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Journal of Phytopathology. 2017;1–10. wileyonlinelibrary.com/journal/jph
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© 2017 Blackwell Verlag GmbH
Received:13April2017
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Accepted:23August2017
DOI: 10.1111/jph.12655
ORIGINAL ARTICLE
Seedling and adult- plant stage resistance of a world collection
of barley genotypes to stripe rust
Sanjaya Gyawali1 | Ramesh Pal Singh Verma1 | Subodh Kumar2 |
Subhash Chand Bhardwaj2 | Om Prakash Gangwar2 | Rajan Selvakumar2 |
Pradip Singh Shekhawat3 | Sajid Rehman1 | Dipak Sharma-Poudyal4
1BiodiversityandIntegratedGene
management(BIGM),ICARDA,Rabat,
Morocco
2IndianInstituteofWheatandBarley
Research(IIW&BR),IndianCouncilof
AgriculturalResearch(ICAR),Shimla,India
3RajasthanAgriculturalResearchInstitute
(RARI),S.K.N.AgricultureUniversity,
Durgapura,Rajasthan,India
4OregonDepartmentofAgriculture,Salem,
OR,USA
Correspondence
S.Gyawali,BIGMP,ICARDA,Rabat,Morocco.
Email:gyawalisanjaya@gmail.com
Abstract
Barleystripe rustcaused byPuccinia striiformis f.sp.hordei (PSH)is oneof themajor
diseasesinbarleyproductionregionsworldwide.Atotalof336barleygenotypeswith
diversegeneticbackgroundstargetedforlow-inputbarleyproductionweretestedfor
seedlingandadult-plantstageresistanceagainstsixPSHraces(0S0,0S0-1,1S0,4S0,
5S0and7S0)originatedfromIndia.Theseedlingresistancewasevaluatedbyinoculat-
ing the barley genotypes with six races separately under controlled conditions in
Shimla,India.Thesamebarleygenotypeswereevaluatedforadult-plantstageresist-
anceintheAgricultural Research Station(ARS)ofRajasthan Agriculture University,
Durgapura,Rajasthan,India.Outofthe 336barleygenotypestestedforseedlingre-
sistance,119(35.4%),101(30.1%),87(25.9%),100(29.8%),91(27.1%)and70(20.8%)
genotypeswereresistanttoraces0S0,0S0-1,1S0,4S0,5S0and7S0,respectively.In
thefield,102(30.3%)genotypesshowedtheresistanceresponseofwhich18(5.3%)
genotypeswerehighlyresistantto PSH.BarleygenotypesAM-14,AM-177, AM-37,
AM-120,AM-300,AM-36,AM-103,AM-189,AM-291,AM-275andAM-274showed
resistanceresponsetoallsixracesatseedlingandadult-plantstages.Seedlingresist-
ancereportedinthecurrent studyiseffective againstthe newlyemergedrace 7S0
andpreviouslyreportedfiveracesinIndia.Therefore,resistantbarleygenotypesiden-
tifiedinthecurrentstudyprovidedeffectiveprotectionagainstallsixracesatseedling
andadult-plantstages.Thestriperustresistanceidentifiedinthecurrentstudiesmay
bepotential donorsof striperust resistanceto barleybreeding programmesinIndia
andelsewhere.
KEYWORDS
barley,race,resistance,striperust,yellowrust
1 | INTRODUCTION
Barley (Hordeum vulagere L.) is one of the most important cereal
cropsgrown onmore than49.7 millionha (FAOStat2015)andis
mainlyusedas feed,foodandmalt inmanycountries(Newman&
Newman,2006).This cerealisadaptedtodry areascharacterized
byerraticrainandpoorsoilfertilitywhichareoften describedas
low-inputbarley(LIB)production systems.Biotic stresses,mainly
stripe rust (caused by Puccinia striiformis Westend. f.sp. hordei
Erikss.) (PSH), cause significant yield losses in barley.Stripe rust
often causes serious epidemics in South Asia (India, Nepal and
Pakistan)(Bahl&Bakshi,1963;Bakshi,Bahl,&Kohli,1964;Luthra
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GYAWALI et AL.
&Chopra,1990;Murty,1942;Pradhanang&Sthapit,1995;Upreti,
2005;Vaish, Ahmed, & Prakash,2011), West Asia (Safavi,2012),
EastAfrica(Stubbs,1985;Woldeab,Fininsa,Singh,&Yuen,2007),
SouthAmerica(Capettini,2005;Stubbs,1985)andNorthAmerica
(Chen,2007,2008;Chen&Line,2002;Chen,Line,&Leung,1995;
Dubin & Stubbs, 1986; Line, 2000 and Roelfs & Huerta-Espino,
1994).Frequentand seriousstriperust epidemicscaused signif-
icantyieldlossrangingfrom5%to25%inwheatand barleywhile
yieldlossashighas70%wasreportedinbarleyinSouthAmerica
(Wellings,2011).
Deployment of durable resistance is the most profitable, cost
effective and environmentally sound strategy to manage the rust
disease(Park,2008).Incerealrusts,twomajortypesofresistances
have been described, including seedling/all-stage resistance and
adult-plantresistance(APR).Ithasbeendemonstratedthatall-stage
resistanceiseffectivethroughoutallstagesofplant growth,which
isoftencharacterizedbythehypersensitivetypeofresponseswhile
theAPRiseffectiveonlyatadult-plantstage,andisoftenregarded
asslowrusting (Park,2008). Recently,a newstriperust race, 7S0
was reported in 2014 which overcomes seedling stage resistance
ofbarleycultivarseffectiveagainstracesprevalentinIndia.Several
studieshavebeenreportedon seedlingandAPRresistanceinbar-
leyleafrustcausedbyPuccinia hordeiwhereasinformationonAPR
to stripe rust is still scant. Forexample, several P. hordeiall-stage
resistancegenesconferringhighlevelofresistance,includingRph1-
Rph19 (Golegaonkar, Singh, & Park, 2009), Rph21 (Sandhu etal.,
2012)andRph22(Johnson,Niks,Meiyalaghan,Blanchet,&Pickering,
2013),havebeencharacterized.Recently,Dracatosetal.(2016)and
EsveltKlosetal.(2016)reportedQTLmappingofPSHresistanceat
seedlingstageusing Europeanand NorthAmerican PSHraces, re-
spectively.Often,all-stageresistancegenesaredominant innature
withlargeeffects.Frequentmutationsinrustvirulencegenesoften
leadtothe breakdownofcorresponding majorresistance genesin
thehost withina shortperiod ofdeployment (Park,2008). Incon-
trast, APR is mostlyquantitative in nature, is often referred to as
incompleteorslowrustingandisoftenadditiveinnature(Carlborg&
Haley,2004;Golegaonkar etal.,2009;Singh,Dracatos,Derevnina,
Zhou,&Park,2015).Therefore,APRgenesaremoreofteneffective
foralongerperiod.
TheAPRgenesarelessstudiedinbarleyduetotheirpartialmode
of action. Verma etal. (2016) reported seedling (against five races)
andadult-plantstageresistancetostriperustingenotypesoriginat-
ing from high-inputbarley breeding programmeof the International
Center forAgricultural Research in the Dry Areas (ICARDA). They
identified 12 stripe rust-resistantgenotypes against five PSH races
inIndia.However,informationonAPRgenesagainstPSHracesfrom
barleyis stillinadequate.AmongPSHreported inIndia, race24has
been widely reported in major barley-growing regions across the
globe(Chen,2007)whileotherPSHracesusedbyVermaetal.(2016)
are endemic to India. Therefore, the objective ofthis study was to
identifysourcesofseedlingandAPR inbarleygenotypes adaptedto
LIB breeding programmes toIndian PSH races, including the newly
emergedrace7S0.
2 | MATERIALS AND METHODS
2.1 | Barley genotypes and stripe rust races
A worldcollection of association mapping (AM-2014) panel of 336
barleygenotypes withdiverse sources(TableS1) wasassembledfor
theLIBbreedingprogrammeofICARDA.Thegeneticdiversityandde-
taildescriptionsofAM-2014werereportedbyAmezrouetal.(2017).
Inbrief,outof336 barleygenotypes,230genotypeswerecollected
fromtheLIBbreedingprogramme(genotypesadaptedforabioticand
bioticstresstolerances)and82 fromthehigh-inputbarleybreeding
programme(genotypesadaptedtofavourableconditions)ofICARDA
andtheremaining26werefrequentlyusedinbothprogrammes(Table
S1).Basedon grain types,276genotypes werehulled and 60were
hull-lessbarley.Intermsofrowtype,137genotypesweretwo-rowed
and 199 were six-rowed. The majority (73.8%) of the barley geno-
types was collected from barley breeding programmes of ICARDA
(advancedbreeding lines), but also represented genotypes fromdif-
ferentsources, including the Genetic Resource Unit (GeneBank) of
ICARDA(9.5%)andbarleyvarietiesreleasedbybreedingprogrammes
(16.6%)fromIndia,Australia,USA,Canada andMorocco.Apartfrom
a few genotypesthat originated from Indian breeding programmes,
mostgenotypesintheAM-2014hadneverbeentestedforreactions
toIndian PSHraces.TheAM-2014wasevaluatedforPSHracesbe-
causeseveralgenotypesincludedinthispanelfurnishcrossingblock
ofthe LIBprogrammeofICARDAtargetedforfeedand foodbarley
improvementacrosstheglobe.
The AM-2014 was evaluated for seedling resistance undercon-
trolled glasshouse conditions at Indian Institute of Agricultural
Research (ICAR)-Indian Institute of Wheat and Barley Research
(IIW&BR), Regional Station, Shimla, India. Five common PSH races
[(57(0S0),24 (0S0-1),M (1S0),G (4S0) andQ (5S0)]anda recently
reportedrace,7S0,wereusedtoevaluateseedlingresistance.
2.2 | Seedling stage evaluation of resistance to stripe
rust in the glasshouse
Theseedlingresistanceof336barleygenotypeswasevaluatedtoeach
ofthesixPSHraces,57(0S0),24(0S0-1),M(1S0),G(4S0)Q(5S0)and
7S0atICAR-IIW&BR,Shimla, India,followingthemethods described
byresearchers(Nayar,Prashar,&Bhardwaj,1997;Prashar,Bhardwaj,
Jain,& Datta,2007; Vermaetal., 2016;Zadoks,1961).Inbrief,alu-
miniumtrays29cm long×12cmwide×7cm deepwerefilled with
amixture offine loamand farmyardmanure (3:1).Twenty holes(10
holesineachrow,4cmdeepand5cmapart)weremadewiththehelp
ofwoodenmarkerinthesoilbed.Fiveseedsofatestgenotypewere
sownineachhole,and18genotypeswereseededinonetray.Ineach
tray,thesusceptiblecheck“Bilara-2”wasincludedatlocationsof7th
and14thholes.Bilara-2doesnotcontain anyknownPSH resistance
againstanyracesknownso farinIndia. Theseedlingswereraisedin
glasshousechambersat22±2°C,50%–70%relativehumidityand12-
hrdaylightcycle.One-week-oldseedlingswithfullyexpandedprimary
leaves were inoculated with 100mg spores of individual races sus-
pendedin 10mllightgrademineraloil (Soltrol170;ChevronPhillips
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GYAWALI et AL.
Chemicals Asia Pvt. Ltd., Singapore). The inoculated seedlings were
keptfor48hrindewchambersat16±2°Cwith>90%relativehumid-
ityand12hroftheday/nightcycle.Theplantswerethentransferred
toglasshousebenchesandincubatedat16±2°Cwith>70%relative
humidity,illuminatedatapproximately15,000luxfor12hr.Powdery
mildewwascontrolledbysprayingsulphurpowder.
Reactionsofgenotypesasinfectiontypes(IT)torustinfectionwere
recorded16–18daysafterinoculationfollowingthemodifiedmethod
(Nayaretal., 1997; Stakman, Stewart, & Loegering, 1962): where0;
(naughtfleck)=novisibleinfection,;-(fleckminus)=slightlynecrosis/
microfleckingvisible,;(fleck)=nourediabutsmallhypersensitiveflecks
present,1(one)=urediaminute,surroundedbydistinctnecroticareas,
2(two)=smalltomediumuredia surroundedbychloroticornecrotic
boarder,3(three)=urediasmalltomediuminsizeandchloroticareas
maybe present,3+(three+)=uredia largewith orwithout chlorosis,
sporulatingprofuselyandformingrings.Infectiontype33+isclassified
whenboth3and3+pustulesoccurtogether.Apictorialviewofthese
ITsispresentedinFigureS1.Theexperimentwasrepeatedtwotimes.
In repeated experiments,the majority of ITswere consistent except
veryfewcaseswheresusceptibleITswerekeptoverresistanceITs.The
ITs0to2ratingswereconsideredresistantand3to3+assusceptible
while2+,22+and3−wereconsideredintermediateITs.
2.3 | Adult- plant stage evaluation of resistance to
stripe rust in the field
All genotypes screened for seedling resistance were also screened
foradult-plantstageresistancetostriperustattheARSofRajasthan
Agricultural University (RAU) Durgapura (75° 47’ E, 26° 51’ N),
Rajasthan (RJ), India, in the 2014–2015 cropping season. The ex-
periment was laid out in an augmented design where the suscepti-
blecheck,Bilara-2,wasrepeatedineachblockof20testgenotypes.
Seeds were sown in one-metre rows with 25-cm row to row dis-
tanceforeachgenotypeon 15November 2015.Bilara-2 wassown
asspreaderperpendicular totheplots throughout theexperimental
blocks and around the perimeter of the test blocks 15days before
thesowingofexperimentalgenotypes.Striperust epidemicwascre-
atedbyinoculatingamixtureofthesixPSHraces,including57(0S0),
24(0S0-1), M (1S0),G (4S0), Q(5S0)and 7S0receivedfrom ICAR-
IIW&BRShimla,India.Theseracesweremixedinequalamountbefore
inoculation.ThespreaderplotswerefirstsyringeinoculatedatZadoks
GS10-19(21daysofseedlingstage)(Zadoks,Chang,&Konzak,1974)
withthemixedinoculaofracesfollowedbyrepeatedspraysofinoc-
ulacollectedfromspreaderrowsontothetestgenotypes.Irrigations
werecarried outas requiredtomaintainsufficienthumidityforbet-
terrustinfection.Diseaseseverityandreactionswererecordedthree
timesatZadoks60-69growthstages.
A modified Cobb scale (Peterson, Campbell, & Hannah, 1948)
wasusedinthefieldtoassessstriperustseverityandhostreactions.
HostresponseswererecordedasR=nourediapresent;TR=traceor
minuteuredia onleaves withoutsporulation;TMR=traceorminute
urediaonleaveswithsomesporulation;MR=smallurediawithslight
sporulation; MR-MS=small-to-medium-sized uredia with moderate
sporulation; MS-S=medium-sized uredia with moderate to heavy
sporulation; and S=large uredia with abundant sporulation, uredia
oftencoalescedtoformlesionsasdescribedbyRoelfs,Singh,andSaari
(1992).Thecoefficientofinfection(CI)wascalculatedbyusingdisease
severityand hostresponseaccordingtoStubbs, Prescott,Saari, and
Dubin (1986). Areaunder the disease progress curve (AUDPC) was
calculated using CI ofdisease severity data recorded threetimes at
10-dayintervals.
AUDPC=
n
i=1
[
CIi
+1
+CIi
∕2]
ti
+1
−ti
where, CIi=Coefficient of Infection as defined above on ith
days, ti =time in days at ith observation, and n =total number of
observations.
2.4 | Statistical analysis
The adult-plant stage rust severity wassubjected to ANOVA using
augmented block design. The ANOVA was performed using PROC
GLM of the SAS (SAS Institute 1988) statistical software package.
TheAUDPC ofbarleygenotypeswasdifferentiated byFisher’sleast
significant difference (LSD) (p=.05) based on the standard error of
themeandifference of17repeated checks,Bilara-2, thatwasused
in the experiment. The cut-off of rust resistance and susceptible
genotypewas245.7 AUDPCwhichwas determinedbysignificant t
testofBilara-2andtestgenotypesat0.05probability[AUDPC=162
(p < .05)] plus LSD0.05 which was AUDPC=83.7. Therefore, geno-
typeswithrust severity lowerthanthe cut-offAUDPC 245.7 were
consideredresistanceandviceversa.
3 | RESULTS
TheITsofstriperustonbarleygenotypesevaluatedatseedlingstage
arepresented inTable S1.Of thetotal genotypesevaluated,35.4%,
30.1%,25.9%,29.8%,27.1%and20.8%genotypesshowedresistance
reactionstothe races57(0S0),24 (0S0-1),M(1S0),G(4S0), Q(5S0)
and7S0, respectively(Table1). Amongthesegenotypes,91(20.8%)
genotypeswereresistant(R)andhadITsofeither0,ʹ;ʹ1,2or2-and
12(3.6%) genotypesweremoderatelyresistant(MR) andhad ITsof
2+, 22+ or 3− to race 7S0. In contrast, 225 (67%) genotypes were
susceptible(S)ITs(3,33+or3+)to7S0.TheITsofbarleygenotypesto
otherpreviouslyreportedracesarealsopresentedinTable1.
TheAUDPCof the336barleygenotypesscreenedinthefieldis
presented inTable S1 and Figure1.The ANOVAof AUDPC ofrust
severityispresentedinTable2.Highlysignificant(p < .001)effectsof
genotypeswerefoundonrustseverityatadult-plantstage.Basedon
ITs at seedling stage and AUDPC cut-off(<245.5) for resistance re-
actions, nine genotypes, namelyAM-14, AM-177,AM-37,AM-120,
AM-300,AM-36,AM-103,AM-189andAM-291,showedresistance
in both seedling and adult-plant stages (Table3). Bilara-2 showed
highly susceptible reactionwith 100S severity at 65-69 Zadoks GS
andAUDPCLSmeanwas3,282.2.Incontrast,fivegenotypes(Group
2) showed resistance IRs to all six races in seedling but showed
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GYAWALI et AL.
susceptiblereactiontothemixture ofsixPSH races(AUDPCranged
from1,350to3,100)atadult-plantstagesinthefield.
Theevaluationofadult-plant stageresistancerevealedthat18
genotypeswereimmune(I), 26genotypeshighlyresistant(HR),58
R,91MR,77moderatelysusceptible(MS),54Sand10highlysus-
ceptible(S)(Figure1). Intotal, 102(30.5%)genotypes wereresis-
tant,141(42.2%) genotypes weresusceptible whiletherest 27%
genotypeswereeitherMR.TheAPRtothe mixtureofthesixPSH
racesispresentedinTable4. Ofthe336 genotypes,88genotypes
that showed susceptible ITs at seedling stage to at least one or
more races,but were found resistance at adult-plantstage in the
field.TheAUDPCseverityinthese 88genotypesrangedfrom0 to
218. It was interestingto note that 16 genotypes which showed
susceptibleITs (3,33+ or 3+)to one ormultiple racesatseedling
screeningshowedhighlyresistancereaction(AUDPC=0)atadult-
plantstages(Table4).Amongthe89genotypeswhichshowedAPR,
68genotypesshoweddiseaseseverityof<20R, <20MRor<20MS
whileAUDPC rangedfrom3.4to162.However,sevengenotypes
TABLE1 Seedingreactionsofbarleygenotypes(n = 336)tosixPuccinia striiformisf.sp.hordeiracesundercontrolledconditionsin
glasshousein2015inShimla,India
Infection Number of genotypes
Type 57 (0S0)e24 (0S0- 1)eM (1S0)eG (4S0)eQ (5S0)e7S0e
ʹ0ʹʹ;ʹ 60(17.9) 65(19.3) 42(12.5)f22(6.5) 49(14.6) 58(17.3)
ʹ1ʹ 0(0) 0(0) 0(0) 22(6.5) 0(0) 0(0)
ʹ2ʹʹ2-ʹ 59(17.6) 36(10.7) 45(13.4) 56(16.7) 42(12.5) 12(3.6)
Resistanta119(35.4) 101(30.1) 87(25.9) 100(29.8) 91(27.1) 70(20.8)
ʹ3ʹ 33(9.8) 16(4.8) 17(5.1) 104(31) 51(15.2) 32(9.5)
ʹ33+ʹʹ3+ʹ 125(37.2) 172(51.2) 194(57.7) 72(21.4) 137(40.8) 193(57.4)
Susceptibleb158(47) 188(56) 211(62.8) 176(52.4) 188(56) 225(67)
Intermediatec33(9.8) 14(4.2) 15(4.5) 19(5.7) 30(8.9) 12(3.6)
NTd26(7.7) 33(9.8) 23(6.8) 41(12.2) 27(8) 29(8.6)
aNumberofgenotypesshowingresistantinfectiontype(IT)ʹ0ʹʹ;ʹʹ1ʹʹ2ʹʹ2-ʹ.
bNumberofgenotypesshowingsusceptibleinfectiontypeʹ3ʹʹ33+ʹʹ3+ʹ.
cIntermediateinfectiontypeswereconsideredasʹ2+ʹʹ22+ʹʹ3-ʹ.
dNottestedduetopoorgermination.
eStriperustracesusedinthestudy.
fNumberofgenotypes,valuesintheparenthesesarepercentage.
FIGURE1 Leastsquare(LS)meanof
areaunderthediseaseprogresscurve
(AUDPC)of336barleygenotypesto
striperust(Puccinia striiformisf.sp.hordei)
inDurgapura,Rajasthan,India.Disease
severityandinfectiontypeswererecorded
threetimes(attheintervalof10days)at
ZadoksGS60-69onbarleyleaves,and
areaunderthediseaseprogresscurve
(AUDPC)wascalculatedusingcoefficient
ofinfection(CI).TheAUDPCLSmeanof
Bilara-2(repeatedsusceptiblecheck)was
estimatedas3,282.2
TABLE2 Analysisofvarianceofareaunderthediseaseprogress
curve(AUDPC)ofstriperustseverityin336barleygenotypes
Source of
variation df SS MS p- Value
Block 8 4271995.5 533999 <.0001
Genotype 335 380209737 1134954 <.0001
Error 7 35535.9 5076.6
Coefficientofvariation(CV)=6.3%.
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GYAWALI et AL.
showedeither 10Sor 20MSreactionandAUDPCofthesegeno-
typeswas either187.5 or218.Bilara-2,the susceptiblecheck re-
peatedmultipletimesintheexperiment,alwaysrecorded3+ITtoall
sixracesatseedlingandrustseverityof100SorAUDPC=3,282.2
atadult-plantstages.
4 | DISCUSSION
Inthisstudy,wehavereportedstriperustresistanceofspringbar-
leygenotypesoriginatedfromICARDAtoIndianPSHraces.Nearly
21%(70outof336)genotypesshowedahighlevelofresistanceto
recentlyreportedvirulentrace7S0.Striperustresistancesidentified
inthisstudy arevaluablegeneticresourcesforthebarley breeding
programmeinthe subcontinent andelsewhere.Specifically, stripe
rustisoneofthemajorproductionconstraintsinbarleyproduction
inAsiancountriesincludingIndia,NepalandPakistan(Bahl&Bakshi,
1963;Chenetal.,1995;Luthra&Chopra,1990;Vermaetal.,2016).
Vaishetal.(2011) reportedthatPSH wasthe major foliardisease
reportedintrans-HimalayanLadakhregionofIndiawith>45%PSH
prevalence in the field. Similarly, the most popular barley cultivar
“SoluUwa”isreportedhighlysusceptibletostriperustcausing30%
yield loss in Nepal (Upreti, 2005). Several PSH-resistant cultivars
were released periodically in India in last two decades. However,
theeffectivenessofPSHresistanceislimitedtoIndiaduetothefre-
quentemergenceofnewracesandthebreakdownofseedlingand
all-stageresistance(Vermaetal.,2016).Chen(2007,2008)reported
that22newPSHisolatesweredetectedsince2002intheUSAwhile
74newraces werereported since1995–2005.The emergenceof
new PSH races was due to changes in the virulence spectrum of
TABLE3 ResistancereactionsofbarleygenotypestosixPuccinia striiformisf.sp.hordeiracesatseedlingandadult-plantstagesscreeningsin
2015 in India
Genotypes
Stripe rust infection type in seedlingaAdult- plant stageb
M (1S0) 24 (0S0- 1) 57 (0S0) G (4S0) Q (5S0) 7S0 Severity AUDPC
Group1c
AM-14 2− 0; 2 – 0; – 0 0
AM-177 2 ; 2 2C 2+ ; 0 0
AM-37 ;–0; 2−2+ 0; 5MR 24.4
AM-120 0; 0; 2–0; 2 0; 5MR 24.4
AM-300 –0; ; –2 0; 5MR 24.4
AM-36 0; 0; 0; ;- 0; 0; 20MR 109
AM-103 2−; 0; 0; 0; 0; 20MR 146
AM-189 ; 2 0; 2N 2 0; 10MS 150
AM-291 2− 2− 2− 1CN – – 10MS 150
Group2d
AM-188 2 0; 2 1 –0; 60S 1,350
AM-283 0; –2−0; 2+ 0; 100S 2,060
AM-261 2−2 2−2−2 0; 80S 2,190
AM-173 2 2 2−2−2−0; 100S 2,530
AM-87 2−2 2 1C 22+ 100S 3,100
Bilara-2e3+ 3+ 3+ 3+ 3+ 3+ 100S 3,282
BoldfacedgenotypesarealsoresistanttoleafandstemrustracesatseedlingstageinIndia.
aSeedlingresistancetesting(SRT)usingsixstriperacesinRustResearchStation,ICAR-IIW&BR,Shimla,India.C=pronouncedchlorosis,N=pronounced
necrosis,CN=bothnecroticandchloroticareapresentwithrustpostules,–=nottestedduetopoorgermination.
bStriperustresistanceevaluatedatadult-plantstageinDurgapuraResearchStation,Rajasthan,India.Theareaunderthediseaseprogresscurve(AUDPC)
wascalculatedforstriperustseverity.TheCV=6.3%andLSD0.05=83.7forAUDPCwereestimatedusingProc.GLMinSAS.
cGroup1—barleygenotypeswithseedlingandadult-plantstageresistancetostriperust.Thepedigreesofthebarleygenotypesarelistedbelow.
AM-14=GK58/3/Kc/MullersHeydla//Sls/4/Wieselbuger//Ahor1303-61//Ste/Antares.
AM-36=PENCO/CHEVRON-BAR/3/LEGACY//PENCO/CHEVRON-BAR.
AM-37=PENCO/CHEVRON-BAR/3/LEGACY//PENCO/CHEVRON-BAR.
AM-103=Arar/H.spont.19-15//Hml/3/H.spont.41-1/Tadmor/4/Barque.
AM-120=ArabiAbiad/Arar//H.spont.41-5/Tadmor/3/ArabiAbiad/Arar//H.spont.41-5/Tadmor.
AM-177=Rihane-03/3/As46/Aths*2//Aths/Lignee686/4/Alanda-01.
AM-189=Avt/Attiki//M-Att-73-337-1/3/Aths/Lignee686/4/CYDBA89#49/3/Ssn/Bda//Arar.
AM-291=IG:153849(landracefromNepal).
dGroup2—seedlingresistancebutsusceptibletoadultstage.
eBilara-2wasastriperustsusceptiblecheck.
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GYAWALI et AL.
TABLE4 Barleygenotypesshowingadult-plantresistance(APR)toPuccinia striiformisf.sp.hordeiin2015inDurgapura,Rajasthan,India
Genotypea
Infection type at seedling stageb
Adult- plant
severitycGenotypea
Infection type at seedling stageb
Adult- plant severityc
IS0 0S0- 1 0S0 4S0 5S0 7S0 IS0 0S0- 1 0S0 4S0 5S0 7S0
AM-52 2 0; 0; ;- 3+ 0; 0(0)dAM-43 3+ –e0; 3 3+ 3+ 10MR(75)
AM-73 233+ 23− 32− 0(0) AM-119 3+ 33+ 0; 2+ 2+ 2− 10MR(75)
AM-90 3+ 3+ 33+ 333+ 3+ 0(0) AM-143 0; 33+ 23N 33+ 3+ 10MR(75)
AM-108 3+ ;2+ 3C 2+ 0; 0(0) AM-147 3+ 3+ 33+ 33+ 3+ 10MR(75)
AM-162 3+ 0; 3+ 33− 3+ 0(0) AM-201 2+ ;2+ 1C 33+ 0; 10MR(75)
AM-169 3+ 3+ 3+ 3+ 3+ 3+ 0(0) AM-210 3+ 2 2 2 33+ 33+ 10MR(75)
AM-178 –e3 0; – 2 33+ 0(0) AM-245 3 0; – 3 0; 0; 10MR(75)
AM-222 333+ 33+ 33+ 30(0) AM-248 0; 3+ 3+ 33+ 3+ 10MR(75)
AM-226 3+ 33+ –3+ 30(0) AM-251 ; – 3 3 – – 10MR(75)
AM-228 3+ 33+ 3+ 3+ 3 2 0(0) AM-264 32+ 21C 33+ 2+ 10MR(75)
AM-235 3+ 3+ 3+ 3 ; 33+ 0(0) AM-305 2+ 33+ 2+ 3 3 33+ 10MR(75)
AM-247 233+ 3 3 33+ 3+ 0(0) AM-314 3+ – ––––10MR(75)
AM-252 3;- 0; 2 ; 33+ 0(0) AM-40 3+ – 0; 22+ 33+ 0; 10MS(82.8)
AM-312 0; 0; – – 3+ –0(0) AM-70 3+ 22+ 2− 23+ 10MS(82.8)
AM-319 2− 33+ 33+ 32+ 30(0) AM-187 3+ 3+ 2− 3C 33+ 3+ 10MS(82.8)
AM-322 2 ; 2 3 3 33+ 0(0) AM-306 33+ 0; 2 2− 3 3 10MS(82.8)
AM-10 3+ 3+ 3+ 33+ 3+ TMR(3.4) AM-307 33+ 33+ 222+ 2+ 3+ 10MS(82.8)
AM-96 33+ 233+ 3 3 3+ TMR(3.4) AM-213 3+ 32+ 3C 3+ 3+ 20MR(109)
AM-227 3+ 3+ 3+ 3+ 3+ 3+ TMR(3.4) AM-45 3+ 0; 0; 3+ 0; 0; 10MR(111.5)
AM-296 3+ 3+ 33+ 3+ 33+ TMR(3.4) AM-146 3+ 2− 3+ 3+ 33+ 3+ 10MS(142)
AM-326 33+ 33+ 33+ 23+ 0; TMR(3.4) AM-44 0; – 0; 2− 0; 3+ 15MR(145)
AM-330 3+ 3 2 3 0; 3+ TMR(3.4) AM-74 3+ 2 3 2 0; 0; 20MR(146)
AM-184 3+ 32− 3+ 2+ 3+ 5MR(17) AM-86 33+ 333320MR(146)
AM-76 3+ 3+ ;3N 0; 2− 5MR(20.7) AM-158 3+ 3 0; 2− 33+ 20MR(146)
AM-196 0; 3+ 33+ 333+ 3+ 5MR(20.7) AM-176 3+ ; 0; 3 – 0; 10MS(146)
AM-54 33+ 0; – 1C 2+ 2− 5MR(24.4) AM-282 2− 2 3 ;- 33+ 0; 20MR(146)
AM-83 2;- ;1C ; 1 33+ 5MR(24.4) AM-4 3+ 33+ 3+ 3+ 3+ 33+ 10MS(150)
AM-85 3+ 3+ 33+ 33+ 33+ 5MR(24.4) AM-38 3+ 3+ 3+ 33+ 3+ 10MS(150)
AM-113 3+ 0; 3 3 33+ 3+ 5MR(24.4) AM-63 33+ 3 2 3 3 3+ 10MS(150)
(Continues)
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GYAWALI et AL.
Genotypea
Infection type at seedling stageb
Adult- plant
severitycGenotypea
Infection type at seedling stageb
Adult- plant severityc
IS0 0S0- 1 0S0 4S0 5S0 7S0 IS0 0S0- 1 0S0 4S0 5S0 7S0
AM-114 3+ 33+ 3+ 33+ 33+ 3+ 5MR(24.4) AM-193 33+ 3+ 3+ 3C 33+ 10MS(150)
AM-118 3+ 3+ 3+ 3 3 3+ 5MR(24.4) AM-277 ;33+ 3+ 3+ 33+ 10MS(150)
AM-241 333+ 2+ 3+ 2 0; 5MR(24.4) AM-281 3+ 3+ 3+ 3 3 3+ 10MS(150)
AM-263 –2+ 2 3 0; – 5MR(24.4) AM-302 3+ 3+ 33+ – – 33+ 10MS(150)
AM-272 0; 0; 3+ ;- 0; 0; 5MR(24.4) AM-236 3+ 33+ 0; 3 2+ 3+ 10MS(152)
AM-315 3+ 3+ 3+ 33+ 3+ 10R(37.5) AM-200 3+ 3+ 3+ 3+ 3+ 3+ 20MR(162)
AM-128 2 0; 2− 1N 23+ 10MR(41.4) AM-270 3+ 3+ 3+ 33+ 3+ 20MR(162)
AM-205 0; 3+ 0; 3+ 3+ 310MR(41.4) AM-293 33+ 3+ 3+ 33+ 3+ 3+ 20MR(162)
AM-78 0; 3+ 33+ 3C 3+ 3+ 5S(61) AM-81 33+ 33+ 0; 2N 33+ 10S(187.5)
AM-333 3+ 3+ 3+ 3+ 3+ 3+ 10MR(71) AM-123 3+ 3+ 2 – 0; – 10S(187.5)
AM-7 2 – 0; 2 3+ 3+ 10MR(73) AM-165 3+ 3 3 33+ 33+ 10S(187.5)
AM-102 3+ 3+ 33+ 33+ 3+ 3+ 10MR(73) AM-209 33+ 22+ ; 3 2+ 3+ 10S(187.5)
AM-160 33+ 33+ 33+ 32+ 3+ 10MR(73) AM-271 2− 3+ 33+ 3N 33+ 10S(187.5)
AM-3 32+ 0; 2 33+ 3+ 10MR(75) AM-284 3+ 0; 33+ 3+ 3+ 3+ 10S(187.5)
AM-6 3− 3+ 33+ 3 3 3+ 10MR(75) AM-240 3+ 0; 2+ 3+ 3 0; 20MS(218)
AM-23 2− 22− 2N 2+ 3+ 10MR(75)d
Bilara-2f3+ 3+ 3+ 3+ 3+ 3+ 100S(3,282) Bilara-2f3+ 3+ 3+ 3+ 3+ 3+ 100S(3,282)
aBarleygenotypes.
bInfectiontypeofbarleygenotypesatseedlingstageafterchallengedwithsixstriperustracesundercontrolledconditionsintheglasshouseinShimla,India.
cStriperustseverityrecordedatadult-plantstagetoscreenresistance.Valuesintheparenthesesareareaunderthediseaseprogresscurveofstriperustseverity.TheCV=6.3%andLSD0.05=83.7wereesti-
matedusingProc.GLMinSAS.
dStriperustseverityrecordedatthirdreading,valuesintheparenthesesistheareaunderthediseaseprogresscurve(AUDPC)calculatedusingcoefficientofinfectionestimatedfromstriperustseverityrecorded
atthreedatesafterpostfloweringgrowthstages(ZadoksGS60-69)inDurgapura,Rajasthan,India.
eDatanotrecordedduetopoorseedgermination.
fBilara-2wasastriperustsusceptiblecheckandwasrepeated18timesinbothseedlingscreeningintheglasshouseinFlowerdale,Shimla,andadult-plantstagescreeninginthefieldinDurgapura,Rajasthan,
India.
TABLE4 (Continued)
8
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GYAWALI et AL.
stripe rust (Chen, 2007). Kumar, Holtz, Xi, and Turkington (2012)
reportedhighlydiversePSHpathotypesfromCanadacompared to
isolatesreportedinthepast.Theemergenceofnew PSHrace7S0
in India was consistent with previous reports (Chen, 2007, 2008;
Kumar etal., 2012). Genotypes AM-177, AM-37, AM-120, AM-
300,AM-36,AM-130,AM-189andAM-274providedresistanceto
newlyevolvedvirulent race 7S0 atseedlingand adult-plantstage
besidespreviouslyreportedPSHraces.Therefore,theidentification
ofresistance sourcesin low-input genotypes,in thecurrent study,
willprovideprotectionagainstmajorPSHracescurrentlyprevalent
in India.
GenotypesAM-14,AM-177, AM-37,AM-120,AM-300,AM-36,
AM-130,AM-189,AM-291and AM-274showed resistanceat both
seedlingandadult-plantstages.Park(2008)suggestedthatwhengen-
otypesshow rustresistance atboth seedlingand adult-plantstages,
itcanbereferredtoasall-stageresistance.Possibly,thesegenotypes
mighthaveall-stageresistanceto PSHracesprevalentinIndia. The
seedlingresistanceisnotgrowthstage-dependent(Park,2008;Singh,
1992;Singhetal., 2015). However,seedlingresistance does notal-
waysprovide protectionagainst rust atadult-plant stages.Our data
also suggested that genotypes AM-87, AM-173, AM-188,AM-261
andAM-283possessedseedlingresistance,butfailedtoprotectfrom
PSH,withAUDPC>218,atadult-plantstage.Therefore,a genotype
withstriperust resistanceat seedling stagealone is notsustainable
andeffectivefor along-term deployment(Park,2008; Singh,1992;
Singh etal., 2015). Often, seedling resistance is governedby major
gene(s)andfrequentmutationsin correspondingavirulencegenes in
therust pathogenmayleadtocatastrophicfailureofthecrop(Park,
2008). Therefore, identification of any new sources of resistance
to new PSH races is extremely important for barley breeding pro-
grammes. The central barley breeding programme ofICAR-IIW&BR
at Karnal aswell as several regional barley breedingprogrammes in
Indiawillimmediatelybenefitfromthecurrentlyidentifiedstriperust
resistancesinthisstudy.
Eightgenotypes,resistancetoPSHrace7S0thatisidentifiedin
thecurrentstudy,havediverse pedigrees.AM-36andAM-37are
sister lines and share a common pedigree(PENCO / CHEVRON-
BAR/3/LEGACY//PENCO/CHEVRON-BAR);however,thedonor
plant is unknown. Genotypes AM-103 and AM-120 also share
commonparentagesapartfromonewildbarleyaccession.TheAM-
103 contains two wild accessions in its pedigree, Hordeum spon-
taneum19-15andH. spontaneum41-5(IG_138213)whileAM-120
has H. spontaneum 41-5 only. Among these, two wild accessions,
IG_138213 is one of the important sources ofdrought tolerance
in the LIB programmes of ICARDA.We do not know which wild
accessions contributed to PSH resistance in these two resistant
genotypes.Therefore,furtherresearch iswarranted to studyPSH
7S0resistanceinthesewildaccessions.Similarly,AM-177andAM-
189alsosharecommonparentage,buttheirITsweredifferentthan
otherresistantgenotypes.Possibly,thesegenotypesmaycarrydif-
ferentresistantgene(s),but furtherresearchonallelic relationship
oftheseresistance sourcesisneededtoverifythenatureofthese
resistancesources.
TheAPRto IndianPSHracesreportedinthisstudyisunique.Of
88genotypes,whichshowedahighlevelofAPR,16genotypesexhib-
ited immune (AUDPC=0) responses at adult-plant stage screening.
Vermaetal. (2016) reported that weather conditions in Durgapura,
RJ,favoursthestriperustdevelopmentinbarleycomparedtoKarnal
andotherlocationsinIndia.Theweatherconditions,temperatureand
humidity in 2014–2015 growing season (data not presented) were
favourableforstripe rustinfection, rustdevelopmentandsecondary
spreadsofstriperusturediniosporesfromspreaderrowstotestgeno-
types.AsBilara-2consistentlyscored100SandanabaverageAUDPC
of3,282onall17repeatedplots,the16linesthatshowedimmunere-
sponsesarelikelyduetostrongresistance.Park(2008),Carlborgand
Haley(2004),Golegaonkaretal.(2009);Singhetal.(2015)andSingh
(1992)reportedthatAPRisconditionedbyadditivegenes;therefore,
phenotypicresponsesofAPRgenesaregenerallyquantitativeinna-
ture.Similarly,theadult-plantstagePSH-resistantgenotypesreported
by Safavi (2012) exhibitedslow rusting responses which suggested
thatPSH resistancewasquantitativeinnature.In thisstudy,the im-
muneresponseofthese16genotypes,atadult-plantstagescreening,
wasuniqueinnatureandrequiresfurthergeneticstudiestoelucidate
natureofPSHresistance.However,thisresultwasconsistentwithim-
munetype ofstriperustresistanceattheadult-plantstagereported
byVermaetal.(2016) inIndia.Inwheat,severalreportsareavailable
whereimmuneorhigherlevelofAPRhasbeenreported(Milus,Moon,
Lee,& Mason,2015;Sørensen, Hovmøller,Leconte,Dedryver, &de
Vallavieille-Pope, 2014). Milus etal. (2015) described these APRs
asrace-specificAPRin winterwheat.The89 barleygenotypeswith
higher levelof APR reported in this studyshowed susceptible IT to
atleastone PSHraceatseedlingstage, butrecordedAUDPC ≤218
(Table4). Therefore, these genotypes were able to slow down the
stripe rust infections at adult-plantstage, which were in agreement
withpreviouslyreportedAPRto stripe,leafandstemrusts inbarley
(Carlborg&Haley,2004;Golegaonkaretal.,2009;Park,2008;Singh,
1992;Singhetal.,2015)andAPRtostriperustinwheat(Hickeyetal.,
2011;Milusetal., 2015;Sørensen etal.,2014). TheAPR genotypes
identifiedin thisstudyarevaluable resourcesofPSH resistanceand
canprovideeffectiveanddurableresistanceagainstPSHparticularly
iftheyarecombinedwithseedlingresistance.Themarker–traitasso-
ciationstudiesusing9KiSelectIlluminaInfiniumSNPschipandstripe
rustresistanceto thesixracesatseedlingandadult-plantstagesare
inprogress.
ACKNOWLEDGEMENTS
Theauthors sincerelyacknowledgeinternal reviewerDr.SeidKemal
fromICARDAforvaluablecomments andsuggestions.Thisresearch
wasfundedbytheCRPDrylandCerealsProgram.Theauthorsdeclare
thatthereisnoconflictofinterest.
ORCID
Sanjaya Gyawali http://orcid.org/0000-0003-1202-909X
Om Prakash Gangwar http://orcid.org/0000-0002-5393-163X
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GYAWALI et AL.
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