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The endophytic continuum

Mycol.Res.109(6):661–686(June2005).fTheBritishMycologicalSocietydoi:10.1017/S095375620500273XPrintedintheUnitedKingdom.

661

Review

Theendophyticcontinuum

BarbaraSCHULZ1andChristineBOYLE2

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InstituteofMicrobiology,TechnicalUniversityofBraunschweig,Spielmannstrasse7,D-38106Braunschweig,Germany.Augustastrasse.32,D-02826Go¨rlitz,Germany.E-mail:b.schulz@tu-bs.de

Received25February2004;accepted15February2005.

Inspiteoftheterm‘endophyte’beingemployedforallorganismsthatinhabitplants,mycologistshavecometousetheterm‘fungalendophyte’forfungithatinhabitplantswithoutcausingvisiblediseasesymptoms.Thetermrefersonlytofungiatthemomentofdetectionwithoutregardforthefuturestatusoftheinteraction.Thispaperisareviewofliteratureonnon-balansiaceousfungiinvolvedinasymptomaticcolonisationsofplants.Thesefungalendophytesrepresentacontinuumoffungiwithrespecttophysiologicalstatus,infectionmodus,colonisationpattern,secondary

metabolism,life-historystrategy,anddevelopmentalandevolutionarystages,butalsowithrespecttothefungalandhosttaxainvolvedinthesymbioses.

Wehypothesizethattherearenoneutralinteractions,butratherthatendophyte-hostinteractionsinvolveabalanceofantagonisms,irrespectiveoftheplantorganinfected.Thereisalwaysatleastadegreeofvirulenceonthepartofthefungusenablinginfection,whereasdefenceoftheplanthostlimitsdevelopmentoffungalinvadersanddisease.Itisalsohypothesizedthattheendophytes,incontrasttoknownpathogens,generallyhavefargreaterphenotypicplasticityandthusmoreoptionsthanpathogens:infection,localbutalsoextensivecolonisation,latency,virulence,pathogenityand(or)saprophytism.Thisphenotypicplasticityisamotorofevolution.

INTRODUCTION

Takenliterally,thewordendophytemeans‘intheplant’(endonGr.,within;phyton,plant).Theusageofthistermisasbroadasitsliteralde nitionandspec-trumofpotentialplanthostsandinhabitants,includingbacteria(Kobayashi&Palumbo2000),fungi(Stone,Bacon&White2000),algae(Peters1991),andinsects(Feller1995).Anyorganofthehostcanbecolonized.Equallyvariableisthelife-historystrategyofthesym-biosis,rangingfromfacultativelysaprobic,toparasitic,toexploitive,tomutualistic.However,commontoallendophyticinteractionsistheprovisionofnutrientsandabu erfromexternalenvironmentalstressesandmicrobialcompetition.

Theendophyticpartnersandtheirrelationshipstoeachothervary.Therearepathogenicendophyticalgae(Bouarabetal.1999),parasiticendophyticplants(Marleretal.1999),mutualisticendophyticbacteria(Chanway1996,Adhikarietal.2001,Baietal.2002),ectomycorrhizalhelperbacteria(Founouneetal.2002),aswellasendophyticbacteriainpathogenicandcom-mensalisticsymbioses(Sturz&Nowak2000).Thereareequallydiverseendophyticinteractionsoffungiwiththeirplanthosts:mutualisticmycorrhizalfungiwiththerootsofthehostaretermedendophytic(Sieber2002),butalsothoseoftheorchidwithitsfungalendo-phytes,inspiteofthehostbeingmyco-heterotrophicandexploitingthefungalendophyte(Gardes2002).Somedark-septatefungalendophytesthatcolonizetherootsofmanyherbaceousplantsandtreesaremutu-alistic,whereasothersbecomepathogenic(Jumpponen2001,Sieber2002).Otherfungalendophytesinhabitsolelyabove-groundplantorgansandtheseagainmaypartakeinvariedandvariableinteractionswiththeplanthost,rangingfrommutualistic(Redmanetal.2002,Schulzetal.2002)tocrypticcommensal(Deckert,Melville&Petersen2001)tolatentandviru-lentpathogens(Sinclair&Cerkauskas1996,Schulzetal.1998).Incontrasttothebroadusageoftheterm‘endophyte’,manymycologistshavecometoemploythistermonlyforthosefungithatcolonizeaplantwithoutcausingvisiblediseasesymptomsatanyspeci cmoment(Petrini1991,Wilson1995,Stoneetal.2000).Someevenspeakofthe‘trueendophytes’,mean-ingthosewhosecolonisationneverresultsinvisible

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