research repository · 16 management of powdery scab although the results of preliminary studies...
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RESEARCH REPOSITORY
This is the author’s final version of the work, as accepted for publication following peer review but without the publisher’s layout or pagination.
The definitive version is available at:
http://dx.doi.org/10.1007/s13313-017-0466-3
O’Brien, P.A. and Milroy, S.P. (2017) Towards biological control of Spongospora subterranea f. sp. subterranea, the causal agent of powdery
scab in potato. Australasian Plant Pathology, 46 (1). pp. 1-10.
http://researchrepository.murdoch.edu.au/id/eprint/35687/
Copyright: © 2017, Australasian Plant Pathology Society Inc.
It is posted here for your personal use. No further distribution is permitted.
160708SssRevv9.1 1
Towards biological control of Spongospora subterranea f. sp. subterranea, 1
the causal agent of powdery scab in potato 2
3
PA O’Brien* & SP Milroy. School of Veterinary & Life Sciences, Murdoch 4
University, Murdoch WA 6150 Australia 5
*Correspondingauthoremail:[email protected]
7
Abstract:8
Powderyscabofpotato,causedbytheobligatebiotrophicprotozoanpathogen9
Spongosporasubterraneaf.sp.subterranea(Sss),isamajorprobleminpotato10
growingareasthroughouttheworld.Itresultsinlesions(scabs)onthesurface11
ofthetuberswhichrendersthemunmarketable.Inrecentyearstherehasbeen12
anincreasingnumberofreportsofthedisease,manyfromnewareas.13
Managementofthediseasehasproveddifficultandreliesontheintegrated14
applicationofarangeofmethods.Biocontrolisnotcurrentlyusedforthe15
managementofpowderyscabalthoughtheresultsofpreliminarystudieshave16
beenencouraging.Thisreviewevaluatesthepotentialfordevelopinga17
biocontrolstrategyforpowderyscab.18
19
20
Introduction21 22
Powderyscabofpotato,causedbythebiotrophicprotozoanpathogen23
Spongosporasubterraneaf.sp.subterranea(Sss),isamajorprobleminmany24
potatogrowingareasthroughouttheworld.Itresultsinlesions(scabs)onthe25
surfaceoftubersthatarefilledwithabrownpowderconsistingofsporosori26
(alsoreferredtoassporeballs),hencethecommonname(Harrisonetal.1997).27
Affectedtubershavelowacceptanceatmarketandaredown‐gradedorrejected28
bytraders,leadingtoreducedreturnstogrowersandincreasedwastewithinthe29
industry.Forproducersofseedpotatoes,thelesionsmayleadtorejectionof30
entireconsignmentsasthediseaseisspreadthroughinfectedtubers(Falloonet31
al.1996;Kirkham1986).Economiclossesinthefreshpotatomarketarevery32
160708SssRevv9.1 2
difficulttoquantify.AnnuallossestotheAustralianprocessingindustryhave33
beenestimatedatA$13.4million(Wilson2016).34
35
Inadditiontoproducinglesionsontubers,thepathogenalsoinfectsroots,36
aprocessthatleadstoreducedwaterandnutrientuptakeandthusimpaired37
shootandtubergrowth(Falloonetal.2016).Historicallythisaspecthas38
receivedlessattentionbecausetuberlesionsaremoreevident,butrootinfection39
isnowconsideredtohavethegreaterdeleteriouseffectoncropproduction.In40
fieldtrials,impairmentofwaterandnutrientutilisationcanleadtoa25%41
reductioninshootdryweight,a26%reductioninthenumberoftubersperplant42
anda42%reductionintuberweightperplant(Falloonetal.2016).43
Susceptibilityofcultivarstorootinfectionisonlylooselyrelatedtopreviously44
determinedsusceptibilitytopowderyscab(i.e.developmentoftuberlesions)45
andhencetheyareconsideredtobeseparatediseaseprocesses(Falloonetal.46
2016;Nitzanetal.2008).Rootinfection,withimpairedwaterandnutrient47
utilisation,canoccurfromearlyinthegrowthofplants,butgallformationand48
tuberlesionsonlybecomeevidentatlaterstagesofplantdevelopment(Falloon49
etal.2016).Gallformation,whensevere,canalsoleadtoimpairedwaterand50
nutrientutilisation(JohnsonandCummings2015).51
52
Inadditiontoitsdirectimpactonthehostcrop,Sssisalsothevectorof53
thepotatomop‐topfurovirus(Arifetal.1995).Mop‐topvirushasbeenreported54
tocauseyieldlossesofbetween30and60%(Carnegieetal.2010)andtubers55
expressingthecharacteristic‘spraing’symptomsareunacceptableatmarket.56
Thevirushasspreadaroundtheworldinthelast40yearsanditcanremain57
infectiveinfieldswithoutcultivationofpotatoesformanyyears(Kirk2008;58
Kalischuketal.2016).Itisspeculatedthatalternativehostsmayprolong59
survivaloftheinfectiousvirusalthoughthehostrangeofthevirusismore60
restrictedthanthatofitsvector(Kirk2008).61
62
ThepathogenSsshasprovedchallengingtocontrol,withnosingle63
methodreliablygivingfullcontrol.Rather,managementreliesontheintegrated64
applicationofarangeoftools(Falloon2008).Inthispaperwewillbrieflyreview65
160708SssRevv9.1 3
thebiologyofthepathogenandcurrentcontrolmethodsasabasisforexploring66
thepotentialtodevelopeffectivebiologicalcontroloptions.67
68
69
Occurrence70 71
PowderyscabwasfirstreportedasadiseaseinGermanyin184172
(Harrisonetal.1997).Subsequentlytherewerereportsonoccurrencesofthe73
diseasefrommanylocationsbetween1846and1992(Harrisonetal.1997).In74
recentyearstherehasbeenaresurgenceinreportsofthedisease,manyfrom75
newareassuchasAustralia,NewZealand,Columbia,Pakistan,Koreaandothers76
(Balendresetal.2016;Harrisonetal.1997;Merz2008).Theresurgenceinthe77
diseasehasbeenattributedtoincreasedcultivationofpotatocultivarswithlong78
growingseasons,useofsusceptiblecultivars,increasedirrigationofcrops,79
inadequatecroprotation,andde‐registrationofmercurybasedfungicides80
(Braithwaiteetal.1994;Harrisonetal.1997;Merz2008).Asthediseaseis81
transmittedthroughinfectedtubers,theincreasedtransportofseedtubers82
aroundtheworldmayhaveexacerbatedthespreadofthedisease(Gauetal.83
2015).Increasedawarenessandincreasedefficiencyindetectionofthedisease84
mayalsohavecontributedtotheincreaseinreporting.85
86
87
Taxonomy88 89
Spongosporasubterranea(Wallr.)Lagerhf.sp.subterraneaTomlinson,the90
causalagentofpotatopowderyscab,isasoil‐borneobligatepathogenanda91
plasmodiophoridcharacterizedashavingcruciformnucleardivision,92
multinucleateplasmodia,biflagellatezoosporesandrestingspores(Hutchison93
andKawchuk1998).Thetaxonomicpositionoftheplasmodiophoridshasbeen94
uncertainforsometime.Traditionallytheywereplacedinthefungialthough95
otherresearchershavearguedforaprotozoalorigin(reviewedin(QuandChrist96
2004)).AnalysisofSSU‐rDNAsequencesinfiveindependentstudiesledtothe97
conflictingviewsthattheyareunrelatedtoanyothereukaryotes(threestudies)98
orarerelatedtotherhizopoda(twostudies).Theresultsofmorerecent99
160708SssRevv9.1 4
analysesnowrobustlyplacethemwithintheeukaryotesupergroupRhizaria,as100
asistergrouptotheomnivorousvampyrellidamoebae(Neuhauseretal.2014).101
Plasmodiophoridsarethebetterknownmembersofthegroupbecausethey102
includeanumberofplantparasitescausingeconomicallysignificantdiseasesof103
cropsincludingbrassicas,potatoes,andgraincrops(e.g.maize,rice,wheat,104
sorghum).Themoststudiedspeciesistheclubroot‐causingPlasmodiophora105
brassicae,aparasiteofcruciferswhichaccountsforupto10%lossofthe106
worldwideproductionofBrassicacrops.Otherwell‐studiedspeciesinclude107
Spongosporasubterranea,whichcausespowderyscabofpotatoandcanserveas108
avectorforPotatoMopTopVirus.Non‐pathogenicspeciessuchasPolymyxa109
graministransmitseconomicallyimportantvirusestoanumberofgrainplants110
whilePolymyxabetaeisthevectorforbeetnecroticyellowveinvirus,thecause111
ofsugarbeet“rhizomania”.112
113
114
LifeCycle115116
Thelifecycle(Fig1)hasbeendescribedintheexcellentreviewsof117
Harrisonetal.(1997),(Merz2008),andBalendresetal.(2016).Intheasexual118
orzoosporangialphase(Fig1innercircle)thehostplantisinfectedbyhaploid119
biflagellatezoosporesthatencystontherootortubersurfacesandpenetratethe120
planttissue.Withintheplantthezoosporesdevelopintomulticellular121
plasmodia.Afterrepeatedcelldivisionstheplasmodiadifferentiateinto122
zoosporangiafromwhichhaploidbiflagellatesecondaryzoosporesarereleased.123
Theseexitthesporangiathroughporesthatextendsthroughthesporangium124
wallsandtherootsurfacesresultinginreleasedirectlyintothesoil.The125
secondaryzoosporescaninitiateinfectionsonotherpartsofthesameplantsuch126
astubers,oronadjacentplants.Thisprovidesthebasisformultiplere‐infection127
inasinglegrowingseasonandthusthepotentialforveryrapidinoculumbuild‐128
up.129
130
Inthesexualphase(Fig1outercircle)thickwalledrestingsporeseach131
germinatetoreleaseaprimarybiflagellatehaploidzoospore.Twohaploid132
160708SssRevv9.1 5
zoosporesmayundergocellfusion(plasmogamy)toformabinucleatezoospore133
thatinfectstheplant(althoughthislaststepisstilldebated).Thisdevelopsinto134
amultinucleateplasmodiumwithbinucleatecells.Eventuallythenucleifuse135
(karyogamy)andundergomeiosistodifferentiateintothickwalledspores136
withinastructureknownasasporosorus.Therestingsporesareveryresistant137
structuresandcanpersistinsoilfor4‐5years.Thesexualstagehasnotbeen138
detectedinSssbuthasbeendescribedinthecloselyrelatedspecies139
Plasmodiophorabrassica(TommerupandIngram1971).140
141
The potential for rapid increases in inoculum level and the persistence of 142
resistant spores in the soil are key considerations in the development of management 143
strategies for Sss. 144
145
PathogenDiversity146 147
InconsideringthedevelopmentofcontrolstrategiesforSssitisessential148
tounderstandthedegreeofgeneticdiversityin,andthegeneticstructureofthe149
pathogenpopulation.Variousstudieshaveshowntheexistenceofgenotypic150
variation,includingbetweengeographiclocations.AnalysisofITSsequences151
showedthatNorthAmericanisolates,togetherwithAustralasianandsome152
Europeancollectionsformedaclonalpopulation(groupII)whilstSouth153
AmericanandsomeEuropeancollectionsformedaseparategroup(groupI)154
(Bulmanetal.2001;Gauetal.2015;QuandChrist2004).TheSouthAmerican155
collectionsshowedgreatergeneticdiversitycomparedtocollectionsfromthe156
restoftheworld,suggestingthatthisisthecentreoforiginofthespecies(Gauet157
al.2013;Gauetal.2015).158
159
QuandChrist(2004)foundthattheirEuropean(fromIrelandand160
Scotland)collectionswereassociatedwithparticularpotatocultivars.The161
EuropeangroupIcollectionswereallfromcv.Saturnafromdifferentlocationsin162
IrelandandScotlandoverseveralyearswhilsttheEuropeangroupIIcollections163
werefromcvKerrsPinkfromlocationsinIrelandoverseveralyears.Insome164
instancescollectionswereobtainedfrombothcultivarsfromthesameareaby165
160708SssRevv9.1 6
thesamegrowers.SimilarobservationswerereportedbyGauetal.(2013).In166
someAndeanregionsofSouthAmericashortdayrelativesofthewidelygrown167
longdaypotatospeciesSolanumtuberosumssptuberosumarecultivated.These168
areS.tuberosumssp.andigena,andS.tuberosumphureja.SouthAmerican169
samplesofSssfromS.t.phurejarootgallsformedonegroup,whilstsamplesfrom170
tuberlesionsonS.t.tuberosumandS.t.andigenaformedanothergroup.Samples171
fromtherestoftheworldformedathirdgroupwithahighlyclonalstructure.172
173
AnalysisofNorthAmericanisolateswithasuiteofRFLPmarkersshowed174
thattheyclusteredintotwogroups,oneincludedisolatesoriginatingfrom175
westernNorthAmerica.,,andthesecondincludedisolatesoriginatingfrom176
easternNorthAmerica(QuandChrist2006b).177
178
Theresultsofthedifferentstudiesshowthatthereisgenotypicvariation179
acrossgeographicalregions.Theyalsohighlighttheneedforalargescalestudy180
onaworldwidepopulationusingmultiplegeneticlocisuchasmicrosatellite181
markers(Dobrowolskietal.2003)orRFLPmarkers(QuandChrist2006b).The182
greatergeneticdiversityfoundintheSouthAmericanpopulation(Gauetal.183
2015)suggeststhatthismaybethecentreoforiginofthepathogen.Movement184
ofpotatopropagulesfromSouthAmericaneedstobeappropriatelyregulatedto185
minimizetheriskofintroducingnewpathogendiversityintotheworld’s186
productionregions.187
188
189
CurrentControlofPowderyScab190191
Hostresistance192 193
Althoughanumberofpotatocultivarswithdifferentlevelsofresistance194
toSsshavebeenidentified(Falloonetal.2003),nocultivarisknowntobe195
completelyresistanttopowderyscab(Falloon2008;HernandezMaldonadoetal.196
2013).Resistancevariesfromveryresistanttoverysusceptible(quantitative)197
suggestingapolygenicbasis(Falloon2008).Ingeneral,moreresistantcultivars198
havefewergallsandfewerzoosporesintheirrootsalthoughthecorrelationis199
160708SssRevv9.1 7
nottightandexceptionsexist(Falloonetal.2003).HernandezMaldonadoetal.200
(2013)comparedSssaccumulationinrootsandthenumbersofgallsthat201
developedonaresistantandasusceptiblepotatocultivarandfoundthat202
althoughtherewaslittledifferencebetweenthecultivarsatearlystagesof203
infectiontherewasincreasingdivergenceasthediseaseprogressed.This204
suggeststhatalthoughtheprimaryinfectionmaybethesameinbothcultivars,205
secondaryinfectionmayberestrictedintheresistantcultivar.206
207
Chemicalcontrol208 209
Thereareanumberofagro‐chemicalsthatcanbeappliedtoseedtubers210
ortothesoil,atorbeforeplanting,thathavebeenshowntoreducepowdery211
scablevels(reviewedinFalloon(2008)).Braithwaiteetal.(1994)evaluated25212
fungicidetreatmentsappliedtoseverelyinfectedtubersjustbeforeplanting.213
Plantemergencewasassessed,andatmaturitytuberswereharvestedand214
scoredforpowderyscabinfection.Anumberofthetreatmentsreducedthe215
proportionofdiseasedtubersfrom95%atplantingtoanaverageof29%inthe216
subsequentcropcomparedwiththeuntreatedcontrolswhichdeclinedto70%.217
Someoftheothertreatmentsresultedinphytotoxiceffects.Treatmentoftubers218
withzincsulfateandzincoxidesixweeksbeforeplantingalsoreducedinfection219
inthesubsequentcropcomparedwithuntreatedcontrols.220
221
Asubsequentstudyevaluatedchemicalsappliedeitherastuberdressings222
orasin‐furrowapplications.Thefungicidesfluazinam,mancozeb,dichlorophen‐223
Na,wereeffectiveastuberdressingsofinfectedtubers,reducingtheincidenceof224
powderyscabandincreasingtheyieldoftubers(kg/plot)byupto36%(Falloon225
etal.1996).Thesamestudyevaluatedin‐furrowtreatmentsbyplanting226
uninfectedtubersofcvsRuaandAgriaintoheavilyinfestedsoil.Treatments227
withfluazinamreducedpowderyscabincidence,andincreasedyieldof228
marketable'Rua'tubersbyupto55%,and'Agria'tubersby140%.Highratesof229
mancozebalsoreducedincidenceofthediseaseandincreasedmarketableyield230
of'Rua'by34%,andof'Agria'by68%.In‐furrowtreatmentwithzincoxideand231
foliartreatmentswithphosphorousaciddidnotcontrolthedisease.232
160708SssRevv9.1 8
233
Croprotation234 235
Longrotationswithnon‐hostspeciesarerecommendedastheresting236
sporesofSsscanpersistformanyyearsinthesoil(Falloon2008).However,the237
hostrangeofSssismuchwiderthanwaspreviouslythoughtandincludesmany238
non‐solanaceousspecies(QuandChrist2006a).Of26specieswithin10families239
frommonocotyledonsanddicotyledonstested,16specieswerefoundtobe240
susceptibletoSss.TwelvespecieswerenewlyrecordedhostsforSss.However241
QuandChrist(2006a)alsoobservedthatalthoughsomespecieswereinfected,242
theydidnotproducesporosori.Itwassuggestedthatthesecouldpossiblybe243
usedtoreducetheinoculumlevelsinsoil.Sparrowetal.(2015)monitored244
pathogenDNAlevelsinsoilsofSouthEasternAustraliaoveraneightyears245
periodandsuggestedaminimumoffiveyearsbetweenpotatocrops.246
247
LarkinandGriffin(2007)evaluatedthepotentialofrotationwithbrassica248
cropstodecreasethelevelofpathogeninoculuminsoilandsoreducedisease249
severityinsubsequentpotatocrops.Brassicasproducesulphurcompounds,250
glucosinolates,whichbreakdowntoisothiocyanatesthataretoxictoawide251
rangeofphytopathogens.Inafieldtrial,Indianmustardsignificantlyreduced252
Sssinoculumlevelsinthesoilasmeasuredbyabioassay.Cropsofrapeseedor253
yellowmustardwerelesseffective.Allthreebrassicaspeciesdecreasedthe254
severityofpowderyscabby25‐39%relativetoastandardoatsrotation.The255
brassicasalsoreducedtheincidenceoftuberswithscabsby19‐40%withIndian256
mustardagainbeingthemosteffective.Indianmustardproduceshighlevelsof257
glucosinolates,someofwhichconverttothemostbiologicallyactiveformsof258
isothiocyanatesproducedbybrassicas(CharronandSams1999).Inthesame259
study,rotationwith‘Lemtal’ryegrassledtosimilarreductionsindisease260
severityandincidenceoftuberswithlesionsaswereobservedafterrotation261
withthebrassicas.Thissuggeststhatfactorsotherthantheproductionof262
isothiocyanatesmayhavebeenresponsibleforthereductioninincidenceand263
severity.264
265
160708SssRevv9.1 9
Asanalternativetodirectpathogeninhibition,rotationcropsmayalso266
affectpathogensindirectlybyinfluencingchangesinthesoilmicrobial267
community.Thismayincreasediseasesuppressionbythesoil.Inastudyto268
examinetheeffectsofrotationsystemsonsoilmicrobialcommunities,Larkin269
andHoneycutt(2006)demonstrateddistinctiveeffectsofspecificrotationcrops270
andcroppingsequencesonthesecommunities.Theyalsofoundhigher271
populationsofmicroorganismsthataregenerallybeneficialtoplants,suchas272
Pseudomonasspp.andTrichodermaspp.,afterplantingbarley,canola,andsweet273
corncrops.274
275
Agronomicfactors276 277
Agronomicfactors,particularlysoilnitrogenstatusandsoilwatercontent278
werefoundtoaffecttheseverityofdisease(Shahetal.2014).Theincidence279
and/orseverityofpowderyscabwereincreasedbynitrogen(nitrateand280
ammonium)applications.Nitrogenapplicationresultedinagreateramountof281
SssDNAinthesoilandthiseffectwasobservedfortwoyearsafterthetrial.A282
positivecorrelationbetweensoilSssDNAanddiseaseseveritywasobservedby283
Brierleyetal.(2013)andbyNakayamaandSayama(2013).However,Shahetal.284
(2012)reportedthatintheirstudytherewasnoconsistentlystrongrelationship285
betweentheamountofinoculumattimeofplantingasmeasuredbythenumber286
ofsporosoripergsoilanddiseaseincidenceorseverityatharvest.Irrigation287
treatmentalsoaffecteddiseaseseverity.Anirrigationregimeoptimalforpotato288
growthresultedingreaterseverity,butnotgreaterincidence,ofpowderyscab289
thanaconstrainedirrigationinput(Shahetal.2014).Thisisconsistentwith290
highersoilmoisturecontentfacilitatingthemovementofzoosporesthroughthe291
soilandincreasingthechancesofplantinfection(Merz2008;Balendresetal.292
2016).293
294
295
PotentialforBiocontrol296297
Biocontrol,basedontheuseofanorganismtorestricttheabilityofa298
pathogentocausediseaseisanaspectofplantdiseasecontrolthathasreceived299
160708SssRevv9.1 10
muchattentioninrecentyears.Thisisfuelledbytheemergenceoffungicide300
resistanceinpathogenpopulations,deregistrationoffungicides,andgrowing301
concernsabouttheuseofchemicalsinfoodproduction.Incontrastbiocontrolis302
seenasasafe,non‐toxic,renewablealternative.Insomecasesofbiocontrolthe303
levelofcontrolrivalsthatachievedwithchemicalsalthoughalackofconsistency304
ofcontrolisoftenaconcern.305
306
Identifyingbiocontrolagents307 308
Therearefewreportsofstudiesaimedtoidentifypotentialbiological309
controlagents(BCAs)forSssinpotato.Themostextensivestudyisthatof310
NakayamaandSayama(2013).Theyreported54–70%suppressionofdisease311
developmentoverthreeyearsbyapplicationofanisolateofAspergillus312
versicolourtotubers.Thesevaluescomparedto77to93%suppressionbythe313
syntheticfungicidefluazinamappliedinfurrow.WhiletheBCAwaslesseffective314
thanthesyntheticfungicide,thesuppressionwasstatisticallysignificant.315
316
AnotherapproachwastakenbyNielsenandLarsen(2004)whoused317
tomatoasamodeltoexaminetheefficacyofcommerciallyavailablebiocontrol318
productstoreducetheinfectionofroothairsbyprimaryzoosporesofSss.Each319
agentwasassessedintwoexperiments.Thecommerciallyproducedbiocontrol320
productsTRI002andBinabTF(bothcontainingTrichodermaharzianum)gavea321
statisticallysignificantreductioninrootcolonizationinbothexperiments.By322
contrastthebiocontrolproductTRI003(alsocontainingTrichoderma323
harzianum)gavenosignificantreductionineitherexperiment.Theproduct324
FZB24,containingBacillussubtilis,gaveareducedinfectioninonlyoneofthe325
twoexperiments.Ineachexperiment,allplantgrowthparametersexamined326
weremarkedlylowerintheinfectedcontrolsthantheuninfectedcontrols.While327
someofthecontrolagentsincreasedtheplantgrowthparametersabovethatin328
theinfectedcontrol,theseincreaseswerenotconsistent.329
330
IntheexperimentsofNielsenandLarsen(2004)averyhighinoculum331
concentrationofthepathogenwasused;muchgreaterthancouldbeexpectedin332
160708SssRevv9.1 11
fieldsoilorinsoiladheringtothesurfaceofseedtubers(e.g.0‐148sporosori/g333
ofsoil;(Brierleyetal.2013)).Itispossiblethatmoreeffectiveandmore334
consistentcontrolcouldbeobtainedwithmoretypicaldiseasepressures;335
biologicalcontrolofPlasmodiophorabrassicaehasbeenfoundtobemore336
effectiveatlowerpathogenpressure(Narisawaetal.2005;Pengetal.2011).It337
wasnotknownwhethertheBCAstestedbyNielsenandLarsen(2004)were338
inhibitorytoSss.Incontrast,inthestudybyNakayamaandSayama(2013)soil339
fungiwereinitiallyscreenedforinhibitionofSssinfectivityusingabioassay.340
341
AlthoughresearchonbiocontrolofSssislimited,biocontrolof342
Plasmodiophorabrassicae,hasbeenstudiedmoreextensively.Anumberof343
studieshaveidentifiedendophyteswiththeabilitytosuppressthispathogen.344
TheseincludeBacillussubtilis,Gliocladiumcatenulatum,Heteroconium345
chaetospira,Microbisporaroseassprosea,Streptomycesgriseoruber,S.346
griseoviridis,S.lydicus,S.olivochromogenesandTrichodermaatroviride,T.347
harzianumandT.viride.(Lahlalietal.2014;Leeetal.2008;Narisawaetal.1998;348
Pengetal.2014;Pengetal.2011;Wangetal.2012;Wangetal.2011).Insome349
studiesanumberofthesepotentialbiocontrolagentshaveshownlevelsof350
suppressionofclubrootgreaterthan85%andapproachingthelevelof351
effectivenessobservedfromsyntheticfungicides.352
353
Theevidencefromthelimitedstudiesthathavebeencarriedoutsuggests354
thatdevelopingbiocontrolstrategiesforplasmodiophoriddiseasesispossible.355
Howeveraproblemcommontoallbiocontrolstrategiesisthelackofconsistency356
ofdiseasereduction.Severalresearchershavereportedthatusingmixturesof357
BCAshasincreasedtheconsistencyofbiocontrolacrosssiteswithdifferent358
conditions.Sliningeretal.(2001)intheirinvestigationintopostharvestdryrot359
ofpotatofoundthatformulationsofmixedBCAsperformedmoreconsistently360
across32storageenvironmentsvaryingincultivar,washingprocedure,361
temperature,harvestyear,andstoragetime.Enhancedbiocontrolusing362
mixturesofBCAshasbeenreportedforcontroloflateblightinpotato(Slininger363
etal.2007),diseasesofpoplar(Gyenisetal.2003),chilli(Muthukumaretal.364
2011),andcucumber(RaupachandKloepper1998;Robertsetal.2005).Itis365
160708SssRevv9.1 12
alsopossiblethatdifferentmixturesmayneedtobeusedindifferentclimatic366
areas.Thusthereisaneedtoidentifyanumberofpotentialbiocontrolagents.367
Mixturesdonotalwaysgiveincreasedcontrol.Insomecasestheremaybe368
antagonismbetweentheBCAsthatresultsinreducedcontrolcomparedtosingle369
strains.Inevaluatingagentsforcontroloffireblightinpear,Stockwelletal.370
(2011)foundthatmixturesofPseudomonasfluorescensA506,PantoeavagusC9‐371
1andPantoeaagglomeransEh252werelesseffectivethantheindividualstrains.372
ThePantoeastrainsexerttheireffectsthroughtheproductionofpeptide373
antibiotics.Inthemixturetheseweredegradedbyanextracellularprotease374
producedbyP.fluorescensA506.Robertsetal.(2005)alsoreportedantagonism375
betweenBCAstrains.TheyobservedthatpopulationsofTrichodermavirensGL3376
orGL321werebothsubstantiallyreducedafterco‐incubationwithBacillus377
cepaciaBC‐1orSerratiamarcescensisolatesN1‐14orN2‐4incucumber378
rhizospheres.Thesereportshighlighttheimportanceofconsideringpossible379
antagonismbetweenstrainswhendevelopingbiocontrolformulations.Co‐380
cultivationinvitrocansometimesrevealinhibitoryeffects(Robertsetal.2005)381
butnotalways.InthestudybyStockwelletal.(2011)theantagonisticeffects382
wouldnothavebeendetectedbyco‐cultivationastheBCAsthemselveswerenot383
affected,onlytheirpotentialactiononthepathogenwasdisrupted.384
385
BCAsaretypicallyidentifiedbyscreeningrhizosphericorendophytic386
bacteriaandfungiforinhibitionofpathogengrowthinvitro,followedby387
greenhousetrialsofgrowthinhibitingisolatesandfinallyfieldtrials.Theuseof388
invitroscreeningasaninitialstephasanumberofsignificantlimitations;most389
notably,itonlyidentifiesorganismwhichactonthepathogenthroughaspecific390
subsetofmechanisms.ControlofdiseasebyaBCAoccursthroughavarietyof391
mechanismsandinmanycasesdirectcontactwiththepathogenisnot392
necessary.Mechanismsofcontrolinclude:detoxificationoftoxinsproducedby393
thepathogen(Newmanetal.2008),degradationofthepathogencellwall394
leadingtolysis(mycoparasitism)(Janetal.2011),productionofantibiotics395
(Raaijmakersetal.2002),antimicrobialsurfactants(Raaijmakersetal.2010),396
siderophoresandvolatiles(Santoyoetal.2012)bytheBCA,inductionofplant397
defenses(Tingetal.2012),stimulationofplantgrowth(vanderLelieetal.398
160708SssRevv9.1 13
2009),physicalocclusionofthepathogenbyoccupyingsitesonrootsurfaces399
thatthepathogenwoulduseforentry(Blumensteinetal.2015),andbiofilm400
formation(Newmanetal.2008).AgivenBCAmayusemorethanone401
mechanismofinhibition,anddifferentBCAsmayexerttheireffectsatdifferent402
timesduringthecropgrowingseason.Invitroscreeningonlyidentifiesthose403
BCAsactingthroughtheproductionofantibioticsorcelllysis.Further,inthe404
specificcaseofSss,invitroscreeningisnotpossibleasthespeciesisanobligate405
biotroph.Thusinitialscreeningwouldneedtoemployinplantamethodssimilar406
tothoseusedbyNakayamaandSayama(2013).407
408
Invitroinhibitionorinhibitionofdiseasedevelopmentingreenhouse409
trialsdoesnotalwaystranslatetoeffectivediseasemanagementinthefield410
whereweather,soilandbiologicalvariabilityarelikelytobemuchgreater.411
Ultimately,theonlyrealisticevaluationisbyfieldtrials.Giventherangeof412
edaphicandenvironmentalfactorsthatcaninfluencetheeffectivenessofBCAs413
(asnotedinthefollowingsection),thenumberandlocationofevaluationsites414
needstobeselectedtoappropriatelyreflecttheanticipatedrangeofusage.As415
theproductionofpotatoexpandsgeographicallyintoMediterranean,sub‐416
tropicalandevenhighaltitudetropicalareas,thisaspectbecomesmore417
significant.Further,giventhatsoilmicrobialcommunitiescanvarydramatically418
withsoiltypeandlandmanagement,variationinthesefactorsneedstobe419
capturedalso.420
421
Sss,impactspotatoveryearlyincropdevelopment(Hughes1980;Taylor422
etal.1986).Screeningmethodologymustreflecttheneedforprotectiontobe423
establishedbythetimeofplantemergence.Withafocussolelyonreducingtuber424
symptoms,protectionwouldneedtopersisttobeyondtuberinitiation;although425
longerprotectionwouldbepreferableasrootdamagecontinuestooccurbeyond426
thatstage(Hughes1980),impactinghostnutrientandwateruptake.427
428
Stabilityacrossproductionenvironments429 430
Studiesontheinfluenceofenvironmentontheefficacyofbiological431
160708SssRevv9.1 14
controlofsoil‐bornediseasesdemonstratetheinfluenceoftemperature(Janget432
al.2011;Landaetal.2001;Landaetal.2004;Schmidtetal.2004),soilwater433
status(Schmidtetal.2004)andsoilphysicalandchemicalcharacteristics434
(Ownleyetal.2003)onthelevelsofcontrolachieved.Giventheincreasingly435
diverseconditionsandgeographiclocationsunderwhichpotatoisnow436
produced(Birchetal.2012;Devauxetal.2014),thiswillbeanimportant437
consideration.438
439
Noresearchhasbeenreportedthatevaluatestheinfluenceof440
environmentalvariables(eithersoilorweather)ontheeffectivenessofBCAsin441
supressingSssandlittlehasbeenreportedinrelationtoP.brassicae.Studying442
thecontrolofP.brassicaebyHeterconiumchaetospira,Narisawaetal.(2005)443
foundeffectivesuppressionunderlowtomoderatemoistureconditionsbutnot444
athighwaterstatus.Ontheotherhand,Pengetal.(2011)foundthatperiodsof445
drysoilimpededtheeffectivenessofarangeofBCAstovaryingdegrees.Bacillus446
subtilisandthesyntheticfungicide,fluazinamwereparticularlysensitive.447
Significantly,whiletheresultsofZhouetal.(2014)showedvariationinthe448
effectivenessofbacterialisolatesinsuppressingP.brassicaeinChinesecabbage,449
theeffectivenessofthesyntheticfungicidealsovaried.450
451
EffectiveformulationofBCA452 453
TheforminwhichaBCAisappliedtoacropmayaffectitspersistenceand454
thusitseffectiveness.Resistantpropagulessuchasbacterialendospores,fungal455
conidia,chlamydosporesoroosporesaremorepersistentthanvegetative456
bacterialcellsorfungalhyphalfragments(Schisleretal.2004).Forspore‐457
formingbacteria,yeasts,andfungi,theproductionsystemcanbeoptimisedfor458
theproductionofspores.Fermentationenvironmentsandcultureageinfluence459
theefficacy,stabilityanddesiccationtoleranceofmanyBCAsincludingfungi,460
yeasts,andbacteria(Schisleretal.2004).Thefungalbiocontrolagent461
Trichodermaharzianumdevelopedmyceliumafterfourdaysat280Cand462
chlamydosporesafter10daysinliquidmedium(potatodextrosebroth)at28°C463
whileonsolidmedia(e.g.,PDA,grains,wheatbran,)itproducedconidia(Mishra464
160708SssRevv9.1 15
etal.2012).465
466
PersistencecanbeenhancedbymixingtheBCAwithadditivesthatsupply467
nutrients,protectitfromdesiccation,fromUV,andantagonisticorganisms,and468
increaseitsabilitytosticktothesurfaceofplants.Thedifferenttypesof469
additiveswerereviewedbySchisleretal.(2004).Theadditionofcalcium470
carbonatetoricegrainculturesofTrichodermamartialestimulatedconidia471
productionandenhancedthepersistenceoftheBCAinthefieldandduring472
storage(Hanadaetal.2009).FormulationofstrainsoffluorescentPseudomonas473
withtalchasbeenreportedtoenhanceefficacyincontrolofFusariumwiltin474
banana(Saravananetal.2004)andtomato(Sarmaetal.2011).Inclusionof475
chitininthegrowthmediumfortheproductionofchitinolyticstrainsofSerratia476
hasbeenfoundtobeeffectiveanditispostulatedthatthechitinmayalso477
stimulatethegrowthofotherchitinolyticspeciesinrhizosphereswhichwould478
helptopreventfungalinfection(Kimetal.2008).479
480
EncapsulationoftheBCAwithinabiodegradablematrixofprotein(whey,481
poly‐Lysine)polysaccharide(e.g.,cellulose,alginates,chitosan,pectin),orother482
polymerssuchaslignin,protectstheBCAfrombioticandabioticstressfactors483
andpromotesshelflifeandpersistenceintheenvironment.Overall484
encapsulationresultsingreaterdiseasecontrol.Thetopicofencapsulation,485
includingthetypesofmaterialsandhowtomakecapsules,isreviewedby486
VemmerandPatel(2013).487
488
MethodsofapplicationofBCA489 490
Amajorfactorintheefficacyofbiocontrolagentsisthemethodof491
application.BCAscanbeappliedasseed(tuber)dressings,assoil‐drenchesoras492
afoliarspray.Forrhizosphericorganismsthatwillencounterthepathogen493
beforeitentersthehostplant,andpreventsentryeitherbyocclusionorkilling494
thepathogenitisessentialthattheBCAisabletocolonizerootsastheydevelop.495
496
Forsoil‐bornediseases,soildrenchesaremosteffectiveastheyallow497
160708SssRevv9.1 16
extensivecolonizationofroots(Gossenetal.2013).In‐furrowapplicationsor498
seeddressingsarealternativesalthoughtheymaynotbeaseffectivein499
providinghighlevelsofinoculation.McLeanetal.(2005)comparedmethodsof500
introducingTrichodermaatroviridaeasaBCAforSclerotiumcepivorum(white501
rot)inonions.Inaglasshousetrial,theyfoundthatapelletformulation502
maintainedgreaterlevelsoftheBCAinthesoilcomparedtosolid‐substrateor503
seed‐coatingformulations.Pelletsalsogavemoreextensivecolonizationofroot504
systemsoftheonionseedlings.Inasubsequentfieldtrialapelletformulation505
resultedinagreaternumberofCFU/gofsoilthanasolidsubstrateform.The506
pelletformulationalsogaveamorepersistentinoculum.507
508
Timingoftheapplicationmayalsohaveanimportantimpact.Inatrialof509
suppressionoftherelatedclubrootpathogenP.brassicabythefungalBCAH.510
chaetospira,itwasfoundthatsoilapplicationofagranularformulationofthe511
fungusreducedclubrootseverityby>80%relativetothecontrol.However,512
applyingH.chaetospiraatseedingwasmuchlesseffectivethanearliersoil513
application.MoreextensiverootcolonizationbyH.chaetospiraresultedin514
greatersuppressionofP.brassicaeinfectionandsubsequentclubroot515
development(Lahlalietal.2014)Thus,thegreatersuppressionbytheearlier516
applicationmayhaveresultedfrommoreextensiverootcolonization.517
518
InthecaseofSss,protectionisrequiredfromaboutthetimeofplant519
emergence(Hughes1980;Tayloretal.1986).Thus,foranyBCAtobeeffective,520
earlycolonizationofthebelowgroundplantpartswillbecritical.521
522
Incorporationintodiseasemanagementsystems523 524
Falloon(2008)reviewedthedevelopmentofintegratedmanagement525
systemsforSss.Thereiscurrentlynosinglemanagementpracticeavailablethat526
providesfullandreliablecontrolofthedisease.Effectivemanagementrelieson527
thecoordinateduseofanumberofapproaches.Themaincomponentslistedby528
Falloon(2008)werecroprotation,fieldselection,resistantcultivars,pathogen‐529
freeplantingmaterial,appropriatepesticideuseandsoundcropmanagement.530
160708SssRevv9.1 17
Theuseofbiologicalcontroliscompatiblewiththemajorityofthese531
components;howevercompatibilitywithagro‐chemicals(fungicidesandor532
pesticides)isanobviouschallenge.533
534
Potatoproducersuseawiderangeofagro‐chemicalsasdressingsforseed535
tubers,appliedeitherbeforeorafterstorage,orasin‐furrowapplicationsat536
plantingsinbandsupto20cmwide.Fungicideswhichareusedagainstarange537
ofpossiblepathogens,areaparticularissue.Thesevaryfrombroadspectrum538
treatmentstoproductstargetingspecificdiseaseorganisms.Theirmobility539
withinpotatoplantsalsorangesfromcontacttofullysystemic.Thiswillbea540
majorconsiderationfortheincorporationofBCAsintotheproductionsystem.541
Clearly,thesignificancewilldependontheparticularchemicalinuseandits542
modeofapplicationontheonehandandtheidentityoftheBCAandthemodeof543
inoculationontheother.Forexample,in‐furrowapplicationoffungicidesmay544
interferewiththesuccessfulestablishmentofBCAsappliedin‐furrowortothe545
seedpiecedependingontheidentityoftheBCAandthefungicideapplied.Onthe546
otherhandbroad‐spectrumsoilfumigantssuchasmetam‐sodium(sodiumsalt547
ofmethyldithiocarbamate)arestillinuseinsomeregionsasameansof548
reducingsoil‐bornediseasespriortoplantingpotatoes.Althoughthese549
treatmentsarebroadspectrum(Xieetal.2015),thereislikelytobelimited550
interferencewithBCAsappliedtotheseedpotatooratplantingasthefumigants551
arereleasedfromthesoilsomeweekspriortoplanting.However,questions552
havebeenraisedregardingtheimpactofsuchfumigantsonthesizeand553
structureofsoilmicrobialcommunities(DeCaletal.2005;Macaladyetal.1998).554
Significantalterationsincommunitystructuremayhaveunforeseen555
consequencesforthesuccessoftheBCA,thepathogen,orsoilfunctions.556
557
Approachestocombiningbiocontrolagentsandagrochemicalsforuse558
againstthetargetpathogenareimportantforIPM.Levelsofdiseasesuppression559
achievedbycombiningthecontrolmethodsaretypicallyequalorsuperiortothe560
useofBCAalone(Deberdtetal.2008;Hidalgoetal.2003)(seediscussionin561
Hanadaetal.(2009)).562
563
160708SssRevv9.1 18
Giventhatpotatoisvegetativelypropagated,introducinganendophyte564
intopotatotubersviatheparentseedcropmayprovidealevelofprotection565
fromnon‐systemicagrochemicals.Thismayprovideanovelmethodof566
combiningbiocontrolwithseed‐tuberdressingsorin‐furrowpesticide567
applicationsinanintegratedsystem.Iffeasible,thisapproachwouldalso568
provideadegreeofprotectionfortheBCAfromenvironmentalandsoil569
variability,aswellasprovidingtheearliestpossibleintroductionoftheBCA570
whichisimportantgiventheearlyimpactofSssonpotatoplantsandtuber571
quality.Astructuredexperimentalinvestigationisrequired.572
573
574
IsSuccessfulBiologicalControlofSssPossible?575 576
Thelimitedworkavailablesuggeststhateffortstoidentifyorganisms577
capableofsuccessfullysuppressingdiseasedevelopmentbySssarelikelytobe578
successful.Toachievethis,ahighthroughputinplantaassaywillberequiredfor579
screeningendophyticandrhizosphericorganisms.Themethoddescribedby580
NakayamaandSayama(2013)couldbeusedforthispurposeascouldthe581
procedureofNielsenandLarsen(2004).InthisregardAndreaRamirezetal.582
(2013)havedescribedastemcuttingassaytoscreencultivarsforresistanceto583
Sssthatcouldbeadaptedtoscreenfordiseasecontrolbymicrobialisolates.584
AnotherpossibilitydescribedbyMerzetal.(2004)isaproceduretoscreen585
potatocultivarsforresistanceusingtissuecultureplantlets.586
587
However,identifyingbiologicalantagonistswouldappeartobethemore588
straightforwardaspectoftheresearch.Thegreaterchallengeliesindeveloping589
aformulationandmethodofapplicationthatwillprovideadequateprotection590
consistentlyacrossproductionsystemsandgeographiclocationswithinthe591
intendedrangeofuse.MixturesofBCAsmayprovevaluableinthisrespect.592
Importantly,theformulationandmodeofusewillneedtoallowintegrationwith593
otherdiseasecontrolmethods,especiallytheuseoffungicidesandpesticides.594
595
GiventhecommercialsignificanceofthediseaseprocessescausedbySss596
160708SssRevv9.1 19
andthepersistentchallengeofeffectivecontrol,afocusedefforttoexplorethe597
potentialtodeveloppracticalbiologicalcontrolsystemsforthispathogenwould598
appearwarranted. 599
600
601
Acknowledgements602603
ThankstoProf.RichardFalloon(LincolnNZ)forhelpfulcommentsonanearly604
versionofthemanuscript.ThankstoProf.UMerz(Zurich)forpermissionto605
includeFigure1.606
607
608
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CaptionsforFigures925926927
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Figure1.TentativelifecycleofSpongosporasubterraneaf.sp.subterranea.The929
outerpathrepresentssexualreproductionandtheinnerpathrepresentsasexual930
reproduction.(ReproducedfromMerz(2008)withpermissionofSpringer).931
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Fig1:934935
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