Epidemiology of Mycotoxin Producing Fungi: Under the aegis of COST Action 835 ‘Agriculturally Important Toxigenic Fungi 1998–2003’, EU project (QLK 1-CT-1998–01380)

132 Pages·2003·1.8 MB·English

by  Antonio Logrieco

EPIDEMIOLOGYOFMYCOTOXINPRODUCINGFUNGI
Epidemiology of Mycotoxin Producing Fungi
Under the aegis of COST Action 835 ‘Agriculturally Important
Toxigenic Fungi 1998–2003’, EU project (QLK 1-CT-1998-01380)
Edited by:
X. Xu, J.A. Bailey and B.M. Cooke
ReprintedfromEuropeanJournalofPlantPathology,Volume109,Issue7,2003
SPRINGER-SCIENCE+BUSINESS MEDIA, B.V.
AC.I.P.CataloguerecordforthisbookisavailablefromthelibraryofCongress
ISBN 978-90-481-6387-8 ISBN 978-94-017-1452-5 (eBook)
DOI 10.1007/978-94-017-1452-5
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Coverphoto:
BleachingofwheatspikeletscausedbyFusariumHeadBlightdisease.
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©2003Springer Science+Business Media Dordrecht
Originally published by Kluwer Academic Publishers in 2003
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Contents
Foreword vii
EpidemiologyoftoxigenicfungiandtheirassociatedmycotoxinsforsomeMediterraneancrops 645–667
A.Logrieco,A.Bottalico,G.Mule´,A.MorettiandG.Perrone
Modellingplantdiseaseepidemics 669–682
A.vanMaanenandX.-M.Xu
EffectsofenvironmentalconditionsonthedevelopmentofFusariumearblight 683–689
X.Xu
Moleculartoolstostudyepidemiologyandtoxicologyoffusariumheadblightofcereals 691–703
P.Nicholson,E.Chandler,R.C.Draeger,N.E.Gosman,D.R.Simpson,M.ThomsettandA.H.Wilson
EpidemiologyofFusariumdiseasesandtheirmycotoxinsinmaizeears 705–713
G.P.Munkvold
Epidemiologyoftoxin-producingfungiandochratoxinAoccurrenceingrape 715–722
P.Battilani,P.GiorniandA.Pietri
Post-harvestfungalecology:Impactoffungalgrowthandmycotoxinaccumulationinstored 723–730
grain
N.Magan,R.Hope,V.CairnsandD.Aldred
StrategiesforthecontrolofFusariumheadblightincereals 731–742
S.R.Pirgozliev,S.G.Edwards,M.C.HareandP.Jenkinson
MajorchangesinFusariumspp.inwheatintheNetherlands 743–754
C.Waalwijk,P.Kastelein,I.deVries,Z.Kere´nyi,T.vanderLee,T.Hesselink,J.Ko¨hlandG.Kema
InfluenceofclimaticfactorsonFusariumspeciespathogenictocereals 755–768
F.M.Doohan,J.BrennanandB.M.Cooke
AssociationofFusariumspeciesinthewheatstemrotcomplex 769–774
T.Pettitt,X.XuandD.Parry
EuropeanJournalofPlantPathology109:vii,2003.
Foreword
Mycotoxins continue to be a very serious threat to human health and a major concern for those entrusted with
regulatingthesafetyoffoodandfoodproducts.Infectionofcerealsandothercrops,notablegrapevine,byFusarium,
AspergillusandPenicilliumareaworld-wideproblemandrecentepidemicsinEurope,theUSAandCanadahave
focusedattentiononthisproblem.ApreviousSpecialIssueoftheEuropeanJournalofPlantPathology(108(7)
2003)wasconcernedwiththenatureofthesetoxinsandthefungithatcanproducethem.
The aim of this publication is to review the environmental factors that influence the success of these fungi as
pathogens and as organisms affecting stored products, and to discuss how these factors can also influence the
amountsoftoxinthataccumulate.ThesereviewswereoriginallypresentedataWorkshopoftheEUCOSTAction
835entitled‘AgriculturallyImportantToxigenicFungi’(ChairpersonAntonioLogrieco,Bari,Italy),heldinEast
Malling,UKattheHorticulturalResearchInternationalinSeptember2002.Wehopetheinformationprovidedwill
stimulatescientistsworld-widetoassesstheriskoftoxinsaccumulatinginplantsunderarangeofenvironmental
conditionsandthatthiswillprovideaninsightintohowtheaccumulationofthesetoxinscanbekepttoaminimum.
XiangmingXu
JohnBailey
MichaelCooke
EuropeanJournalofPlantPathology109:645–667,2003.
©2003KluwerAcademicPublishers.
Epidemiology of toxigenic fungi and their associated mycotoxins
for some Mediterranean crops
AntonioLogrieco,AntonioBottalico,GiuseppinaMule´,AntonioMorettiandGiancarloPerrone
InstituteofSciencesofFoodProduction,CNR,vialeEinaudi51,70125Bari,Italy
(E-mail:[email protected])
Keywords:Fusarium-diseases,Alternaria-diseases,Aspergillus-diseases,Penicillium-diseases,trichothecenes,
fumonisins,zearalenone,moniliformin,fusaproliferin,beauvericin,enniatins,tenuazonicacid,alternariols,
aflatoxins,ochratoxins,citrinin,patulin
Abstract
Recent data on the epidemiology of the common mycotoxigenic species of Fusarium, Alternaria, Aspergillus
andPenicilliumininfectedorcolonizedplants,andinstoredorprocessedplantproductsfromtheMediterranean
areaarereviewed.Emphasisisplacedonthetoxigenicityofthecausalfungalspeciesandthenaturaloccurrence
of well known mycotoxins (aflatoxins, ochratoxins, fumonisins, trichothecenes, zearalenone, patulin,Alternaria-
toxins and moniliformin), as well as some more recently described compounds (fusaproliferin, beauvericin)
whose toxigenic potential is not yet well understood. Several Fusarium species reported from throughout the
Mediterranean area are responsible of the formation of mycotoxins in infected plants and in plant products,
including:Fusariumgraminearum,F.culmorum,F.cerealis,F.avenaceum,F.sporotrichioidesandF.poae,which
produce deoxynivalenol, nivalenol, fusarenone, zearalenone, moniliformin, and T-2 toxin derivatives in wheat
and other small grains affected by head blight or scab, and in maize affected by red ear rot. Moreover, strains
of F. verticillioides, F. proliferatum, and F. subglutinans, that form fumonisins, beauvericin, fusaproliferin, and
moniliformin, are commonly associated with maize affected by ear rot. Fumonisins, were also associated with
FusariumcrownandrootrotofasparagusandFusariumendosepsisoffigs,causedprimarilybyF.proliferatum.
Toxigenic A. alternata strains and associated tenuazonic acid and alternariols were commonly found in black
mouldoftomato,blackrotofoliveandcitrus,blackpointofsmallcereals,andblackmouldofseveralvegetables.
ToxigenicstrainsofA.carbonariusandochratoxinAwereoftenfoundassociatedwithblackrotofgrapes,whereas
toxigenicstrainsofA.flavusand/orP.verrucosum,formingaflatoxinsandochratoxinA,respectively,werefound
in moulded plant products from small cereals, peanuts, figs, pea, oilseed rape, sunflower seeds, sesame seeds,
pistachios,andalmonds.Finally,toxigenicstrainsofP.expansumandpatulinwerefrequentlyfoundinapple,pear
andotherfreshfruitsaffectedbybluemouldrot,aswellasinderivedjuicesandjams.
Introduction raspberries), tubers and roots from temperate and
sub-tropical plants. On these host plants, pathogenic
TheMediterraneanbasinisalargegeographicalregion fungi may induce plant disease and both pathogens
withatemperateclimateandadiversifiedagricultural and saprophytes can synthesise toxic secondary
system that includes cereals (maize, rice, wheat and metabolites, which may lead to the accumulation of
other small grains), legumes (beans, peas, peanuts), mycotoxinsinthecolonisedtissues.Mycotoxinforma-
several kind of vegetables (cucurbits, solanaceous, tion may begin in preharvest infected plants standing
brassicas), citrus fruits (oranges, mandarin, lemons, inthefieldandbecontinuedorinitiatedinpostharvest
grapefruitsandlimes),pomefruits(applesandpears), and stored products. Mycotoxins in plant products
stone fruits (peaches, nectarines, apricots, plums andinprocessedfoodandfeedhaveasignificanteco-
and cherries), nuts (almond, hazelnuts, pistachios, nomic impact and pose a serious problem for animal
walnuts) olive, grapes, soft fruits (figs, strawberries, andhumanhealth(IARC,1993).Mycotoxigenicfungi
646
belong mainly to Fusarium, Alternaria, Aspergillus Type-AtrichotheceneshaveafunctionalgroupatC-8,
and Penicillium genera. The toxigenic Fusarium and other than a keto, and include: T-2 toxin (T2) and its
Alternariaspeciesareoftenclassifiedas‘fieldfungi’, derivatives (HT-2 toxin, T-2 triol, T-2 tetraol), pro-
becausetheyrequireveryhighmoisturecontentinthe ducedbystrainsofF.sporotrichioides,F.acuminatum,
substrateforgrowthandmycotoxinsynthesis(>20%). andF.poae;diacetoxyscirpenol(DAS)andmonoace-
The ‘storage fungi’, primarily species of Aspergillus toxyscirpenol(MAS),producedbystrainsofF.poae,
and Penicillium also grow well at lower moisture F. equiseti (syn. F. scirpi) (Gibberella intricans),
contents.Thus,FusariumandAlternariausuallyrep- F.sambucinumandF.sporotrichioides;andneosolan-
resent a high mycotoxicological risk in preharvested iol(NEO),producedbystrainsofF.sporotrichioides,
or freshly harvested plant that are drying, whereas F.poaeandF.acuminatum.ThetypeB-trichothecenes
toxigenicspeciesofAspergillusandPenicilliumrepre- arecharacterisedbythepresenceofacarbonylgroup
sentahigherriskforproductsinstorageorbeingused at C-8 and include: deoxynivalenol or vomitoxin
in food and feed processing. The mycotoxicological (DON) and their mono-(3-AcDON, 15-AcDON) and
aspects review here are related primarily to field and di-acetylated derivatives (3,15-AcDON), produced
storage fungal diseases of important Mediterranean by strains of F. graminearum (Gibberella zeae),
cropsandtothemycotoxinssynthesisedbystrainsof and F. culmorum; nivalenol (NIV) and its mono-
Fusarium (fumonisins, trichothecenes, zearalenones, acetylated derivative fusarenone X (FUS) and the
moniliformin, beauvericin and fusaproliferin), di-acetylated derivative (4,15-AcNIV), produced by
Alternaria (alternaric acid, alternariols, altertoxins), strains of F. cerealis (syn. F. crookwellense), F. poae,
Aspergillus (aflatoxins, ochratoxins) and Penicillium F. graminearum and F. culmorum. Trichothecenes
(ochratoxins,citrinin,patulin). can cause a variety of toxic effects in laboratory and
farm animals including skin inflammation, digestive
disorders, haemorrhagic syndrome in internal organs,
FUSARIUM DISEASES blood disorders, haemolytic imbalance and depletion
ofthebonemarrow,immunosuppression(leukopenia)
Fusariumspeciesaredistributedworldwideasimpor- anddisturbanceofthenervoussystem(IARC,1993).
tantplantpathogens,aswellasopportunisticcolonisers Trichothecenes are responsible for several mycotoxi-
of plants and agricultural commodities, or as sapro- coses in livestock, including haemorrhagic syndrome
phytesondebrisandcellulosicplantmaterials.Several causedbyAtypetrichothecenes(T2,DASandMAS),
speciescausearangeofplantdiseases,suchasvascular andemeticandfeedrefusalsyndromesassociatedwith
wilt,rootandstemrot,seedlingblight,cerealearrot, the occurrence of B type trichothecenes (DON, NIV
andfruitrot.Fusariumspeciesarealsothemajorcause andFUS).T2andDONalsohavebeenimplicatedin
ofstoragerotoffruitsandvegetablesandarefrequently humantoxicoses(ATA).However,theyhavenotbeen
associatedwithcerealandlegumegrains,whichthey proved to be genotoxic and IARC (1993) included
usuallycolonizebeforeharvest.SomeFusariumstrains the trichothecenes formed by F. graminearum,
can synthesise several mycotoxins, which may accu- F. culmorum, F. cerealis and F. sporotrichioides
mulate in infected plants before harvest or in stored amongst the compounds not yet classified for their
orprocessedagriculturalcommodities.Theoccurrence carcinogenicityinanimalsorhumans.
ofFusariummycotoxins,particularlyincerealgrainis
ofgreatconcerninallcereal-growingareas,andtheir
Zearalenones. Zearalenone (ZEA), produced
occurrenceinprocessedfeedsandfoodsisoftenasso-
by F. graminearum, F. culmorum, F. cerealis,
ciatedwithmycotoxicosesinhumansordomesticated
F. equiseti and F. semitectum (syn. F. pallidoroseum,
animals.ThemostcommonFusariummycotoxinsare
F. incarnatum), is found associated with zearalenols
trichothecenes,zearalenones,andfumonisins.Inaddi-
(ZOH) (α- and β-zearalenol isomers). ZEA is among
tion,moniliformin,beauvericin,andfusaproliferinmay
the most widely distributed Fusarium mycotoxins in
occasionallypresentproblems.
agricultural commodities and is often found at rela-
tivelyhighconcentrations,especiallyinmaize.ZEAis
Trichothecenes. Based on the functional group at bothuterotrophicandestrogenic,andmaycauserepro-
the position in the molecule C-8, the Fusarium- ductive disorders in farm animals, particularly swine.
trichothecenesmaybedividedintotwotypes,AandB. ZEAisresponsibleforrecurringtoxicosesinlivestock,
647
characterisedbyhyperestrogenisminswine,infertility in cultures of F. semitectum, F. subglutinans, and
andpoorperformanceincattleandpoultry,andthere F. proliferatum that were isolated from maize and
isapossibleimpactonhumanhealth.Thepreliminary maize-based feed. Some of these samples were asso-
scantyevidenceofthegenotoxicityofZEA,islimited ciated with animal toxicoses. In addition to its high
to mice and cultured mammalian and human cells, toxicity to insects, BEA is cytotoxic to mammalian
and it is not classified as human carcinogen (IARC, cell tissues, can cause apoptosis in both murine and
1993). humancelllinesandreducethecontractilityofguinea
pigs smooth muscle. However, the biological activity
Fumonisins. Fumonisins were first isolated from ofBEA,asfoundmoreingenerallyfortheenniatins,
F. verticillioides (syn. F. moniliforme) and then seems mediated by the ability of ionophoric com-
also found in cultures of F. proliferatum and a few pounds to affect the ion transport across membranes,
other Fusarium species with unclear ecological dis- leadingtodisruptionoftheionicbalanceofcellwall.
tributions. Amongst the characterised compounds, Such activity by BEA could increase the toxicity of
fumonisin B (FB ) and fumonisin B (FB ) present other Fusarium mycotoxins that co-occur with BEA
1 1 2 2
the greatest mycotoxicological concern. Feeds con- incontaminatedcereals.
taminated by FB cause leukoencephalomalacia in
1
Fusaproliferin. Fusaproliferin (FUP) is a novel ses-
horses,pulmonaryoedemainswine,poorperformance
terterpene produced by strains of F. proliferatum and
in poultry, and altered hepatic and immune function
F. subglutinans isolated from maize ear rot and is
incattle.Moreover,home-grownmaizecontaminated
oftenfoundinnaturallyinfectedmaize.FUPislethal
by FB has been associated with oesophageal cancer
1
to Artemia salina larvae and cytotoxic to insect and
of humans in Africa, China, and the United States.
human cell lines. FUP also caused high mortality in
Thestructuralsimilaritywithsphingosinessuggestsa
broilerchicksfedwithmaizeculturesofF.proliferatum
roleforfumonisinsasdepletionagentsofthecomplex
and had severe teratogenic effects in chick embryo
sphingolipids from biological membranes. This that
bioassays.
couldaccountfortheirtoxicityand,perhaps,theircar-
cinogenicity. However, the evidence that cultures of
F.verticillioidesandsamplesofFB canpromoteliver
1 Headblightofwheatand
cancer in rats, led to the classification of fumonisins
othersmallcereals
as carcinogenic to animals and possibly to humans
(Group2B)(IARC,1993).
Causal agents and symptoms. The species predom-
inantly found associated with head blight of wheat
Moniliformin. Moniliformin (MON) has been puri- and other small-grain cereals in the Mediterranean
fiedfromculturesofseveralFusariumspecies,includ- region are F. graminearum and its widespread teleo-
ing: F. proliferatum, F. subglutinans, F. avenaceum morph G. zeae, F. culmorum, and F. avenaceum.
(G. avenacea), and F. tricinctum. Diets containing Less frequently isolated species are F. poae,
materialnaturallycontaminatedwithMONcancause F. cerealis, F. equiseti, F. sporotrichioides, and
reduced performance, haematologic disorders, and F. tricinctum. Other species encountered sporadically
mortality in rodents, chicks, ducklings, and pigs. Its include F. acuminatum, F. subglutinans, F. solani,
significance as a contaminant of maize and other F. oxysporum, F. semitectum, F. verticillioides, and
cerealgrainshasnotbeenclarified.Atpresent,MON F.proliferatum.
is regarded as cytotoxic but not genotoxic, and has Fusarium pathogens on wheat, barley and other
yettobeassociatedwithanaturaldiseaseoutbreakin small-grain cereals, are responsible for two forms of
domesticatedanimals.MONissuspectedasthecause disease,a‘footrot’,whichaffectsrootsandcrowns,and
ofKeshandisease,ahumanheartproblemthatoccurs maycauseseedlingblightatearlystages;anda‘head
inruralregionsofChinaandSouthAfrica(Transkei) blight’(FHB),whichaffectsindividualkernels,single
inwhichmaizeconstitutesalargeportionofthediet. earspikeletsorentireheads,andresultsin‘scab’ofthe
kernels. Infected spikelets first appear water soaked,
Beauvericin and enniatins. Beauvericin (BEA) is a thenlosetheirchlorophyllandbecomestrawcoloured.
cyclic hexadepsipeptide first reported to be produced In warm, humid weather, pinkish-red mycelium, and
by some entomopathogenic fungi and then found conidia develop abundantly in infected spikelets and
648
theinfectioncanspreadtoadjacentspikeletsorthrough of several Fusarium species usually referred to as a
theentirehead.Infectedkernelsbecomeshrivelledand ‘complex’. It is not uncommon to isolate up to nine
discoloured with a white, pink, or light-brown scaly different Fusarium species from a single fragment of
appearanceasaresultofmycelialoutgrowthsfromthe infectedtissue,ortorecoverasmanyasseventeendif-
pericarp. From the mycotoxicological point of view, ferent Fusarium species from freshly harvested grain
FHB is of greatest concern, because of the potential samplescollectedinalimitedgeographicarea.How-
accumulationofmycotoxinsinscabbygrainsintended ever, only a few species are regarded as pathogenic
forfoodsandfeeds.However,theriskassociatedwith andgenerallyonlyalimitednumberdominateinany
theconsumptionofcontaminatedforageandstrawby particularhost-agroclimaticsystem.Strainsoftheless-
domesticated animals should not be underestimated. pathogenicoropportunisticFusariumspeciescanalso
FHB causes severe damage to wheat and the other produce considerable amounts of mycotoxins. Thus,
cereals, especially in areas with warm temperatures thetoxigenicprofileofacontaminatedcropisaffected
and high relative humidity or frequent precipitation not only by the predominant pathogenic Fusarium
duringtheheadingandblossomingperiods.Inaddition species, but also by the opportunistic species making
to favourable environmental conditions, other factors upthe‘complex’.TheFusariumspecies(Table1)most
involved in determining FHB severity, include agro- frequentlyisolatedfrom105samplesofcerealsgrain
nomicfactors(e.g.farmingsystems,soilmanagement (wheat, barley, rice, oat, rye, and maize) collected
andtillage,croprotationandprecedingcrop,andfungi- fromMediterraneancountries(Egypt,France,Greece,
cide applied) and host genotype, e.g. varietal disease Lebanon, Turkey, and Yugoslavia) were F. culmorum
escapeandvarietalgeneticresistancetothepathogen andF.graminearumfromwheat,F.verticillioidesand
orthetoxinsitproduces.Theetiologicalcharacteristic F. proliferatum from maize, and F. semitectum from
of FHB is the co-occurrence, or quick succession, rice(Logriecoetal.,1990c).
Table1. ToxigenicFusariumspeciesassociatedwithcerealsandtheirmycotoxins
Fusariumspeciesa Mycotoxinsb
F.acuminatum T2,MON,HT2,DAS,MAS,NEO,BEA
F.anthophilum BEA
F.avenaceum MON,EN,BEA
F.cerealis(F.crookwellense) NIV,FUS,ZEA,ZOH
F.chlamydosporum MON
F.culmorum DON,ZEA,NIV,FUS,ZOH,AcDON
F.equiseti ZEA,ZOH,MAS,DAS,NIV,DAcNIV,FUS,FUC,BEA
F.graminearum DON,ZEA,NIV,FUS,AcDON,DAcDON,DAcNIV
F.heterosporum ZEA,ZOH.
F.nygamai FB ,BEA,FB
1 2
F.oxysporum MON,EN,BEA
F.poae DAS,NIV,FUS,MAS,T2,HT2,NEO,BEA
F.proliferatum FB,BEA,MON,FUP,FB
1 2
F.sambucinum DAS,T2,NEO,MAS,BEA
F.semitectum BEA
F.sporotrichioides T2,HT2,NEO,MAS,DAS
F.subglutinans BEA,MON,FUP
F.tricinctum MON,BEA
F.verticillioides(F.moniliforme) FB ,FB ,FB
1 2 3
aAcDON=mono-acetyldeoxynivalenols (3-AcDON, 15-AcDON); AcNIV=mono-acetylnivalenol
(15-AcNIV); BEA=beauvericin; DiAcDON=di-acetyldeoxynivalenol (3,15-AcDON);
DAcNIV=diacetylnivalenol (4,15-AcNIV); DAS=diacetoxyscirpenol; DON=deoxynivalenol
(Vomitoxin); EN=enniatins; FB =fumonisin B; FB =fumonisin B ; FB =fumonisin B;
1 1 2 2 3 3
FUP=fusaproliferin;FUS=fusarenone-X(=4-Acetyl-NIV);FUC=fusarochromanone;HT2=HT-
2toxin;MAS=monoacetoxyscirpenol;MON=moniliformin;NEO=neosolaniol;NIV=nivalenol;
T2=T-2toxin;ZEA=zearalenone;ZOH=zearalenols(αandβisomers).
bBoldlettersindicatethemainmycotoxinproduced.