2-Pm40

ORIGINALPAPER

CharacterizationandchromosomallocationofPm40incommonwheat:anewgeneforresistancetopowderymildewderivedfromElytrigiaintermedium

P.G.LuoÆH.Y.LuoÆZ.J.ChangÆH.Y.ZhangÆM.ZhangÆZ.L.Ren

Received:19May2008/Accepted:6January2009/Publishedonline:5February2009ÓSpringer-Verlag2009

AbstractPowderymildew,causedbyBlumeriagraminisf.sp.tritici,isaverydestructivewheat(Triticumaestivum)disease.ResistancewastransferredfromElytrigiainter-mediumtocommonwheatbycrossingandbackcrossing,andlineGRY19,thatwassubsequentlyselected,possessedasingledominantgeneforseedlingresistance.Fivepoly-morphicmicrosatellitemarkers,Xgwm297,Xwmc335,Xwmc364,Xwmc426andXwmc476,onchromosomearm7BS,weremappedrelativetothepowderymildewresis-tancelocusinanF2populationofMianyang11/GRY19.ThelociorderXwmc426–Xwmc335–Pm40–Xgwm297–Xwmc364–Xwmc476,with5.9,0.2,0.7,1.2and2.9cMgeneticdistances,wasconsistentwithpublishedmaps.TheresistancegenetransferredfromElytrigiaintermediumintowheatlineGRY19wasnovel,andwasdesignatedPm40.Thecloseflankingmarkerswillenablemarkerassistedtransferofthisgeneintowheatbreedingpopulations.

P.G.LuoandH.Y.Luocontributedequallytothework.CommunicatedbyE.Guiderdoni.

P.G.LuoÁH.Y.LuoÁH.Y.ZhangÁM.ZhangÁZ.L.Ren(&)

StateKeyLaboratoryofPlantBreedingandGenetics,SichuanAgriculturalUniversity,Ya’an,Sichuan625014,China

e-mail:auh5@sicau.edu.cn;renzllab@sicau.edu.cnP.G.LuoÁZ.L.Ren

SchoolofLifeScienceandTechnology,

UniversityofElectronicScienceandTechnologyofChina,Chengdu,Sichuan610054,ChinaZ.J.Chang

InstituteofCropGenetics,

ShanxiAcademyofAgriculturalScience,Taiyuan,Shanxi030031,China

Introduction

Powderymildew,causedbyBlumeriagraminisf.sp.tri-tici,isoneofthemostdestructivefoliardiseasesofwheat(Triticumaestivum)inChina(ZhuangandLi1993).InsouthwestChina,powderymildewprobablyexceedsstriperustasthemostdamagingdisease,especiallyundercoolerconditionswithhighinputsofirrigationandnitrogenousfertilizer.Race-specificresistancetopowderymildewisusuallyshort-lived,especiallywhenasingleresistancegeneisdeployedoverawidearea,andongoingsearchesarerequiredtoidentifynewsourcesofresistanceforuseinbreedingprograms.Morethan60resistancealleleslocatedat37lociforresistancetopowderymildew(Pm1–Pm39)havebeenidentifiedanddesignatedinwheat(McIntoshetal.1998,2006;Mirandaetal.2007).Amongthem,25werederivedfromTriticumaestivum,sixfromT.turgi-dum,twofromT.monococcum,twofromAegilopsspeltoides,onefromA.longissina,onefromA.ovata,onefromA.umbellulata,twofromT.timopheevi,fourfromSecalecereale,onefromHaynaldiavillosaandfourfromA.tauschii.NoresistancegenecamefromElytrigiain-termedium(2n=42;E1E1E2E2StSt),agrassrelativeofwheatreportedtobeimmunetowheatpowderymildew(Wangetal.2000a).Thisspeciesiseasilyhybridizedwithwheatandthereforeisofpotentialvalueforwheatimprovement.Variousdisomicadditionlinesandtranslo-cationlinesresistanttopowderymildewhavebeenproducedinChina(LiandWang2002;Linetal.2005).ThewheatderivativeYU25isimmunetopowderymildew.GeneticanalysisshowedthatresistanceinYU25iscon-trolledbytwogenes(Maetal.2007).Thelocationofthesegenesonchromosomesandtheidentificationofmarkerscloselylinkedtothemshouldbebeneficialtotheirutili-zationinwheatbreedingprograms.

123

1060Molecularmarkersarenowwidelyusedforgenetagging,genemapping,andothergeneticsresearchbecausetheyarenotinfluencedbyenvironmentalcondi-tionsandgrowthstage.Molecularmarkerstightlylinkedtogenesconferringtraitsofinterestcanbeusedinmarker-assistedselection(MAS)toimprovetheefficiencyofconventionalplantbreeding(Guptaetal.1999).Amongthevariousmolecularmarkersystemscurrentlyavailabletowheatworkers,microsatellites,orsimplesequencerepeats(SSR),arethemostwidelyutilizedandseveral

microsatellitemapsofwheathavebeenreported(Ro

¨deretal.1998;Stephensonetal.1998;Pestsovaetal.2000;Guptaetal.2002;Somersetal.2004).SSRlociareevenlydistributedalongthechromosomemapsprovidingexcel-lentcoverageofthewheatgenome.SSRmarkersweresuccessfullyusedtotaganumberofpowderymildewresistancegenes(Huangetal.2000;Jarveetal.2000;Liuetal.2002;Xieetal.2003,2004;Zhuetal.2005;Mirandaetal.2006,2007).

Thepurposesofthepresentstudyweretousemicro-satellitemarkerstocharacterizeandlocateamildewresistancegene,alreadyintrogressedintowheatfromElytrigiaintermedium.MaterialsandmethodsPlantmaterials

WheatlinesorcultivarsGRY19,YU24,YU25,CM107,TAI7047,Taiyuan768and76(64),andE.intermediumwereusedinpowderymildewresponsetests.Chuanmai107(CM107)asmaternalparentwascrossedwithoctoploidTrititrigiaTAI7047,derivedfromtheinterspecificcrossT.aestivumcv.Taiyuan768/Elytrigiaintermedium//T.aestivumline76(64).Twowheatlines,Yuan24(YU24)andYuan25(YU25)selectedfromanF5populationofthecrossexhibitedimmuneresponsestopowderymildewoverseveralyearsofobservation.GRY19,selectedfromanF4populationofMianyang11(MY11)/YU25,isalsoimmune.F1plants,reciprocalbackcrossF1sandF2s,andF3families(about50seedlingsperfamilypertest)andreciprocalBCF2populationsderivedfromthecrossMY11/GRY19,wereusedingeneticstudies.ChancellorandSy95-7wereusedassusceptiblecontrols.Pathogenmaterials

AnisolateoftheprevailinglocalB.graminisf.sp.tritici(Bgt)race15(Xieetal.2003)wasusedintheseedlingstageassays.InoculationswereperformedbydustingconidiafromsporulatingseedlingsofChancellorontothetestseedlings.Infectiontypes(ITs)producedonindividual

123

TheorApplGenet(2009)118:1059–1064

plantsorlineswererecordedabout2weeksafterinocu-lation.AlthoughrecordingsareusuallybasedonasixITscaleonlyplantswithIT0(immune)orIT4(Xieetal.2003)wereobservedontheparentalsegregatingmaterials.

PreparationofgenomicDNA

TotalDNAwasextractedfrom5-weeks-oldseedlingleavesaccordingtothemethodofLuoetal.(2004).PCRamplificationandproductanalysis

GenomicDNAofparentsandindividualF2plantsderivedfromMY11/GRY19wereusedformolecularanalysis.SSRmarkerslinkedtotheresistancegenewereidentifiedbybulkedsegregantanalysis(BSA).PCRwereperformedinvolumesof25llinaMJRESEARCH(PTC-200)thermocycler,usingpubliclyavailableGWM(Bryanetal.

1997;Ro

¨deretal.1998)andWMC(Guptaetal.2002)primerpairs.SSRanalysisfollowedtheprocedureofRo

¨deretal.(1998)withminormodifications.PCRfol-lowedtheprogramdescribedbyLuoetal.(2008).EachPCRproductwasmixedwith3llofloadingbuffer(98%formamide,10mMEDTA,pH8.0,0.25%bromo-phenolblue,and0.25xylenecyanol),denaturedat95°Cfor5minandchilledonice.Sixmicrolitersofeachsamplewasloadedon6%polyacrylamide(19:1acrylamide:Bis,8Mureaand19TBE[90mMtris-borate(pH8.3),2mMEDTA]gels,whichwererunat80Wforapproximately1.5h,andvisualizedbysilverstaining(Bassametal.1991).

Statisticalanalysisandlinkageanalysis

Thegoodnessoffitofsegregationdatawithhypothesizedratioswasdeterminedbychi-squaredtestsusingSigmaplot2001software(SPSSInc.,Chicago,IL,USA).LinkagedistancesbetweenmarkersandtheresistancegeneweredeterminedusingMAPMAKER3.0(Landeretal.1987).MarkerswereacceptedataLODthresholdof3.0,andthelinkagemapwasconstructedbythemethodofLincolnetal.(1992).MapdistanceswerebasedontheKosambifunction(Kosambi1944).

Results

Powderymildewresponses

Infectiontypesproducedbyninewheatlines,octoploidTritelyitrigiaTAI7047,andE.intermediumafter

TheorApplGenet(2009)118:1059–1064inoculationwithBgtrace15showedthatGRY19,YU24,YU25,TAI7047,E.intermediumwereimmune(IT0),andthatMY11,CM107,76(64),Taiyuan768,Chancellor,andSy95-7weresusceptible(IT4).ThisconfirmedthatoneormoregenesforresistancehadbeentransferredfromE.intermediumintowheatlinesGRY19,YU24andYU25.Responsesegregationandinheritance

FormappingtheresistancegeneinGRY19usingmolec-ularmarkers,F1plants,396F2individuals,and213F3familiesfromthecrossMY11/GRY19,161BC1F2familiesfromMY11/GRY19//MY11,and132BC1F2familiesfromMY11/GRY19//GRY19wereinoculatedwithrace15.F1plantswereasresistantasGRY19indicatingthatresistancewasdominant.TheF2populationsegregated294resistant:102susceptible(v23:1=0.121,P[0.7),andasshowninTable1theF3linessegregated1homozygousresistant,2segregating:1homozygoussusceptible,F2linesfromthebackcrosstoMY11segregated1segregating:1homozy-goussusceptible,andthebackcrosstoGR19segregated1homozygousresistant:1segregating.TheseresultsclearlyshowedthatGRY19carriedasingledominantgeneforpowderymildewresistance.

Identificationofmicrosatellitemarkerslinkedtothepowderymildewresistancegene

Atotalof238(34.3%)of683microsatelliteprimerpairs,mappedtowheatchromosomesamplifiedclearbands,andgavepolymorphismsbetweenMY11andGRY19.Amongthem,Xgwm297,Xwmc335,Xwmc364,Xwmc426andXwmc476amplifiedidenticalbandsintheresistant(BR)F2bulksandGRY19,andcontrastingbandsinthesusceptible(BS)F2bulksandMY11(Fig.1),indicatingthatthesemarkerswerelinkedwithPm40.Becauseallfiveprimerpairs,previouslylocatedonwheatchromosomearm7BS,amplifiedonlysinglebands,Pm40waslikelyalsolocatedonthatchromosomearm.TherelationshipsbetweenthepowderymildewresistanceresponsegenotypesandmoleculargenotypesareshowninTable2.Eachmarkerlocusexhibiteda1:2:1segregationratio.Thelocusorder

Table1ResponsesofF3linesandreciprocalbackcrossF2popula-tionsofMY11//GRY19toBgtrace15Cross

GenerationResponsesExpectedv2a(families)HRSegHSratioMY11/GRY19F356

106511:2:10.239MY11/GRY19//

BC1F27883

1:10.078MY11MY11/GRY19//BC1F26270

1:1

0.242

GRY19

aValuesforsignificanceatP=0.05are3.84(1df),5.99(2df)

1061

Fig.1AmplifiedPCRproductswithSSRprimerpairsXgwm297,Xwmc335,Xwmc364,Xwmc426andXwmc476inpolyacrylamidegels.P1GRY19,Brresistantbulk,RresistantF2plants,P2MY11,Bssusceptiblebulk,SsusceptibleF2plants,Mmarker(with100bpladder);asteriskheterozygousloci

Table2MarkerandpowderymildewresponsegenotypesfortheMY11/GRY19F2populationMarker

ResistanceMarkergenotypeTotal

genotype

AHB

Xgwm297RR

55

156Rr1051106rr1

5051Total55107

51213v21:2:1

¼0:155;P=0.925;linkedwithPm40(0.7cM)

Xwmc335RR

56

56Rr105

1106rr5151Total56105

52

213v21:2:1

¼0:192;P=0.908;linkedwithPm40(0.2cM)

Xwmc364RR

56

56Rr104

2106rr44751Total

5610849

213v21:2:1¼0:502;P=0.778;linkedwithPm40(1.9cM)

Xwmc426RR

53356Rr3958106rr84351Total

56106

51213v21:2:1¼0:239;P=0.887;linkedwithPm40(6.1cM)

Xwmc476RR

5656Rr4993106rr34851Total

60

102

51

213v21:2:1¼0:141;P=0.565;linkedwithPm40(4.8cM)

AhomozygousfortheGRY19allele,Hheterozygous,Bhomozygous

fortheMY11allele

123

1062wasXwmc426–Xwmc335–Pm40–Xgwm297–Xwmc364–Xwmc476,withgeneticdistancesof5.9,0.2,0.7,1.2,and2.9cM,respectively(Fig.2).

Discussion

Originoftheresistancegeneanditsmodeofinheritance

Intermediatewheatgrasscanbeusedasapotentialsourceofresistancetowheatpowderymildew(Wangetal.2000a,b).GRY19isaderivativeofthatspeciesandallcommonwheatparentsinvolvedinitspedigreewerehighlysusceptibleindicatingthattheresistanceshouldhavecomefromE.intermedium.Geneticsegregationdataclearlyshowedthepresenceofasingledominantgeneforresistance.Sincenocurrentformallynamedwheatgeneforpowderymildewresistanceisderivedfromthisdonorspeciestheresistancegenemustbenovel.Chromosomallocationofthepowderymildewresistancegene

ThemicrosatellitemarkersXgwm297,Xwmc335,Xwmc364,Xwmc426andXwmc476,earlierplacedonchromosome7BS(Ro

¨deretal.1998;Guptaetal.2002;Somersetal.2004)123

TheorApplGenet(2009)118:1059–1064

werecloselylinkedwiththepowderymildewresistancegeneinGRY19.Thegeneticdistancesbetweenfourofthemarkers(exceptforXwmc426)andtheresistancegenewerelessthan5cM(Table2andFig.2),makingthemusefulformolecularMAS,especiallytheflankingXwmc335andXgwm297allelesseparatedby\\1cM.Somersetal.(2004)reportedthesamemarkersinthesequenceXwmc426–Xwmc335–Xgwm297–Xwmc476/Xwmc364withseparatingintervalsof5.1,0.4and2.7cM,respectively.BoththeorderanddistancesfortheselocicloselyagreedwiththoseinFig.2.Theuniquechro-mosomallocationsuggestedthattheresistancegeneforpowderymildewisnewlocusanditisnamedPm40.Thetransferredresistanceappearstobepresentinacryptictranslocation

Chromosometranslocationisacommonandusefulmethodfortransferringaliengenesfromwildrelativestocommonwheat.Manyalientranslocations,despitecarryingpoten-tiallyusefulgenes,havequestionablevalueinwheatimprovement,becausetheoftenlargetransferredchromo-somesegmentsdonotadequatelycompensateforthewheatgenestheyreplace,orcarryadditionalgenesconferringundesirabletraits.However,inafewinstances,traitsofinterestweretransferredtorecipientgenotypeswithoutdetectablecytologicalorgeneticchanges(Multanietal.1994;RenandZhang1997;Dongetal.2004;Kuraparthyetal.2007).Wheatprimersdidnotspantheresistancegene.WheatSSRprimersyieldedPCRproductsonwheatgeno-typeGRY19andSSRmarkerlociclosedflankedthePm40withoutsignificantchangesintheorderanddistancewhencomparedtotheconsensusgeneticmap.PreviouslystudyshowedthatYU24anditssisterselection,YU25,weregenetically(2n=42,21II)andagronomicallyuniform(Maetal.2007).TheresistancegeneinGRY19behavedasanormalMendelianunit.Moreover,wecouldnotdetectinsituhybridizationsignalsusingE.intermediumgenomicDNAasaprobe(datanotshown).ThispersuadedustoconcludethatwheatgenotypeGRY19doesnothavealargealienchro-mosomalsegment.ThustheonlyevidencethatGRY19carriesresistancefromE.intermediumispedigree.GeneticanalysisshowedthatYU25carriestwogeneticallyinde-pendentgenesforresistancetopowderymildew(Maetal.2007),andthatYU24probablycarriesthesametwogenes(unpublisheddata).Oneofthegenesconfersimmunity(IT0),andtheother,anintermediateresponse.GRY19appar-entlyinheritedonlytheimmunityfactor.ProspectsofPm40inwheatresistancebreedingprograms

InChina,especiallysouthwestChina,powderymildewisthemostcommonwheatdiseaseduetothetemperaterainy

TheorApplGenet(2009)118:1059–1064environmentduringthewheatgrowingseason(ZhuangandLi1993).Inrecentyears,powderymildewlevelshaveincreasedbecausealmostallpreviouslydeployedresistancesarenolongereffective(Liuetal.2002).Thesingleresistancegenelocatedinchromosome7BSinGRY19showednormalinheritance.Group7chromosomesinwheatarehighlytoleranttothepresenceofalienchromatinasevidencedbytheobservationthathomologousgroup7nullisomics(especiallynulli-7B)arethemostnormalofallwheatnull-isomics.Hencethelossorgain(orreplacement)ofgeneticmaterialinthischromosomeislikelytohaveminimaldet-rimentaleffects.ThecloselylinkedSSRmarkersandthedefinedlocationofPm40shouldaccelerateitsincorporationintocommercialcultivarsbyMAS.Therefore,thereisahighlikelihoodthatthepresentmaterialcanbeutilizedbybreeders,especiallywhenitisrealizedthattheonlycurrentlyeffectivehighlyresistantalternatesourceofresistanceinsouthwesternChinaisPm21whichisalsoderivedfromanaliensource,namelyH.villosa.

AcknowledgmentsFinancialsupportwasprovidedbytheNationalNaturalScienceFoundationofChina(30730065),theFokYingTungEducationsFoundation(No.111030),ChinaPostdoctoralScienceFoundation(No.0070411148)andtheSpecificFoundationofAgronomy(No.nyhyzx07-048).WearegratefultoDrR.A.McIntosh,UniversityofSydney,Australia,foracriticalreviewofadraftofthispaper.

References

BassamBJ,Caetano-AnollesG,GresshoffPM(1991)Fastand

sensitivesilverstainingofDNAinpolyacrylamidegels.AnalBiochem196:80–83

BryanGJ,CollinsAJ,StephensonP,OrryA,SmithJB,GaleMD

(1997)Isolationandcharacterizationofmicrosatellitesfromhexaploidbreadwheat.TheorApplGenet94:557–563

DongYS,BuXL,LuanYS,HeMY,LiuB(2004)Molecular

characterizationofacrypticwheat—Thinopyrumintermediumtranslocationline:evidenceforgenomicinstabilityinnascentallopolyploidandaneuploidlines.GenetMolBiol27:237–241GuptaPK,VarshneyRK,SharmaPC,RameshB(1999)Molecular

markersandtheirapplicationsinwheatbreeding.PlantBreed118:369–390

GuptaPK,BalyanHS,EdwardsKJ,IsaacP,KorzunV,RoderM,

GautierMF,JoudrierP,SchlatterA,DubcovskyJ,delaPenaR,KhairallahM,PennerG,HaydenM,SharpP,KellerB,WangR,HardouinJ,JackP,LeroyP(2002)Geneticmappingof66newmicrosatellite(SSR)inbreadwheat.TheorApplGenet105:413–422

HuangXQ,HsamSLK,ZellerFJ,WenzelG(2000)Molecular

mappingofthewheatpowderymildewresistancegenePm24andmarkervalidationformolecularbreeding.TheorApplGenet101:401–414

JarveK,PeushaHO,TsymbalovaJ,TammS,DevosKM,EnnoTM

(2000)ChromosomallocationofaTriticumtimopheevii-derivedpowderymildewresistancegenetransferredtocommonwheat.Genome43:377–381

KosambiDD(1944)Theestimationofmapdistancefromrecombi-nationvalues.AnnEugen12:172–175

1063

KuraparthyV,SoodS,ChhunejaP,DhaliwalHS,KaurS,Bowder

RL,GillBS(2007)Acrypticwheat—AegilopstriuncialistranslocationwithleafrustresistancegeneLr58.CropSci47:1995–2003

LanderES,GreenP,AbrahamsonJ,BarlowA,DalyMJ,LincolnSE,

NewburgL(1987)MAPMAKER:aninteractivecomputerpackageforconstructingprimarygeneticlinkagemapsofexperimentalandnaturalpopulations.Genomics1:174–181LiPL,WangHG(2002)Studiesonthecultivationandmorphological

andcytologicalidentificationofwheat-Elytrigiaintermediumaliendisomicadditionlines.ActaBotBoreal–OccidSin22:535–542(inChinesewithEnglishabstract)

LinXH,WangLM,LiXF,LuWH,ZhaoFT,LiWC,GaoJR,Wang

HG(2005)IdentificationofoctoploidTrititrigiaanddisomicadditionlineswithpowderymildewresistance.ActaAgronSin31:1035–1040(inChinesewithEnglishabstract)

LincolnS,DalyM,LanderE(1992)Constructinggeneticmapswith

Mapmaker/EXP3.0(M),TechnicalReport.WhiteheadInstitute,Cambridge

LiuZY,SunQX,NiZF,NevoE,YangTM(2002)Molecular

characterizationofanovelpowderymildewresistancegenePm30inwheatoriginatingfromwildemmer.Euphytica123:21–29

LuoPG,ZhangHY,ZhangHQ,RenZL(2004)Evidenceforthe

possibilityofforeigntransposonexistence.MolPlantBreed2:829–832

LuoPG,ZhangHY,ShuK,ZhangHQ,LuoHY,RenZL(2008)

Diversityofstriperust(Pucciniastriiformisf.sp.tritici)resistanceinwheatgenotypewith1RSchromosomaltransloca-tionsfromdifferentryelines.CanJPlantPathol30:254–259MaQ,LuoPG,RenZL,JiangHR,YangZJ(2007)Geneticanalysis

andchromosomallocationoftwonewgenesforresistancetopowderymildewinwheat(TriticumaestivumL.).ActaAgronSin33:1–8

McIntoshRA,HartGE,DevosKM,GaleMD,RogersWJ(1998)

Catalogueofgenesymbolsforwheat.In:SlinkardAR(ed)Proceedingsof9thinternationalwheatgeneticssymposium,vol5.UniversityofSaskatchewanExtensionPress,Saskatoon

McIntoshRA,DevosKM,DubcovskyJ,RogersWJ,MorrisCF,

AppelsR,AndersonOA(2006)Catalogueofgenesymbolsforwheat:2006supplementhttp://www.wheat.pw.usda.gov

MirandaLM,MurphyJP,MarshallD,LeathS(2006)Pm34:anew

powderymildewresistancegenetransferredfromAegilopstauschiiCoss,tocommonwheat.TheorApplGenet113:1497–1504

MirandaLM,MurphyJP,MarshallD,CowgerC,LeathS(2007)

ChromosomallocationofPm35,anovelAegilopstauschiiderivedpowderymildewresistancegeneintrogressedintocommonwheat(TriticumaestivumL.).TheorApplGenet114:1451–1456

MultaniDS,JenaKK,BrarDS(1994)Developmentofmonosomic

alienadditionlinesandintrogressionofgenesfromOryzaaustraliensisdomaintocultivatedriceOryzasativaL.TheorApplGenet88:102–109

PestsovaE,GanalMW,RoderMS(2000)Isolationandmappingof

microsatellitemarkersspecificfortheDgenomeofbreadwheat.Genome43:689–697

RenZL,ZhangHQ(1997)Inductionofsmall-segment-translocation

betweenwheatandryechromosomes.SciChina(SeriesC)40:323–331

Ro

¨derMS,KorzunV,WendehakeK,PlaschkeJ,TixierMH,LeroyP,GanalMW(1998)Amicrosatellitemapofwheat.Genetics149:2007–2023

SomersDJ,IsaacP,EdwardsK(2004)Ahigh-densitymicrosatellite

consensusmapforbreadwheat(TriticumaestivumL.).TheorApplGenet109:1105–1114

123

1064

StephensonP,BryanG,KirbyJ,CollinsA,DevosK,BussoC,Gale

M(1998)Fiftynewmicrosatellitelociforthewheatgeneticmap.TheorApplGenet97:946–949

WangHG,LiuSB,QiZJ,KongFJ,GaoJR(2000a)Application

studiesofElytrigiaintermediuminhereditaryimprovementofwheat.JShandongAgricUniv(NatSci)31:333–336

WangHG,ZhangJM,LiuSB(2000b)Identificationofwheat-ElytrigiaintermediumalienadditionlinewithresistancetopowderymildewbycytologyandRAPDanalysis.ActaBotBorealOccidSin20:64–67(inChinesewithEnglishabstract)XieCJ,SunQX,NiZF,YangT,NevoE,FahimaT(2003)

ChromosomallocationofaTriticumdicoccoides-derived

TheorApplGenet(2009)118:1059–1064

powderymildewresistancegeneincommonwheatbyusingmicrosatellitemarkers.TheorApplGenet106:341–345

XieCJ,SunQX,NiT,NevoE,FahimaF(2004)Identificationof

resistancegeneanaloguemarkerscloselylinkedtowheatpowderymildewresistancegenePm31.PlantBreed123:198–200

ZhuZD,ZhouRG,KongXY,DongYC,JiaJZ(2005)Microsatellite

markerslinkedto2powderymildewresistancegenesintrogres-sedfromTriticumcarthlicumaccessionPS5intocommonwheat.Genome48:585–590

ZhuangQS,LiZS(1993)Presentstatusofwheatbreedingandrelated

geneticstudyinChina.WheatInfServ76:1–5

123