané,personalcommunication), but the possible involvement ofphenoliccompoundshasnotbeeninvestigated.

Influence of abiotic factors. Abiotic factors– e.g.pedoclimatic,agronomicandagrotechnical−influencethephenolicbiosyntheticprocessinplant tissuecellsbeforeandafterharvest.Thegeographicallocationoftheproductionzonecaninfluencethebiosynthesisofpolyphenolsinplanttissues.Tropicalandhighaltitudeplants contain higher proportions of flavonoids thandotemperateplants(Lattanzioetal.,2006),probablybecauseofdifferencesinclimaticregimes.

Seasonalvariabilityinplantphenoliccontentmaybeduetotheeffectsofclimaticfactorssuchassolar

radiation, temperature, rainfall (water availability)and the hydrothermal coefficient between seasons.Spatiotemporalvariationshavebeenfoundtoinfluencethesusceptibilityofbananastocrownrot,butfurtherinvestigationsareneeded toprovideevidencefor theinfluence of these variations on the fruit’s phenoliccontent.Awidearrayofabioticstimuli,suchassalinityanddrought,arecapableof triggeringchangesin theplant’s metabolism and these changes enhance theproduction of plant secondary products (Khan et al.,2011).

High levels of solar radiation coupled with hightemperaturesleadinsomecasestomodificationsintheaccumulationofpolyphenolsintheplant.Theresultingmodificationsmake it difficult to determine whetherphysiologicalchangesrelatedtophenolicsynthesisintheplantarecausedbytheeffectsofeithersolarradiationor high temperature. The literature has reported thattemperaturecanbepositivelyornegativelycorrelatedto theaccumulationofpolyphenolsduringgrowthorprocessing for several plant species (Kalt, 2005; Heetal.,2010;Treutter,2010).Aprominentexampleoftheeffectoftemperatureandlightcanbeseeninthesignificantlyhighlevelofphenolicsfoundintheseedandskinofwinterberriescomparedtosummerberries(Xuetal.,2011).

Someinformationon theeffectof lightexposure,UVandsolarradiationonPALandphenolicssynthesishas been reported in the literature for several plantspecies.The influence of other factors has also beencited,suchassoilfertility,fertilizationmode(nutrientsupplies), irrigation (water availability), rootstocks,elevated atmosphericCO2, and pre-harvest treatment(Kalt, 2005; Lattanzio et al., 2006; He et al., 2010;Treutter, 2010; Pombo et al., 2011).Hence, it is notonly the energy provided for carbon assimilation(carbonresourcesforbiosynthesis)butalsothequality,namelyUVfractions(lightintensity),whichstimulatesthe formation and accumulation of certain phenoliccompounds in plants (Ghasemzadeh et al., 2010;Treutter,2010).Theinfluenceofsoilwithhighlevelsofaluminumchlorideingrapeleaveshasbeenshowntostimulatetheproductionofresveratrol(Adrianetal.,2000).

Cultural practice is another factor that influencesthephenoliccontentofplantsandallows thecontrolof plant growing conditions. Since carbohydrateavailability is a prerequisite for phenylpropanoidaccumulation(Treutter,2010), thedegreeof ripenessorphysiologicalageof thefruitatharvest (maturity)has a considerable effect on the concentration andproportionsofthevariouspolyphenols(Macheixetal.,1990; Macheix et al., 2005). Moreover, So-Si ratiomodificationhasbeenshowntoimprovethechemicalcomposition of Vitis vinifera cultivars through animpact on anthocyanin accumulation (Mota et al.,


2010). So-Si ratio modification also influences thesusceptibilityofthebananafruittocrownrot(Lassoisetal.,2010b).Anevaluationof the levelofphenoliccompound synthesis has not yet been undertaken.Furthermore, cultural conditions such as organic orsustainable agriculture provide higher amounts ofpolyphenols in strawberries, blackberries, and cornthandoconventionalorhydroponicconditionswithoutstress(Asamietal.,2003).

Several studies have reported the influence ofprocessing and storage on the synthesis of phenoliccompounds or on degradation in fruits, vegetablesand plants (Kalt, 2005; Lattanzio et al., 2006; Heet al., 2010; Treutter, 2010).At the packing station,during the preparation of banana clusters, physicalinjurytothefruitthroughcuttingofthecrowntissuesmay lead to oxidative degradation of polyphenols.This oxidative degradation of polyphenols causestheir transformation into brown pigments that arepolymerized to different degrees or else it causespolyphenolsynthesisinthebananatissues.Inaddition,certainwater-solublephenolicspresentinthewoundedcrownmayleachfromfruittissuesintowashingtanks.Finally,thenumberofphenoliccompoundsknowntobe synthesized and stored by higher plants is in thethousandsandrising;however,thefunctionsofmanyphenolicsremainunknown.

3.3. Localization and function of phenolic compounds in plants

Biosynthesisofphenoliccompoundsoccursatvarioussites in plant cells, such as the chloroplasts, thecytoplasmandtheendoplasmicreticulummembrane.Polyphenols (relatively hydrophilic) usuallyaccumulate in the central vacuoles of guard cells,epidermal cells and the subepidermal cells of leavesand shoots. Some polyphenols are found covalentlylinkedtotheplantcellwall(lignin);othersarefoundin waxes (related to lipidic structures) or on theexternal surfaces (cuticle) of plant organs (Lattanzioetal.,2006).Thelocalizationofaphenoliccompoundwithin a tissue reflects its physiological function orits participation in interactions of the plant with itsenvironment (Macheix et al., 2005). For example,polyphenols with a role in signaling or defense areoftenstoredatstrategicallyimportantsites(Lattanzioetal.,2006).

Phenoliccompounds,bothpreformedandinduced,play an essential role in the balance of the plantwithin its environment and its capacity to adapt toenvironmentalchanges(Macheixetal.,2005)throughbiochemical, physiological andmolecular responses.Phenoliccompoundsinterveneinmajorphysiologicalmechanismsoftheplant,suchasgrowth,reproduction,pigmentation,rhizogenesis,vitrificationandresistance

topathogens,byperformingmanyfunctions(Cheynier,2005; Lattanzio et al., 2006). Polyphenols play akeyroleas themajor red,blue,andpurplepigmentsof plants, as antioxidants and metal chelators, andas agents acting both above and below ground insignalingbetween theplantandotherorganismsandasUVlightscreens(Cheynier,2005;Lattanzioetal.,2006). Polyphenols have multiple effects on tissuematurationprocesses andon the sensoryqualities ofplant-derived food products, including astringency,bitterness and aroma. The compounds are alsoresponsible for the browning caused by wounds tofruitorbyconservationaccidentsandnotablyfortheeffectof low temperaturesonpineappleandbanana.Inbanana,dopaminehasbeenidentifiedasasubstratefor polyphenol oxidase, resulting in the browningreaction,andthechemicalisalsoresponsiblefortissuediscoloration (Kanazawa et al., 2000;Someya et al.,2002;Maneenuametal.,2007).Aspolyphenolsplayaroleinregulatingplant-environmentinteractions,someresearchers attribute an ecological function to thesecompounds. Polyphenols are, for instance, reportedto modulate litter decomposition processes and themineralization rate in plants (Macheix et al., 2005;Lattanzio et al., 2006). Plants thus contain severalclassesofpolyphenolswithdifferentlocalizationsandroles.

3.4. Involvement of phenolic compounds in plant defense mechanisms

Phenolic compounds involved in plant defense areeitherpreformed(constitutive)orsynthesizedde novo(postinfectional). Preexisting phenols are antibiotic(antifungal) compounds such as simple phenols,phenolic acids, flavonols, and dihydrochalcones.These preexisting phenols are called phytoanticipinsin order to distinguish them from phytoalexins,which are synthesized from remote precursors inresponsetopathogenicattack(Lattanzioetal.,2006).Phenoliccompoundssynthesizedde novoaccumulatein response to plant infection by a pathogen. Thisdefensive response involves the rapid increase ofspecific phenolic compounds at the infected site,particularly phytoalexins, which can inhibit a broadrange of microorganisms (Lepoivre, 2003; Macheixet al., 2005; Lattanzio et al., 2006). The result isthe development of plant resistance to disease. Anexample of the involvement of polyphenols in plantdefenseistheiractionintheprogrammedcelldeathofonepartof theplant.Therateatwhichprogrammedcell death occurs depends on whether the host-pathogen interaction is compatible or incompatible.Duringtheestablishmentofapathogeninhosttissues,thereisanincreaseintheactivityofspecificenzymessuch as PAL, peroxidase and polyphenol oxidase.


Theseenzymes,whichconsumeoxygenandproducefungitoxicquinones,makethemediumunfavorableforthefurtherdevelopmentofpathogens(Lattanzioet al.,2006). PAL is the key enzyme involved in phenoliccompound metabolism through the phenylpropanoidpathway (Dixon et al., 2002). Peroxidase catalyzesthe condensation of phenol into lignin and is alsoinvolvedinphenolmetabolism(Passardietal.,2004).Polyphenoloxidaseoxidizesconstitutiveplantphenolsintoquinones,whichhavebactericidalandfungicidalproperties, and is also involved in the oxidativedetoxificationofpathogenphytotoxins(Macheixetal.,1990;Yoruketal.,2003).

Another example of a phenolic compound thatcontributestotheplant’sdefensemechanismsislignin.Ligninisaphenolicpolymer,whichplaysafundamentalrole in solute conductance, mechanical support anddisease resistance. In response to abiotic stress, towoundingortopathogenicinfection,thedepositionoflignins,ligninpolymersandotherphenolicsubstancesrelatedtothecellwallareobserved.Thiscontributestobothathickeningofthecellwall(conferringgreaterrigidityandmechanicalresistance)andtoanincreaseincellhydrophobicity.Ligninthusactsasaphysicalbarrieragainstpathogenicinvasion.Inaddition,lignindepositsreducethediffusionofenzymesandtoxinsthatthepathogenreleasesinordertofacilitatehosttissue

colonization.Ligninalsodeprivesthepathogenoftheplantwaterandnutrientsnecessarytoitsproliferation(Macheixetal.,2005;Lattanzioetal.,2006).

3.5. Involvement of phenolic compounds in banana tree defense

Sincephenoliccompoundsarepotentialtargetsfortheimprovement of plant resistance against pathogenicattack, it is possible that they are involved in thesusceptibility of bananas to crown rot disease and abetter understanding of their involvement in bananatreedefenseisrequired.Thephenoliccompositionandthe roleof severalbanana tree tissues (leaves, fruits,roots)havebeendescribedintheliteraturereview,buttheirpotentialroleinthevariationofsusceptibilityofbananacrownstodiseaseisnotyetknown(Table 1).

Preformed defense mechanisms. The leaf surfacewax,cuticle,suberinandcellwallarethefirstpreformedphysicalbarriersinbanana.Thesepreformedphysicalbarriers are also involved in banana tree defensemechanisms, and contain phenolic compounds(lignin,cross-linkinghydroxycinnamicacids)intheirstructures.Thecuticleformsanenvelopethatprotectstheaerialpartsofplantsfromthemajorityofattacks

Table 1. Somephenoliccompoundsidentifiedinbananatreetissues—Quelques composés phénoliques identifiés dans les tissus du bananier.Phenolic alkaloids Tissues Class (Subclass) ReferencesDopamineNorepinephrine

FruitsRoots

Catecholamines Valetteetal.,1998;Kanazawaetal.,2000;Wuytsetal.,2007

Phenolic compounds Tissues Class (Subclass) ReferencesPhenolicacids

Gallicacid,vanillin Fruit Hydroxybenzoic acids Mendozaetal.,1992;Mendezetal.,2003

Chlorogenic,caffeic,P-coumaric,ferulic,vanillicandsynapicacids

Fruits,roots Hydroxycinnamic acids and derivatives

Wadeetal.,1993;Valetteetal.,1998;deAscensaoetal.,2003;Wuytsetal.,2007

CatechinGallocatechin

Fruits SimplephenolsFlavan-3-ol

Mendozaetal.,1992;Wadeetal.,1993;Someyaetal.,2002;Mendezetal.,2003

FlavonoidsRutin,naringin Fruits

Leaves,rootsFlavonols Flavanones

Valetteetal.,1998;Kanazawaetal.,2000;Wuytsetal.,2007

Anthocyanidins Flavonoids derivatives Collingbornetal.,2000Tannins

Tanninscatechic,Proanthocyanidins

FruitsRoots

Hydrolysable tannins Condensed tannins

Mendozaetal.,1992;Elhadrami,1997;Valetteetal.,1998

Lignin Roots Lignin Valetteetal.,1998;deAscensaoetal.,2003;Wuytsetal.,2007


by pathogenic fungi (Pollard et al., 2008). Suberin,localized in theundergroundpartsof theplants suchasthebarkandscartissues,containshighquantitiesofω-dicarboxylic acid, hydroxycinnamic acids (mainlyferulate) and fatty alcohols (Pollard etal., 2008;Schreiber,2010).Thecuticleand suberincontrol thediffusionofgases,ofwater,andofsolutesinandoutoftheplant.Theyalsoplayaprotectiveroletowardsbioticandabioticstress(Pollardetal.,2008;Schreiber,2010).Thepecto-cellulosicwallplaystheroleof“skeleton”whilemaintainingacertainplasticity/elasticity in theplant,allowinggrowthandcellulardivisions(Macheixetal.,2005),butalsobeinginvolvedinphysiologicalresistance.

The preformed chemical barriers of plants are aplethoraofpeptides,proteinsandsecondarymetabolites(phenolics, sulfur compounds, etc.), which act asantimicrobial compounds during defense responsesagainstmicroorganisms(Lattanzioetal.,2006).Someof these compounds are present in their biologicallyactiveform,andarethereforedirectlytoxic;othersarepresent in the formof inactiveprecursors (combinedforms). In studies comparing varieties of bananasusceptible toblack leaf streakdiseasewithpartiallyresistantvarieties,certainmesophyllcellsspecializedinthestorageofphenoliccompounds(proanthocyanidins)were found tobe lower innumber in the susceptiblevarietiesthaninthepartiallyresistantones(Beveraggietal.,1995;ElHadrami,1997).

Induced defense mechanisms. After infection bydifferent banana pathogens, a rapid increase in bothphenolic compounds and phenylpropanoid pathwayenzymes has been observed in banana tree tissues.Inducedstructuralbarriersareactivatedfollowingthepresenceofpathogensinsusceptibleorresistantplants,and this results in amultitude of defense responses.When a plant recognizes a pathogenic invader, itsdefensemechanismsareinduced,andchemicalbarriersare produced as a result. These chemical barriersare generally in the form of “de novo’’ synthesizedmoleculesandonceproduced,thesemoleculesbecomeaccumulated.

Severalstudiesontheinteractionbetweenbananatreerootsandtheirvariouspathogenshavesuggestedaninvolvementofphenoliccompoundsinthedefenseresponses of the banana tree. These studies focusedon cellwall lignification, on histochemical detectionof phenolic compounds and on the quantification offlavonoids, proanthocyanidins and hydroxycinnamicacidsafterinfectionofbananarootsbyphytophagousnematodes (Valette et al., 1998; Collingborn et al.,2000;Kanazawaetal.,2000;deAscenceoetal.,2003;Wuyts et al., 2007). In resistant banana cultivars, ahighercontentofseveralphenoliccompoundssuchasdopamineandcyanidin-relatedcompounds,lignin,and

ferulicacid(estersandhydrolyzationproductsofferulicacid)wasobserved(Wuytsetal.,2007).Moreover,theroleofthesecompoundsindefensemechanismssuchasphysicalbarriers,toxicagentandprotectionagainstpathogenicattackwassuggested.

In other studies, several phytoalexins(phenylphenalenones, irenolone, and emenolonetypes)havebeeninducedingreenbananafruitsafterwounding or inoculation withColletotrichum musae(Luis et al., 1993; Kamo et al., 1998; Kamo et al.,2001). Recently, in the interaction between Musaspp.andFusarium oxysporumf.sp.cubense(Panamadisease), resistant hybrid plantlets (leaves and roots)werefoundtocontainhigherconcentrationsofphenoland pathogenesis-related proteins and higher activitylevels of PAL and oxidative enzymes (peroxidase,polyphenol oxidase, superoxide dismutase, catalase)than sensitive hybrid plantlets (Kavino et al.,2009). During penetration of host tissues, phenolicsubstances are released around thepathogenhyphae,causing considerablemorphological changes such ascytoplasmicdisorganizationand lossofprotoplasmiccontents (Kavino et al., 2009) and thus forming achemical barrier that blocks or at least slows downmicroorganismprogression.

Asmentioned above,many phenolic compounds,particularly dopamine, have been identified invariousbanana tree tissues.Amongabroad rangeofplants, bananas have the richest dopamine content:100μg.g-1FWinCavendishbananapeelascomparedwith7μg.g-1FWforpotato,thesecondrichestinthislist of dopamine-rich plants (Kulma et al., 2007).This observation suggests that dopaminemight playan important role in banana physiology. Dopamineresults from the hydroxylation of tyrosine to3,4-dihydroxyphenylalanine,andisresponsibleforthebrowningof the fruitpeelandpulp.ProductsarisingfromthedecompositionofbananadopamineseemtohaveafungitoxicactivityagainstC. musae(Mulvenaet al., 1969; Muirhead et al., 1984). Moreover, arecent study on the molecular mechanisms involvedin the variations in the susceptibility of banana fruithas highlighted overexpression of the dopamine-β-monooxygenase gene in bananas less susceptible tocrownrot(Lassoisetal.,2011).

4. CONCLUSION

The occurrence of crown rot disease seems tocorrelatewith the physiological state of the fruits atharvest.Plantpolyphenols are secondarymetabolitesinvolvedinthedefensemechanismsofplantsagainstfungal pathogens. These phenolic compounds arealso involved in thedefense responsesof thebananatree, although theirmechanism(s)of actionand their


antagonisticpropertiesarenotknown.Thus,thepossibleinvolvement of phenolic compounds in variationsfound in the susceptibility of bananas to crown rotmeans that these compounds represent a potentialtarget for developing alternatives to the chemicalcontrolof thedisease. It is thusessential tomeasurepoolsofphenoliccompounds,particularlydopamine,infruitsdisplayingdifferentialsusceptibility,soastoidentifykey“defense”compoundsandtogainabetterknowledgeof thedefensemechanismsof thebananacrowntissues.

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