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MushroomNicholasP.Money

Printpublicationdate:2011PrintISBN-13:9780199732562PublishedtoOxfordScholarshipOnline:January2012DOI:10.1093/acprof:oso/9780199732562.001.0001

AngelsontheLawnNicholasP.Money

DOI:10.1093/acprof:oso/9780199732562.003.0001

AbstractandKeywords

Theintroductorychapterexplainshowmushroomsdevelop.Thecomplexfungallifecycleinvolvesthegerminationofspores,theexpansionoffeedingcolonies,andmatingprocessesthatcaninvolvetensofthousandsofsexesinasinglemushroomspecies.ThestudyofthesemechanismsbeganwiththeFlorentinegenius,AntonMicheliintheeighteenthcentury,and,later,engagedfascinatingpersonalitiesincludingchildren'sauthorBeatrixPotter,WorthingtonSmith(whogotmostofhisfactsspectacularlywrong),andElsieWakefield(whogotherfactsright).Themodernstudyofmushroomdevelopmentisachallengeforthefieldofmoleculargeneticsandcomputersimulationshaveprovidedusefulinsights.Recentchangesinseasonalpatternsofmushroomfruitingmayrelatetoglobalclimatechange.

Keywords:mushrooms,germination,spores,colonies,mating,sexes,AntonMicheli,BeatrixPotter,ElsieWakefield,climatechange

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HowmushroomsdevelopAgrown-upneighborintheEnglishvillageofmychildhoodtoldstoriesaboutangelsthatsatuponourshouldersandfairiesthatlivedinhersnapdragons.Liketheotherkids,Isearchedherflowersforaglimpseofthesprites,butagnosticismimbibedfrommyparentsquicklyoverruledthisinnocentplay.Yet,therewasmagicinmyneighborsgarden,andIhadseenrealangelsonherlawn:littlestalkedbellsthatpokedfromthedew-drenchedgrassonautumnmornings,evanescentbeautieswhosedelicatelybalancedcapsquiveredtothetouch.Byafternoontheyweregone,shriveledintothegreenery.Doesanylivingthingseemmoresupernaturaltoachildthanamushroom?Theirprevalenceinfairy-taleillustrationsandfantasymoviessuggestsnot.Areliablepieceofscenerybehindunicorns,providingforestsheltersforelves,mushroomsareoftentheonlythingsinthesestoriesdrawnfromreality.Likenootherspecies,thestrangenessoffungisurvivesthelossofinnocenceaboutthelimitsofnature.Theytrumpthesupernatural,theirmagicintensifyingaswelearnmoreaboutthem.

Thiscelebrationofthefungalfruitbodybegins,likeeverymushroom,intheair.Onbreezydays,thewindisfullofinvisiblebiology.Fungalsporesthousandsormillionsoftheminacubicmeterofourlife-sustaininggasaccompanypollenfromflowers,cropplants,andcone-bearingtrees,aswellascountlessbacteriaandviruses.Thesesporescomefrominnumerablespeciesthatblanket(p.2) theleavesandstemsofplants,fungithatfeedonanimaldungandrotcorpses,andthethousandsofspeciesofbasidiomycetefungithatformmushrooms.Wearebathedinasoupoftheseprocreativemorselsandinhalethebiospherewitheverybreath.Ifthatdoesntmakeyoureachfornasalspray,considerthateachmushroomthatelbowsitselffromthegroundshedshundredsofmillions,eventrillions,ofmicroscopicspores.Asasourceofairborneparticulates,themushroomisamasterpieceofnaturalengineering.

Mushroomsporescanstartformingacolonywhentheymakelandfallatthatrarestofsites:moistsoilthatisntcrowdedwithotherfungiandpredatorybugs.Thishighlightsacrucialpointinunderstandingmushroombiologyandinassessingthevalueofmushroomsintherestorationofdamagedecosystemsissuesthatwillbeaddressedinlaterchapters.Vastnumbersofsporesaredispersedbecausemostofthemalightonhostilesoil.Considertheblood-footmushroom,acommonspeciesinNorthAmerica.AlsoknownasMycenahaematopus,thislittleorangemushroomweepsabloodyfluidwhenitsstem,orstipe,issevered(Plate1).Abletogrowonwell-rotted,pulpywood,itisabundantinrain-drenchedforestswithplentyoffallentimber.Thousandsofsporessweepfromthebottomofthismushroomscapeverysecondofitsbrieflife.Inperfectlystillair,thesporesdescendataspeedofaboutonemillimeterpersecond,whichmeansthatfreefallfromthebottomoftheblood-footgillsisoverinlessthanoneminute.Yet,theslightestbreezecankeeptheparticlesaloftforhours.Experimentsshowthatmostsporesfallquiteclosetotheparentfruitbody,manydirectlybeneaththecap,wheretheyareevidentasadustydrape;afewdriftmuchfartherthroughthetreesandescapethecanopy.1Withallthewoodinaforest,itwouldseemlikelythatalargenumberofsporessettleontheirpreferredfoodsources.Theactualnumberofsuccessfullandingsisimpossibletoestimatewith(p.3) anyaccuracy,butevenamongthesewinners,most

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perish.Exposedpatchesofwoodarentasinvitingastheymightseem.Thesporemaybeeatenbyaspringtail,slug,oramoebabeforeitgerminates;itmaydryupinthewitheringrayofasunbeamorgetwashedawaybyaraindrop.Itssurvivalisnotfavored.Thewoodylandingplaceofasporemaylackthenutrientsthatthefungusrequires:perhapsitsrelativeshavealreadydigestedthenecessaryfoodstuffsofitsfinickyblood-footdiet.Starvationisareliablereaper.Evenwhenthereisplentyofmoistwood,malnutritionmaybecausedbycompetitionfromthegerminatingsporesofonessiblings.Poisoningbyotherfungalspecies,whosedomainthesporehasentered,isanotherthreat.Therearesomanyotherwaystodieyoung,andtheprobabilityoflongevitytooslimtocalculate.Thiscomputation,however,ispreciselywhatthemushroomhasdone.Itsoutputofsporeshasbeenfinetunedbynaturalselectiontomaximizesurvivalandlimitwastage.

Plate1 Blood-foot,Mycenahaematopus,showingbeadsofbloodysapclingingtothestipe(stem)surface.FromJ.E.Lange,FloraAgaricinaDanica,vol.2(Copenhagen:Recato,1936).

MushroomsillustratetheMalthusianperpetualstruggleforroomandfoodwithgreaterforcethananyanimal.Onaglobalbasis,thetotalfertilityrateforourspeciesis2.3birthsperwoman;thebirthspergiantpuffball,Calvatiagigantea,soarintothetrillions(Plate2).Thisastonishinglyprolificmushroomisalsoacommonspecies,liketheblood-foot,butitinhabitspasturesratherthanforests.Despiteitssedentarycondition,thepuffballdoesnthaveanyobviousproblemscastingsporesoveritshabitat.Themerestgustwillspillitspowderyoffspring,andraindropssendafogofthemintotheair.Thosetrillionsofsporesarenecessary,nottofindfreshgrassland,but,oncedeposited,tosurvivethetrialsenduredbyeveryfungalspore:unpredictableclimate,predation,andcompetition.Thisiswhymeadowsareneverfilledwithpuffballs,butinsteadaredecorated,hereandthereintheirsoggiestspots,withwhiteglobesthatflagtheirsubterraneancolonies.

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Plate2 Calvatiagigantea,thegiantpuffball.PaintingbyJohnAugustusKnapp,courtesyofLloydLibraryandMuseum,Cincinnati.

(p.4) Araindropisallthatsomespeciesrequireforgermination;othershavemorerefinedphysicalorchemicalneeds.Giantpuffballsporesareparticularlyresistanttogerminationinthelab,withonlyoneperthousandagreeingtogrowinaPetridish.2Experimentssuggestthatmorewillgerminateinthepresenceofyeasts(single-celledfungi),whichoffersaglimpseofthecomplexityofasporesnaturalexistence.Thisintertwiningoflifecycles,withmushroomsreliantonyeasts,orinsects,orevenbirds,mayexplainwhythesporesofsomanyfungihaveneverbeengerminatedinthelaboratory.Thesediverseinteractionsmayinvolveexposuretoforeignsecretions,cohabitationwithinthesamefoodsourceforthepurposeofcooperativedigestion,orentailgreaterintimacysuchasthepassagethroughthepartneranimalsdigestivesystem.Examplesofmutuallysupportiverelationshipsbetweeninsectsandmushroom-formingfungiwillbediscussedinChapter3.

Germinationoccurswiththeemergenceofoneormoreslenderfilaments,orgermtubes,fromthespore(Fig.1.1).Somesporesswellbeforetheygerminate,whileothersshownoobvioussignsofactivitypriortotheprocess.Thegermtubeextendsforawhileandthenbranchesbehinditstip,producingasecondinterconnectedfilament.Bothfilamentscontinuetoextenduntilasecondbranchgrowsfromthefirstaxis,thenmore,andthebranchesformbranches,andanetworkoffilamentsemergeswithinafewhours.Thisistheyoungmycelium,acolonywhosemultipletipsexpandthefungusinanever-enlargingcirclefromtheoriginalsporesittingatitshub.Thisrapiddevelopmentofaseriesofperfectlycylindricaltunnelswhoseliquidcontentspulsetowardtheirextendingtipsisabeautifulthingtowatchunderamicroscope.Myintroductiontothemyceliumsshapewasprovidedbymydad,whoexplainedthatAlexanderFlemingdiscoveredtheantibioticpenicillinwhenhenoticedthatthesandwichhewasabouttoshoveinhismouth(p.5) wascoveredwithcirclesofbluemold.DadembellishedhisstorywiththedetailthatFlemingsfungushadfloatedthroughanopenwindowfromaneighborsfilthykitchen,butIwasquiteinspiredthatsomeonebecameaworld-famousscientistsimplybytakingacloselookatthislunch!(Fortyyearslater,Iremaintraumatizedbythememoryoftheteacherwhotoldme,Itdidnthappenquitelikethat,Nicholas,andthenflogged

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mewithhiscanewhilesingingourschoolhymn,OnwardChristianSoldiers).3Speakingofchildhoodagain,thecolonyofbranchedfilamentsistheadolescence,ofsorts,ofthemushroomtocome.

Fig.1.1 Day-oldcolonyofanink-capmushroomthathasdevelopedfromsingleblackspore.FromA.H.R.Buller,ResearchesonFungi,vol.4(London:Longmans,Green,1931).

Thefirstmicroscopistssawthesefilaments,orhyphae,intheseventeenthcentury.MarcelloMalpighi,betterknownforhisworkoninsectanatomy,offeredthefirstillustrationofthesestructuresinhisAnatomePlantarum,publishedinthe1670s.4ThefunctionofsporesasfungalseedswassurmisedacenturybeforeMalpighibutwasnotprovenuntilexperimentsbythebrilliantFlorentinenaturalistPier(p.6) AntonioMicheliwerepublishedin1729.5Michelididntobservegermination,buthepicturedsporesanddemonstratedthatadustingofthemcastfromonemushroomcouldspawnanewflushofthesametypeoffruitbodiesinaleafpile.Theevidentvitalityofthefungiwasasourceofwonderforthesepioneeringinvestigators,andtherewasagreatdealofconfusionsurroundingtheiraffinitywithotherformsoflife.Micheliheldthewidespreadviewthatthefungiweresimplekindsofplants,butotherstreatedthemasacuriousbranchoftheanimalkingdom.(Lessanthropocentricinvestigatorsmightregardtheanimalsasagrotesquebranchofthefungalkingdom.)InhisMicrographia,Hookedescribedmushroomstructureinthesectiononsponges,whileLinnaeuswroteofanimalculesarisingfromfungalsporesandclassifiedtheminthegenusChaosundertheworms(Vermes)inthetwelftheditionoftheSystemaNaturae.Thisisinterestinginlightofthemodernperspective,whichconsidersthefungiasasistergrouptotheanimals,withbothrelatedonlydistantlytotheplants.

ThefirstcleardescriptionofgerminationwaspublishedacenturylaterbytheFrenchinvestigatorBndictPrvost,whoshowedthatsporesofthesmutfungus,Tilletiacaries,causedthebuntorstinkingsmutinwheat.6Detaileddescriptiveworkongerminationfollowedinthe1870s,whenOscarBrefeldintroducedpureculturetechniquesandusedgelatinasasurfaceforgrowingfungalcolonies.7Bykeepinghis

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culturesfreefromcontaminatingmolds,Brefeldwassuccessfulinfollowingthedevelopmentofink-capmushroomsofCoprinopsisstercoreaallthewayfromsinglehyphae.Mostmushroomswillnotdevelopinthisnonsexualfashion,asIllexplainsoon,buttheinkcapchosenbyBrefeldisahandyonanistthatcandoeverythingonitsown.

ExperimentsonsporegerminationwerefurtherpursuedbyanunexpectedfigureinVictorianmycology,awomanbestknownasanauthorandillustratorofchildrensbooks.BeatrixPotterinventor(p.7) ofthemischievousPeterRabbitdevelopedakeeninterestinnaturalhistoryduringherchildhoodholidaysinScotlandandtheEnglishLakeDistrict,andthispassionprovedlifelong.Shepaintedbeautifullyobservedwatercolorsofmushroomsthatwereused,posthumously,toillustrateaninfluentialbookonmushrooms.8Inaddition,Potterworkedwithamicroscopeand,asherinterestinfungigrewinthe1890s,shebeganwrestlingwithquestionsaboutthedevelopmentoflichensandthelifecyclesofmushrooms.Shethoughtthatlichensmightbeformedbyfungicapableofgeneratingtheirownchlorophyll-containingcells.Hoping,perhaps,todocumentthistransformation,PottercarriedoutexperimentsonsporegerminationthatechoedearlierstudiesbyBrefeld.Oneoftheorganismsshestudiedformedlittlediscs,orcrusts,onthesurfaceoftreetrunksandonbranches.Succeedingingerminatingitslargespinyspores,shemayhavebelievedthatshewaswitnessingtheearlieststagesoflichendevelopment.ButtheseinvestigationsceasedwhenshesharedherfindingswithGeorgeMurray,KeeperofBotanyattheNaturalHistoryMuseuminLondon,whoexplainedthatherlichenwasafungus.TheorangediscsofAleurodiscusamorphuscertainlybearsuperficialresemblancetofolioseorcrustoselichens,butrelativesofthisfungusformconventionalumbrella-shapedmushroomsandlackthealgalpartnerofthesesymbioses.PotteralsovisitedKewtodiscussherresearch,butshewasdismissedbyitspompousdirector.Shepersistedwithherwork,however,andseemstohaveparlayedherexperiencewithAleurodiscusintoawiderexplorationofsporegerminationamongothermushrooms.ShepreparedapaperontheseexperimentsfortheLinneanSociety,thenwithdrewthemanuscriptafteranunenthusiasticairingatameetingandabandonedherresearch.Potterwas,nevertheless,apioneeringmycologist,onewhoseintelligenceandinquisitivenessmighthavebeenchanneledintoacareerinscience(p.8) hadshepossessedtheYchromosomerequiredformostVictorianprofessions.Fortunately,herconsiderableartistictalentsgaveherotheroutletsforherambition.

Thetransitionfromsporestocoloniestomushroomsisadevelopmentaljourneythatremainssurprisinglymysterious.SinceBrefeldandPotter,mycologistshavelearnedagreatdealabouttheprocessesthatoccurwhensporesgerminate,andwhencoloniesexpand,butwearealongwayfromacompellingexplanationofthecooperativeinteractionsbetweenindividualcellsthatresultintheformationofafunctionalmushroom.Researchondevelopmentwithinanevolutionarycontext,knownasevo-devo,isamongthemostvibrantandsuccessfulfieldsofmodernbiology.Roundwormsandfruitfliesarefavoritesforevo-devostudies.Theseanimalscontainorganswithfunctionsanalogoustohumanviscera,includingprimitivekidneys,intestines,sexorgans,andsoon,andweknowalotabouthowtheiranatomyisassembled.Amushroomisagooddealsimplerinstructure:itisasingleorganformedfromasingletypeofcell.Thissimplicitybeliesits

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intractabilityasaresearchsubject.Illtellyouwhatwehavelearnedsofar,andoutline,intheparlanceoftheretiredAmericanmilitarygeniusDonaldRumsfeld,theknownunknowns,or,whatweknowwedontknow.

Coloniesthatsupportmushroomscanbeverysmall,occupyingadamptwig,orverylarge,invadinganenormousterritoryofforestsoil.ThecurrentworldchampionisacolonyofArmillariaostoyae,oneofthespeciesreferredtoasahoneymushroom,thathaspopulated2,400acres,or10squarekilometers,oftheMalheurNationalForestinOregon.9Thisfungusspreadsbymeansofrhizomorphs,root-likestructuresthatdevelopfromscoresofinterminglinghyphaeandbearsomeresemblancetomushroomstems.Thesearetheblackenedandoftenflattenedbootlacesthatcanbefoundin(p.9)woodlandsoilandunderthebarkofdecayingtrees.Whenhyphaegrowinthiscooperativefashion,theyallowthefungustoexpandatmuchfasterratesthanbyfinelydissectedcoloniesofindividualhyphae.Bypipingtheirownwatersupplytowardtheirtips,theycangrowacrossdrysoil.Alotofthewood-decayfungiinforestsproducerhizomorphs;theyareavitalaccessorytothehyphaethatperformthefeedingactivitiesofthefungus.

AsBrefeldshowed,sporesgerminatewiththeprotrusionofhyphaltips,usuallyoneperspore,sometimesmore.Hyphalelongationandbranchingshapeacolonywhosecentrifugalexpansioncreatesanetworkinwhicheveryscrapofterritorycanbeprobedbyafeedinghyphaltip(Fig.1.2).Thepatternresemblestheveinsinaleaf,orthebloodvesselsinananimal.Eachofthesenetworksoffersanefficientwaytopermeateaparticularvolumewithtubes.Somefungalcoloniesengageinmorefrequentbranchingthanothers,andthesebranchescanfusetoincreaseconnectivitybetweendifferentpartsoftheorganism.Coloniesofwood-decayfungigrowninwetsandinthelablookquitediffuse,formingbundlesofhyphae(p.10) calledcords(similartorhizomorphs)separatedbyafewunbundledhyphae.Thishungrycolonyenlargesoverthedesert,withoutchangingitsoverallappearance,untiloneregionencountersawoodblock.Whenthishappens,thefungusrespondsbyconcentratinggrowthtowardthefood,creatingcordsthatconnectdirectlytothewoodandabandoninghyphaefartheraway.Intheabsenceofanysophisticatedsniffingsystemforfindingwood,thefungusfansoutinalldirections,wageringthatitwillhitsomethingnutritiousatitsperipheryifitkeepsgrowinglongenough.AflawlessillustrationofthiswouldbefurnishedbyreleasingagroupoffamishedteenagersinanunfamiliarcityandsendingthemoffonallcompasspointswiththesoleinstructionthattheycalltheirfriendscellphonesiftheyfindthemselvesundertheGoldenArches.MostofthemcouldberetrievedfromthesameMcDonaldsafterafewhoursoflistlesswandering.

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Fig.1.2 Scanningelectronmicrographofhyphaltipsgrowingoversolidsurface.Thesearethefeedingstructurescommontoallfungi.PhotographcourtesyofGeoffreyGadd,UniversityofDundee.

Hyphaethatformthecoloniesofmushroom-formingfungiarecompartmentalizedintoshortsegmentsbycross-walls.Whenviewedunderamicroscope,thisgiveshyphaetheappearanceofladderswithwidelyspacedrungs.Themiddleofeachseptumisperforatedbyavalvethatallowsfortheflowofcytoplasmfromonecompartmenttothenextwhenitisopen.Eachcompartmentcanberegardedasacell,althoughitmightbeequallyvalidtoconsiderthatalloftheinterconnectedcompartmentsrepresentasinglecellwithlotsofnuclei.(Howmanyangelscandanceonthepointofaneedle?)Coloniesthatdevelopfromsinglesporeshaveonenucleuspercompartment.Thesecoloniesarecalledmonokaryons,orhomokaryons,referringtotheirsolitarynuclei.Inthetextbookdescriptionofthemushroomlifecycle,twoofthesecoloniesfusetoformanewtypeofcolony,calledadikaryon,inwhicheachcompartmentcontainstwonucleionederivedfromeachoftheoriginalmates(Fig.1.3).Thedikaryonisthecolonyfromwhich(p.11)themushroomdevelops.Eachtimeanewcompartmentformsinthedikaryon,itmustbefurnishedwithcopiesofeachofthenucleibequeathedbythepairofparentalmonokaryons.Thisinvolvessomeshufflingofdividingnucleiaroundthenewseptum,whichisachievedbytheproductionofalittlehookedbranchcalledaclampconnection.Thesearevisibleasbumpsonthesurfaceoftheseptainthedikaryon.

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Fig.1.3 Thebasidiomycetelifecycle.Basidiosporesgerminatetoformcoloniesofmonokaryotichyphaecontainingnucleiofasinglematingtype.Compatiblemonokaryonsmergeandproduceadikaryonfromwhichthefruitbodydevelops.Nucleioftwomatingtypesfusewithinbasidiaonthegillsurfaces;thefusionnucleusundergoesmeiosis,andeachofthefournucleiresultingfromthisdivisionispackagedintoaspore.IllustrationincludesdrawingsadaptedfromH.J.Brodie,TheBirdsNestFungi(Toronto:UniversityofTorontoPress,1975),withpermission.

Thereareexceptionstothiscycle,includingtheformationofmushroomsbycoloniesderivedfromindividualspores(suchastheaforementionedinkcapstudiedbyBrefeld)andtheproductionof(p.12) mosaicmushroomsbymultiplepartners.Themajorityofspecies,however,requiresexbetweentwoconsentingcolonies.Experimentalpairingsofsporescapturedfromsinglemushroomsprovidevaluableinsightintotheunderlyinggeneticcontrols.Inmostcases,onlyone-fourthofthesesiblingcrossesaresuccessful,leadingtotheformationofadikaryon;three-fourthsofthetimethemushroomsbeingmoresophisticatedthanEuropeanroyaltythepairingsfail.Outcrossingisfavored,forallofthegoodreasonsthatlimitinbreedingelsewhereinnature.ButwhilethePopeinsiststhatallofhumanityisordainedheterosexual,KingdomFungihavetakenamorecatholicapproachtogender.Asinglemushroomspeciescanembracetensofthousandsofgeneticallydistinctsexes,andalmostallofthemcan,anddo,matewithoneanother.Maleandfemalearemeaningless.Aslongasonedoesnttrytohavesexwithanest-mate,cellfusionissanctioned.10Thereasonforthislibertinismmaybethatthechanceofmeetinganothercolonyofonesspeciesisquitelimited,duetotheprevalenceofinfantmortalityamongmushroomsdiscussedearlier.Sowhenahyphatouchesahyphainthemoistdarknessofthesoil,cellwallsdissolve,fluidsmerge,andnucleimingle.

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GermanandFrenchscientistsusingthelatestmicroscopetechniquesmademostoftheadvancesinunderstandingfungaldevelopmentinthenineteenthcentury.OscarBrefeldwasoneofthecentralplayers,thoughheisntaswellknownashismentor,HeinrichAntondeBary,whose1866textbook,MorphologieundPhysiologiedePilze,markedthebeginningofmodernmycology.11TheirFrenchcontemporaries,thebrothersLouis-RneandCharlesTulasne,discoveredthatsinglespeciesoffungicouldformdifferentkindsofspores,andtheypresentedtheirfindingsinexquisitelyillustratedfolios.12Thesexualbehaviorofthefungiwasacrucialtopicofexplorationbythemajorpractitionersofmycologyinthenineteenthcentury,andwhereverthecurtainswereopened,themechanicsseemedto(p.13) involvethegentlefusionofcoloniesratherthanthesemen-on-eggsrecipeforreproducinganimals.ThemushroomlifecycleproveddifficulttocrackanditremainedanenigmauntilWorldWarI,due,inpart,tothemisdirectedimaginationofanamateurmycologistinEnglandcalledWorthingtonG.Smith(Fig1.4a).Smithclaimedthathisrelentlessmicroscopicobservationrevealedthatmushroomsdroppedpacketsofspermcellsontothesoilthatejaculatedovertheirspores.Theeffortinvolvedinapprehendingthenonexistentspermcellsisevidentfromhisdescription:

Atfirstitrequireslongandpatientobservationtomakeouttheformofthesebodiessatisfactorily,butwhenthepeculiarshapeisoncecomprehended,thereislittledifficultyincorrectlyseeingtheircharacteristicform.13

ThemostlikelyexplanationforSmithserroristhatheconfusedcontaminatingprotists,single-celledorganismswithahairlikecilia,protrusion,formushroomsperm.Thisconclusionissupportedby(p.14) hisadmissionthatheaddedtheexpressedjuiceofhorsedung,hardlythecleanestoffluids,tokeephismicroscopepreparationshydrated.

Fig.1.4 Britishmycologists.(a)WorthingtonG.Smith(18351917),eccentricmycologistandarchaeologist.(b)ElsieMaudWakefield(18861972),graduatestudentwhoshowednecessityforsexbetweencoloniestoproducemushrooms.(a)PhotographfromTheNaturalHistoryMuseum,London,withpermission.(b)FromC.G.Lloyd,MycologicalNotes7(1924).

Fromafieldofstrongcompetitors,itseemsfairtojudgeWorthingtonSmithasoneofthemostcolorfulfiguresinBritishmycology.Smithtrainedasanarchitectbutbecamea

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celebratedillustratoroffungi,aswellasaninfluentialarchaeologist.Hesaidthatheadoptedthestudyoffungiasamentalexercise,sometimeafterpoisoninghimselfandhisfamilybyeatingEntolomasinuatum.Smithhadmistakenthisforanediblespeciesand,addingtotheunsavorinessofthestory,keptthemushroomsunderaglassbellfortwodaysbeforecookingtheminbutter.Afterlunch,hesetofffromhishomeinKentishTownforthecity.Waitingforthetrain,hewasovertakenbyastrange,nervous,gloomy,low-spiritedfeeling,quitenewtome,thenasevereheadacheaddeditscharmstomyfeelings.Stomachpainsdevelopedonthetrainandvisualhallucinationsathisdestination.Returninghome,hefoundhiswifeanddaughterweakfromvomitingand,overcomewithdrowsiness,Smithsleptfortwelvehours,dreamingoftoadstoolsadvancingandretreating,increasinginsizeanddiminishinginanendlessmazepoisonedchildren,deadfathersandmothers.HedetailedtheexperienceinanarticlepublishedintheJournalofBotanyand,in1867,publishedaguidetomushroomidentification.14

Thebefuddledpictureofmushroomsexualitybequeathedbynineteenth-centurysciencewassweptaway,finally,byElsieMaudWakefield,atwenty-three-year-oldOxfordgraduatewhowasstudyinginMunich.(Fig1.4b).Evidencethatmatingwasnecessarytoproducemushroomsemergedfromherexperimentswithcoloniesproducedfromsinglespores:certaincrossesresultedinfruiting,whileothersremainedbarren.15Wakefieldwasapioneeringscientist,(p.15) oneofthefirstwomentobecomeaprofessionalmycologist,andsheservedastheHeadofMycologyatKewforfortyyears.HerimportanceinthischapterderivesfromherliberationofthemushroomlifecyclefromWorthingtonSmithssemen.Aftercoloniesmerge,theircomminglednucleiserveasgametesbutdelayfusinguntilthemushroomismature.Thepairsofnucleiremainpartnered,withintouchingdistance,ineachcompartmentofthedikaryonfordays,months,orevenyears.Thisextendedforeplayisoneofmanycharacteristicsthatsetthemushroom-formingfungiapartfromtherestoflifeonearth.Bycommittingearly,Isuppose,thecouplecangrowandfeedtogether,andthenshareintheformationofmushroomsfordispersingtheiroffspring.Thefinalactofnuclearfusionoccursonlyinthecells,calledbasidia,thatgeneratethesporesonthegills.

Theemergenceofamushroomfromthecolonyoffeedingfilamentsbeginswithaknotofhyphae.Asthispinhead-sizedcongregationofcellsenlarges,thestem,cap,andgillsbecomevisible,primingthedevelopingembryo,orbutton,forrapidexpansionintothematurereproductiveplatformassoonasenvironmentalconditionsareright(Fig.1.5).

AsImentionedearlier,weknowverylittleabouthowanyofthishappens.Allanimalsshareacatalogofgenesthatdeterminethepositionswhereheadsandtailsandallofthestuffinthemiddledevelop.Differentversionsofthesegenes,withnameslikeHedgehogandNotch,encodeproteinsthatparticipateinsignalingpathwaysthatspecified,whenyouwereanembryo,thatyouranuswouldbeplantedtowardyourtailratherthanthemiddleofyourforehead.Atbest,theeffectsofgenemutationspredicategrossunpopularityoutsideacircustentorjarofformaldehyde.Becausethesekindsofdevelopmentalgenesareubiquitousamonganimals,itseemssensibletolookforrelatedgenes,orhomologs,thatmightplaysimilarrolesindeterminingtheformationofcapsand

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stemsinmushrooms.(p.16) Exhaustivesearchesoffungalgenomes,however,findthattherearenosuchhomologsinamushroom.16Mushroomshearadifferentdrummer.17

Fig.1.5 Developmentoftheink-capmushroomCoprinopsiscinerea.(a)Primordiumshowingminiaturecapandstemsurroundedbyprotectivehyphae.(b)Slicethroughmaturefruitbodythatexpandsfromtheprimordiuminafewhours.BasedonimagesinD.M.Moore,FungalMorphogenesis(Cambridge:CambridgeUniversityPress,1998).

Computersimulationsareeffectiveatgeneratingvirtualmushroomsfromgroupsoffilamentswhosebehaviorisgovernedbyahandfulofrules.18Theserulesincludethedegreetowhichneighboringfilamentsattractorrepeloneanotherastheyextend,thefrequencyofbranching,theanglesatwhichthosebranchesgrow,andthegravitationalresponseofallofthegrowingtips.Thepowerofthemodelliesinthefactthatsofewrulescanspecifyamushroom.(ThisisanapplicationofOccamsrazorincomputermodeling:Pluralityshouldnotbepositedwithoutnecessity.)Forinstance,ifwespecifiedthebehaviorofeachfilamentseparately,thenthevirtualmushroomwouldtellusnothingmorethanapaintingoraphotographoftherealthing,butwhatthecomputer(p.17) simulationsshowisthatthiskindofmanipulationisntnecessary.Bycontrollingafewparametersandapplyingthesetoallofthefilamentsatonce,andthenchangingthemandreapplyingtoallofthefilaments,abeautifulcyberboletecanbegrown(Fig1.6).Thisisanimportantdiscovery,becauseitmeansthattheapparentcomplexityoneseesinthewoods,orinthepagesofamushroomguidebook,mayemergefromarelativelysimplesetofcontrols.

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Fig.1.6 Computer-simulatedmushroomprimordia.FromA.Mekauskas,L.J.McNulty,andD.Moore,MycologicalResearch108,341-353(2004),withpermission.

Thecomputersimulationsalsohintatthereasonthatthekindsofdevelopmentalgenesubiquitousamonganimalsareabsentinthefungi.Accordingtothemodels,adevelopmentalclockdictatingtheexpressionofsuccessivewavesofcellattractionandrepulsionmightbesufficienttoshapeeverythingfromamushroomwithdelicategillstoafatbracketstickingoutofadyingtree.Havingadvancedthispossibility,however,investigatorsstillneedtoidentifythecellbiologicalmechanismsthatenablehyphaetosensethepositionoftheirneighbors(foronecelltogrowawayfromitsneighbor,itmustbeabletosenseitspropinquity),controlbranching,andperceivegravity.And,toindicatetheenormityoftheknownunknowns,wearenowhereclosetopinpointingthegenesthatdistinguishthefruitbodiesofthe16,000speciesofmushroomfromoneanother.Generationaftergeneration,withunwavering(p.18) fidelity,coloniesofscarlet,parrot,lemon,olive,scented,stinking,ivory,andvermillionwaxcaps(speciesofHygrocybe)formtheirownversionsofthick-gilledmushrooms.Someofthenamesofthesemushroomsrefertovariationsincolororodor,butthedifferencesgomuchdeeper.Theshapesofthefruitbodiesarehighlydistinctive,fromthepointedcapofthewitchshat(Hygrocybeconica,plate3),totheflatterformofthelemonwaxcap(Hygrocybechlorophana),andtheslimybellsoftheirrelative,theparrotwaxcap(Hygrocybepsittacina).Beneaththemushroomcap,therearevariationsingillthicknessandspacingthatarepatentedbyeachspecies,alongwithdifferencesintheshapeandsizeofthecellsthatprojectfromthegillsurfacesandofthesporeswhoseproductionistheraisondtreoftheentireorgan.

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Plate3 Hygrocybeconica,thewitchshat.Thestemofthismushroombecomesblackenedwhenbruised.Manyguidebookslistthisaspoisonous,butadventurousmycologistscontinuetodebateitsedibility.PaintingbyJohnAugustusKnapp,courtesyofLloydLibraryandMuseum,Cincinnati.

Cellscalledbasidiaformattheendsofhyphaewhosetipsstopgrowingatthegillsurface.Likethebillionsofothercompartmentswithinthefleshofthemushroom,theyoungbasidiacontaincopiesofthepairofnucleiderivedfromtheparentcolonies.Thesefuseandthenundergomeiosis(thedividingmechanismthatcreateseggsandsperminanimals)toproducefourgeneticallydistinctnuclei,eachofwhichispackagedintoaspore.Thematurebasidiumlooksabitlikeacowudderwithaquartetofsporesarrangedontheteats.(Sporesandbasidiatakecenterstageinthenextchapter.)Oncetheyescapefromthemushroom,thesesporespopulatetheinvisiblebiologyoftheairandtheirdepositioninasuitableplacecompletesthefungallifecycle.Spores,colonies,matedcolonies,mushrooms,andmorespores.

Sunlighttriggerssomeofthestepsinmushroomformation,includingtheinitiationprocessandtheformationofspores,butitdoesnotdictatetheorientationofamushroomcapinthewaythatlightcontrolsplantgrowth.Afterall,lackingtheabilitytopowersugarproductionbyabsorbingphotons,fungihaveevolvedtofeed(p.19) indarknessonthefruitsofplantphotosynthesis.Instead,gravityistheenvironmentalsignalofparamountimportancetoamushroom.Thereasonforthisisapparentwhenwerememberthatmushroomsareplatformsforsporedispersal.Oncethesporesaredischargedfromthegills,theyfallverticallyfromthebottomofthecapandaredispersedbytheairflowswirlingaroundthefruitbody.Ifthemushroomdoesntdevelopinanuprightposition,itsgillspointingstraightdown,thesporeswillneverescapeandthefungushasnochanceofsendingitsgenesintothealwaysuncertainfuture.Gravityiseverythingforamushroom.Moreonthisinthenextchapter,buttheevidenceforgravitationallyinspiredgrowthisdisplayedinthearrangementofthespore-producingtissuesineverymushroom.Theprecisearrangementofthegillsunderthecapcanbeexaminedbylookingatamushroominagrocerystoretheyareformedinthismannerbecausethecultivatedmushroomtakesitscuesfromgravity.Thestemofthemushroomissimilarlysensitivetogravityandthestemofadevelopingmushroomdisplacedhorizontallywillembarkuponaright-angledturntokeepitsgillspointingdown.

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MushroomsgrownontheSpaceShuttlebecomedisorientedandformtwistedstemsastheylookforthecenteroftheearth.19Suchcrueltyis,sadly,anunpleasantpartofthespaceprogramasanyprimate,asidefromtheoneswithmilitaryhaircuts,willtestify.

Withtheexceptionofthecellsthatformthesporesonthegillsurface,allofthecomponentsofamushroomarecapableofabandoningtheirvocationwithinthefruitbodyandseedinganewcolony.Hyphaecutfromamushroomcaporstemwillfashionafeedingcolonyiftheyareplacedonagarinaculturedish.Thistransformationisprobablyarareeventinnature,butthefactthatthecellsinamushroomnevergiveuptheirdevelopmentalflexibilityisanotherofthoseremarkablefeaturesofthefungithatjustifytheirdistinctionasaseparatekingdomoflife.Almosteverycellinamushroom(p.20) isastemcell.20Millionsofthemrunupanddownthestemandmillionspointsidewaysintheexpandedcap;someformsphericalcompartmentsinthefleshofthegills,others(calledcystidia)pokefromthegillsurfaceandformFrench-ticklertips.Positionseemstobeeverything.

Themechanicalprocessofexpansionplaysanimportantroleindetermininghyphalorientation,becausethecellsareyankedintopositionastheembryoinflates.Theterminflationisappropriateformushroomdevelopmentbecausethedramaticovernightappearanceofthefruitbodyonalawn,oranywhereelse,isnotassociatedwithanincreaseinthenumberofcells.21Theprocessishydraulic,involvingtheuptakeofwaterintoallofthepreexisting,preorganizedcellsfromtheyoungeststagesoffruit-bodydevelopment.Forthistooccur,thecellwallsofthehyphaeloosenandwaterinfluxoccurspassivelybyosmosis.Thisisabeautifullysimplemechanisminphysiologicalterms,nothinglikethegrowthanddifferentiationentailedinhumanembryogenesis.Mushroominflationinvolveslimitedgeneexpressionandfinishesinafewhours.Becausethewallsofthehyphaeinthemushroomdonotexpandindefinitely,theybecomepressurizedbythiswaterinflux.Thispressure,calledturgor,inducestensionbetweenthedifferenttissuesinthefruitbody,causingthestemtoelongateandthecaptoexpandoutwards,displayingthegills.Anygravitationallyurgedcurvatureofthestemiscontrolledbydifferentialrelaxationamongthehyphaethatoccupytheoutermostrindofthestem,whiletheinnermostcellscontinuetoproducetheelongatingthrust.Theexertionofasmuchasoneatmosphereofthispressurealsopowerstheemergenceofthefungusfromsoilorrottingwood.22Intheurbanenvironment,thisallowsfungitoliftpavingslabsandcrackasphalt.Intheindoorenvironment,aclusterofmushroomsbeneathyourseatcushionwouldexertsufficientforcetoraiseyou,(p.21) thecatsleepingonyourlap,andyourbrandyballoonafewinchesaboveyourleatherarmchair.23

Byseekingtopaintapictureofmushroomdevelopmentinfairlybroadbrushstrokes,thischapterhasdescribedtheformationofanaverage-lookinggilledmushroom.Thereare,however,allmannerofvariationsonthismodel.InspeciesofAmanita,includingthelethaldeathcap,thebuttonstageiswrappedinacontinuouslayeroftissuecalledtheuniversalveilthatistornapartasthemushroomexpands.Thistissueappearsasremnantsintheformofspots,orscales,onthecap,andcup,orvolva,atthebaseofthestem(fig1.7).Asecondveil,calledthepartialveil,coversthebottomedgeofthegillsandthissplitsaway

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fromtheouteredgeoftheexpandingcapandhangsdownasaringonthestem.Ihavefocusedhereonmushroomswithgills,butmushroomsalsofoldtheirspore-producingtissuesoverridgesbeneaththeircaps,orteeth,orwithintheinnersurfaceoftubes.Otherspeciesdisplaytheirsporesonexposedsurfaces,forming(p.22) mushroomsthatresemblelittlecorals.Stinkhornsandcagefungismearsporesinodorous,insect-attractingpasteonphallicheadsoroverthebarsofcages.Puffballsandearthstarsproducetheirsporeswithinthechambersoftheirlabyrinthineinnards,whilebirdsnestfungiandtheartilleryfungusfashionpacketsofsporesthatresembleminiaturepuffballs.Despitethisastonishingdiversityofforms,allfruitbodiesbeginlifeasaprimordialknotofhyphaethatshowsrapid,hydraulicallypoweredexpansion.Unfortunatelylittleisknownabouttheenvironmentalcuesthatinitiatethisamazingprocess.

Fig.1.7 Originofthemushroomvolvaandring.(a)EmergenceofAmanitaphalloidesshowingoriginofbasalcup,orvolva,fromtornuniversalveilthatwrappedaroundtheentiremushroom.(b)EnormousfloppyringonstemofAgaricussilvicolahangingbeneaththegillsthatitcoveredasapartialveil.Source:(a)FromR.D.delaRivire,LePoisondesAmanitesMortelles(Paris:Masson,1933),(b)Author'sphotograph.

Temperatureandrainfallarethemostobvioussignalsthatmaydictatemushroomemergence.Theappearanceofmushroomsafterrain,ratherthaninthedeadofwinter,isamatterofcommonobservation.Butitsnotassimpleas:rain+warmth=fruiting.AmushroomunfurlingitsgillsinthewoodsonarainymorninginSeptemberwillalsopopuponthesamedaymanymilesawayinanislandoftreesinthemiddleoffarmland.Thisprecisecalendarisafeatureofmanyspecies.Formushroomswhosecoloniesareassociatedwithtreerootsmycorrhizalpartnersordestructiveparasitesthetimingmaybecontrolledpartlybythephysiologyofthehost.Yetspeciesthatfruitonlogsdothesamething,developingacrossawidegeographicareaduringasingleweekeachyear.Thissuggeststhatemergencemaybefacilitatedbymoisturebutallowableonlywhenamultitudeofothervariablesareinplace,includingpermissivesoiltemperature,changesindaylength,andthepulseofnutrientssuppliedbyleaffallintemperateregions.

Mushroomcolonieshavecomplexdietaryrequirements.Nitrogenisacriticalelementbecauseitisinshortsupplywithinmanyofthefoodsourcespreferredbyfungi,ranging,forexample,fromonepartinonehundredtolessthanonepartinonethousandinwood.Estimatessuggestthataone-kilogrambracketfungusneeds(p.23) toharvestallofthe

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nitrogenfrom14kilogramsoftimbertosupportitsannualsporeproduction.Thisillustrateswhycoloniesofsomespeciesmustspreadoverlargeterritoriesbeforeproducingmushrooms.Coloniesthatliveforhundredsoreventhousandsofyearscanaffordtobesparingintheirannualinvestmentinsporeproduction,sheddingsomeoftheirgainswhilemaintainingahealthyfeedingcolonywithintheforestsoil.Aradicallydifferentstrategyistheapproachtakenbyacoprophilousfungusthatlivesanddiesinasteamingmoundofelephantdung.Thingsaregoodforawhile,butbeforelongallofthecaloriesinthisbeetle-riddledmonumenttodefecatoryexcesswillbegoneandafreshdeliveryinthesamespotunlikely.Theindividualcolonycannottravelbeyondthedungandtheonlychanceforsendingitsgenesintothefutureliesinpackagingsporesandreleasingthemintothewind.Itmakessense,therefore,forthiscolonytoloadasmuchofitsresourcesaspossibleintosporesandtodispersetheminsearchoffreshdung.

Notacomfortablebedtimestory,isit?Thefungusislikeahopefulparent,upearlyinthemorningtosendthechildrenoffwiththeirlunchboxesintoaworldoftremendousuncertaintyandthekidscanneverreturnandMummyshrivelstodeathbeforesundown.OhDarwin,youwereawickedman!Theproblemwiththismetaphoristhatthenotionoftheindividual,somethingthatseemssoobviouswhenthinkingaboutanimals,ismorecomplexforafungus.ThatbigthingswimmingoffCapeCodisawhaleandthatotherbigthingsnoringinthearmchairagainisaprofessor.Forafungus,themushroomisonlythemostvisiblepartofthemicroorganismwhosecolonyspreadsunderground.Theindividualfungusisthecolonyandallofitsmushrooms.Youcanestimatethesizeoftheindividualbysamplingthecolonyatvariouspointsandcheckingtheidentityofthefilamentsbyamplifyingtheirgenes,butitisimpossibletotellhowmuchofthewoodlandcolonyisshiftedtothesurfacein(p.24) theformofmushrooms.Studiesoffungiinculturesmakethistaskslightlyeasier.Thesimpleansweristhatagooddealofthecolonyisshiftedtothesurfaceintheformofmushroomsbymobilizingnutrientsfromdistantpartsofthecolonytowardaseriesoffocifromwhichthefruitbodiesdevelop.

ASwissstudyshowedthatthenumberofmushroomsproducedbyupto194differentspeciespeakedinresponsetoabundantrainfallandthatcoolertemperaturesinJulyandAugustpredictedanearlybeginningtothemushroomseason.24Detailedstudiesofhistoricalfruitingpatternshaveshownthatthecalendarforfungalreproductionhasshiftedinrecentdecades.RushLimbaugh,anAmericanradiotalkshowhost,hasexplained,Despitethehystericsofafewpseudo-scientists,thereisnoreasontobelieveinglobalwarming.25Mushroomsholdadifferentviewpoint.InsouthernEngland,forexample,astudyoftensofthousandsofrecordsoffruitingshowedthatthedurationofthefallmushroomseasonhasmorethandoubledsincethe1950s.26ThebehaviorofthefungicorrelateswithwarmertemperaturesinAugustandmoreraininOctober.InNorway,fruitinghasbeendelayedbyanaverageoftwoweeksinthelast60years,withparticularlywarmweatherinfallandwinterpostponingfruitinginthesameyearandinthefollowingyear.ThereasonfortheapparentstretchingofthemushroomseasoninEnglandanditscompressioninScandinaviaisnotknown,butsuchdramaticeffectsonfungalreproductionaddtothemelangeofforebodingindicatorsaboutourchangingclimate.Morealarmingthanchangesinthefallfruitingcalendar,perhaps,isthefinding

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thatsomespecieshavebeguntofruitinthespringandinthefall.Theeffectismostpronouncedamongwood-decaybasidiomycetes,whichsuggeststhatdecompositionisaccelerating.Theecologicalconsequencesofthesechangesarelikelytobeprofound.Butone(p.25) mustremember,accordingtoMr.Limbaughandcolleagues,climatechangeisahoax.

Dismissalofrationalityinfavorofsuperstitionandwishfulthinkinghasbeenanenduringhallmarkofhumanity;weareagulliblespecies,predisposedtolookingforsimpleanswerstocomplexquestions,andfindingwitches,ghosts,andgodsatthemerestprovocation.Itisnotsurprising,therefore,thatmushroomshavebeenlinkedtotheoccultformillennia.Thehallucinatorypropertiesofahandfulofspecieshasledtotheirworship(Chapter7),andthetoxicityofotherstovilificationinfolklore(Chapter6),buttheirficklebehaviorandsuddenerectionshavesurelyencouragedthesesupernaturalassociations.WhileIdonthavemuchpatienceforthesupernatural,Iamawestruck,sometimesoverwhelmed,bythesightofaringoffreshmushroomsinadewymeadow,hugeboletesprotrudingfromwetbanksofforestsoil,ortheflashofpyrotechnicyellowamongrottinglogsthatadvertisesthefirstsulfurshelf,Laetiporussulphureus,oftheyear.Thisisanexpressionofludicroussensitivityratherthanevidenceofspirituality,butperhapstheyarethesamething.IhavearecurringdreaminwhichIfindmyselfinamagicalgarden,amoss-carpeted,pullulatingEden,wherethemerethoughtofamushroomisrewardedbyitsimmediateappearance.

Ihavenightmaredtoo,ofanuclearholocaust,watchedthemushroomcloudsroaronmyunconscioushorizon,andsegued,notsurprisingly,totheirlivingmimics,transformingtheapocalypseintoahallucinatoryforaybeneathtoweringfungi.Theircolonieshavetunneled,metaphorically,throughoutmybrain.Iknowthatentomologists,bryologists,andany-other-ologistsaresimilarlyexcitedbytheirchosenslicesofbiodiversity,butthereissomethingparticularlystrangeaboutthefungalkingdom,somethingalientooursenseofhowtherestoflifeisarranged.Mycology(p.26) isarareobsession,compared,forexample,withastronomyorbirdwatching;buttherearemanythousandsoffellowworshipers,Ihope,forwhomthemushroom-scentedforestisasecularcathedral.Ratherthandiminishingthemagic,thedismissaloffairiesandelves,thisscientificunweavingoftherainbow,intensifiesthebrillianceofnaturesmasterpiece,themushroom.Andthatiswhatthisbookisfor.

Notes:(1.)Recentpapersonthesubjectofbasidiosporedispersal:D.-W.Li,MycologicalResearch109,12351242(2005);B.NordnandK.-H.Larsson,NordicJournalofBotany20,215219(2008);N.HallenbergandN.Kffer,NordicJournalofBotany21,431436(2008).

(2.)R.W.WilsonandE.S.Beneke,Mycologia58,328332(1966).

(3.)E.Lax,TheMoldinDr.FloreysCoat:TheStoryofthePenicillinMiracle(NewYork:HenryHolt,2004).

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(4.)M.Malpighi,AnatomePlantarum(London:JohannisMartyn,16751679).

(5.)P.A.Micheli,NovaPlantarumGenera(Florence:BernardiPaperinii,1729).

(6.)ThesignificanceofPrvostsworkisdescribedinN.P.Money,TheTriumphoftheFungi:ARottenHistory(NewYork:OxfordUniversityPress,2007),103108.

(7.)O.Brefeld,BotanischeUntersuchungenberSchimmelpilze(Leipzig:A.Felix,18721912).

(8.)PotterspaintingsarereproducedinW.P.K.Findlay,WaysideandWoodlandFungi(London:FrederickWarne,1967).

(9.)C.SchmittandM.L.Tatum,TheMalheurNationalForest.LocationoftheWorldsLargestLivingOrganism[TheHumongousFungus](USDAForestService,PacificNorthwestDivision,2008).Thelargestindividual(colony)isestimatedtoweighbetween7,600and35,000tons.

(10.)Herearesomedetails.Dikaryonsformwhencompatiblemonokaryonsfuse,andcompatibilityisdeterminedbyapairofmating-typegenes,whicharedesignatedAandB.Insomefungi,therearehundredsofdifferentversions,oralleles,ofeachmatingfactor.Incompatiblereactionsoccurwhenmonokaryonsthatshareoneorbothmatingtypeallelesattempttofuse:A1B1xA1B1,A1B1xA1B2,orA1B1xA2B1dontwork.InanA1B1xA2B2cross,andhundredsorthousandsofothercrosses,however,afullyfunctioningdikaryonisproduced,andthishasthepotentialtogenerateafertilefruitbody.Whenacompatiblereactionoccurs,nucleifrombothmatingtypesmigratethroughoneanotherscolonies,convertingthemonokaryonintoadikaryon.Thisprocessistermeddikaryotization.

(11.)A.deBary,1887.ComparativeMorphologyandTaxonomyoftheFungiMycetozoaandBacteria,Englishtranslation(Oxford:ClarendonPress,1887).

(12.)L.R.TulasneandC.Tulasne,SelectaFungorumCarpologia,3vols.,translatedbyW.B.Grove,editedbyA.H.R.BullerandC.L.Shear(Oxford:ClarendonPress,1931).SeekcopiesoftheoriginalvolumespublishedinParisbetween1861and1865forthebreathtakingluminosityofthefirstprintingoftheillustrations.

(13.)W.G.Smith,Grevillea4,5363(1875);thequoteisfromp.60.

(14.)W.G.Smith,JournalofBotany2,215218(1864);W.G.Smith,MushroomsandToadstools:HowtoDistinguishEasilytheDifferencesBetweenEdibleandPoisonousFungi:WithTwoLargeSheetsContainingFiguresofTwenty-nineEdibleandThirty-onePoisonousSpeciesDrawntheNaturalSizeandColouredfromLivingSpecimens(London:R.Hardwicke,1867).

(15.)E.M.Wakefield,NaturwissenschaftenZeitschriftfrForst-undLandwirtschaft7,521551(1909).

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(16.)D.MooreandA.Mekauskas,MycologicalResearch110,251256(2006).

(17.)J.W.TaylorandC.E.Ellison,PNAS107,1165511656(2010).Complexmulticellularitymayhaveevolvedseveraltimesamongtheeukaryotes,withseparatedevelopmentalmechanismsarisingintheanimals,plants,ascomycetes,andbasidiomyctes.

(18.)A.Mekauskas,L.J.McNulty,andD.Moore,MycologicalResearch108,341353(2004);N.P.Money,Nature431,32(2004).

(19.)D.Mooreetal.,MycologicalResearch100,257273(1996).

(20.)N.P.Money,BioEssays24,949952(2002).

(21.)Theinflationofpre-existinghyphaeappearstobesufficienttoaccountforstemandcapexpansioninsomemushrooms,whilethecontinuousproliferationofhyphalbranchesoccursduringthedevelopmentofotherspecies.D.Moore,inPatternsinFungalDevelopment,editedbyS.-W.ChiuandD.Moore(Cambridge:CambridgeUniversityPress,1996),136.

(22.)N.P.MoneyandJ.P.Ravishankar,MycologicalResearch109,627634(2005).

(23.)Thetipsofindividualhyphaecanapplymaximumpressuresof1or2atmospheresastheypenetraterottingwoodorotherfoodsources.Hyphaeexertanaveragepressureofabouttwo-thirdsofanatmospherewhentheyarebundledintothestemsofmushrooms,allowingthefruitbodytopushthroughsoilandemergeintotheair.Adensepatchofmushroomsgrowingfromareaof0.01m2exertingtheaveragepressureproducesatotalforceof676N.Thestrongestmushroomscanraiseasnoozingreaderplusbrandyballoonpluscatwithacombinedmassof73kgandgravitationalforceof715N;theaveragemushroompatchcannotdosountilthe4-kgcatjumpsfromthereaderslap,reducingtheloadby39N(to676N).

(24.)G.Straatsma,F.Ayer,andS.Egli,MycologicalResearch105,515523(2001).

(25.)Mr.LimbaughcontinuestoexpressthisopiniononhisradioshowtwodecadesaftercommittingthistoprintinR.Limbaugh,See,IToldYouSo(NewYork:PocketBooks,1993).

(26.)H.Kauserudetal.,PNAS105,38113814(2008).

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