h tt p : / / w w w . b j m i c r o b i o l . c o m . b r /
Environmental
Microbiology
Plant
growth
promoting
rhizobacteria
reduce
aphid
population
and
enhance
the
productivity
of
bread
wheat
Muhammad
Naeem
a,b,
Zubair
Aslam
a,
Abdul
Khaliq
a,
Jam
Nazir
Ahmed
c,
Ahmad
Nawaz
d,
Mubshar
Hussain
b,∗aUniversityofAgriculture,DepartmentofAgronomy,Faisalabad,Pakistan bBahauddinZakariyaUniversity,DepartmentofAgronomy,Multan,Pakistan cUniversityofAgriculture,DepartmentofEntomology,Faisalabad,Pakistan dBahadurSub-Campus,BZU,CollegeofAgriculture,Layyah,Pakistan
a
r
t
i
c
l
e
i
n
f
o
Articlehistory:
Received11April2017 Accepted14October2017 Availableonline24April2018 AssociateEditor:JerriZilli
Keywords: Pseudomonas Bacillus Aphid Breadwheat PGPR Eco-friendly
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c
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Plantgrowthpromotingrhizobacteriaincreaseplantgrowthandgiveprotectionagainst insectpestsandpathogens.Duetothenegativeimpactofchemicalpesticideson environ-ment,alternativestothesechemicalsareneeded.Inthisscenario,thebiologicalmethods ofpestcontrolofferaneco-friendlyandanattractiveoption.Inthisstudy,theeffectof twoplantgrowthpromotingrhizobacterialstrains(Bacillussp.strain6andPseudomonas
sp.strain6K)onaphidpopulationandwheatproductivitywasevaluatedinanaphid sus-ceptible(Pasban-90)andresistant(Inqlab-91)wheatcultivar. Theseedswereinoculated witheachPGPRstrain,separatelyorthecombinationofboth.Thelowestaphidpopulation (2.1tiller−1),andhighestplantheight(85.8cm),numberofspikeletsperspike(18),grainsper spike(44),productivetillers(320m−2),strawyield(8.6Mgha−1),andgrainyield(4.8Mgha−1) wereachievedwhenseedswereinoculatedwithBacillussp.strain6+Pseudomonassp.strain 6K.Thegrainyieldofbothvarietieswasenhancedby35.5–38.9%withseedinoculationwith bothbacterialstrains.Thus,thecombineuseofbothPGPRstrainsviz.Bacillussp.strain 6+Pseudomonassp.strain6Koffersanattractiveoptiontoreduceaphidpopulationtied withbetterwheatproductivity.
©2018SociedadeBrasileiradeMicrobiologia.PublishedbyElsevierEditoraLtda.Thisis anopenaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/
licenses/by-nc-nd/4.0/).
∗ Correspondingauthor.
E-mail:mubashiragr@gmail.com(M.Hussain).
Introduction
Breadwheat(TriticumaestivumL.)isthemostessentialcereal cropandstaplefoodforthemajorityofthemankind.1 Itis grownonanareaof>200millionhectaresallovertheworld andmeets21%ofglobalfoodrequirement.2Itisastaplefood
https://doi.org/10.1016/j.bjm.2017.10.005
1517-8382/©2018SociedadeBrasileiradeMicrobiologia.PublishedbyElsevierEditoraLtda.ThisisanopenaccessarticleundertheCC BY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).
ofPakistani people,andcontributes2.2%inGDPand10.3% towardvalueaddedinagriculture.In2015–16,itwascultivated onanareaof9.26millionhectareswiththeproductionof25.48 milliontons.3
Bioticandabioticstressesareseriousenvironmental con-straintswhichreducetheyieldofcerealsacrosstheglobe.4,5 Duringrecentyears,theRussianwheataphids(blackaphids) have emerged as a serious threat to wheat production in Pakistan.Itsattackismoresevereatreproductiveandgrain fillingstages,thuscausingaseveredeclineincropyieldand thequalityofproduce.Itsworstinfestationmaycauseyield declineof21–92%inaphidsusceptiblecultivarsofwheat.6 Indeed,theaphidsucksthecellsapfromleaves,whichaffects thephotosyntheticefficiencyandreproductivedevelopment ofplants. Italsoexcretessugarymaterialwhichfavorsthe growthoffungiontheleafsurface,7thusaffectingthewheat performancenegatively.
Although,variouspesticidesarebeingemployedto con-trol aphid.8 However, the use of pesticides in wheat may cause the health problems if the pesticide residues retain inthewheatgrain. Moreover,pesticidesare greaterrisk to the long term sustainabilityofour ecosystemdue totheir negativeimpactsonhumanbeingsandothersoilbiological community.9
Thegeneticresistanceofwheattoaphidhasbeenreported. For example,Elek etal.10 tested thediploid, tetraploidand hexaploidwheatlinesfortheirresistanceagainstaphid.They foundthatthesynthesisofhydroxamicacids[especially 2,4-dihidroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA)], was responsible for inducing resistance against aphid in these wheat lines. Another possible way to reduce the aphid populationinwheatistheuseofplant-growth-promoting rhi-zobacteria(PGPR).11 These PGPRsinduce resistanceagainst insectpests throughsynthesisofphytohormones,increase in phosphorus and nitrogen uptake and increase in iron and mineral solubility through chelation growth.12 Several PGPRstrainsespecially,Bacillusand Pseudomonasstrainsare alsobeing used as inoculant biofertilizers,13,14 which have directandindirecteffectsoninsectpestresistance.13,15,16The PGPR(especiallyBacillusandPseudomonasstrains)suppressthe soil-bornepathogensbysiderophoresproductionand antimi-crobial metabolites.16 Indirect effects include the induced systematicresistancethusenhancingtheresistanceagainst variouspathogensandpestsbythesynthesisofphysicaland chemicalbarriersinthehost.17–20Therhizobacteriamediated inducedsystemicresistanceresemblesthesystemicacquired resistancewhichisinducedinpathogensincludingthe nema-todes,insects,bacterial,fungalandviralpathogens.21,22This induced systemic resistance ispromoted byPGPR through signaling pathwaywhereas systemicacquired resistanceis the phenomenon used to explain salicylic acid dependent inducedresistanceactivatedbylocaldisease.23Severalstudies have reported that the spotted cucumber beetle
(Diabrot-ica undecimpunctata),24 green peach aphid (Myzus persicae Sulzer),25 andnymphpopulation ofwhitefly (Aleyrodidae),26 bluegreenaphid(AcyrthosiphonkondoiShinji)onMedicagoand white clover plants,27 and population size and population growthofcottonaphids(AphisgossypiiGlover)oncucumber,28 was significantly decreased by the application ofdifferent PGPRstrains.
However,tothebestofourknowledge,nostudyhasbeen conductedtochecktheinfluenceofPGPRstrainsontheaphid populationandproductivityofbreadwheat.Thus,thisstudy wasconductedtoevaluatetheinfluenceoftwoPGPRstrains (Bacillussp.strain6andPseudomonassp.strain6K)onbread wheatgrowthandaphidpopulation.
Materials
and
methods
Preparationofinoculumandseedinoculationprocedure
The Bacillus strain 6 and Pseudomonas strain 6K – used as positivecontrol–were obtainedfrom theSoilMicrobiology Laboratory,InstituteofSoilandEnvironmentalScience, Uni-versityofAgriculture,Faisalabad.TheBacillusstrainwasgram positive,rodshaped,aerobic,endosporeforming,fastgrowing withwhitishcolonies.ThePseudomonasstrainwasgram neg-ative,fastgrowing,rodshaped,withoff-whitecoloniesand motilecells.
TheInoculumwaspreparedbygrowingthetwoselected PGPR strains in a nutrient broth. It was incubated at 28◦C with 100revmin−1 shaking. Four days old inoculum (107–108CFUmL−1) was inserted into germ free peat at
100mLkg−1peatandincubatedat28◦Cfor24hproceeding towheatseedinoculation.Thepeatwasmadegermfreeby bakingpeatinanovenfor30minat180◦F.
Wheatseeds(Pasban-90andInqlab-91)wereinoculatedby incorporatingwithpeatand10%sugarsolution(100mLkg−1) onpeat;whereascontroltreatmentseedsweretreatedwith peatandsugarsolutionwithoutPGPR.Seedsweredriedup undershadowfor6–8h.
Experimentalsiteandtreatments
ThisexperimentwascarriedoutatStudent’sFarm,University ofAgricultureFaisalabad,Pakistanin2013.Theexperiment comprisedoftwowheatcultivars(Pasban-90andInqlab-91) and twoPGPRstrains(Bacillus sp.strain6andPseudomonas
sp.strain6K).Thebothbacterialstrainswereinoculatedon seeds alone orin combination.Non-inoculatedseeds were alsosownasacontroltreatment.Thewheatseedsofboth varietieswerecollectedfromWheatResearchInstitute,Ayub Agricultural ResearchInstitute, Faisalabad.Theexperiment was carriedout inrandomizedcompleteblockdesignwith factorialarrangementhavingthreereplications.Thenetplot sizewas1.8m×5m.Theseedsofbothvarietiesweresown withsinglerow handseeddrillbymaintaining rowtorow distanceof22.5cmonNovember25,2013,usingseedrateof 125kgha−1.
Onthebasisofsoilanalysis,thefertilizerwasappliedat therateof120–90–60kgN,P,Kha−1,usingurea,diammonium phosphate (DAP)and muriate ofpotash (MOP)as sources, respectively.Halfofthenitrogenandthefulldoseof potas-siumandphosphorouswasappliedatthetimeofsowing.The remaininghalfdoseofnitrogenwasappliedattilleringstage through broadcasting.Dataonaphidpopulation(aphid per tiller)wererecordedfromtwentytillersineachplotmanually andthenaveraged.Moreoverthedataregardingplantheight (cm),productivetillers(m2),spikelength(cm),spikeletsper
Table1–Effectofplantgrowthpromotingrhizobacteriaonplantheight,productivetillersandspikelengthoftwowheat varieties.
Treatment Plantheight(cm) Productivetillers(m−2) Spikelength(cm)
Pasban-90 Inqlab-91 Pasban-90 Inqlab-91 Pasban-90 Inqlab-91
T0 78.7f 82.0de 232d 263c 8.9f 9.04ef
T1 84.1bc 84.0bcd 277bc 273bc 9.8de 9.8de
T2 81.8e 82.3cde 289bc 288bc 10.5cd 11.9b
T3 85.2b 88.9a 300b 339a 11.1bc 13.7a
LSD(p≤0.05) 1.99 30 0.85
Figuresofinteractionsharingthesamecaseletterdonotdiffersignificantlyatp≤0.05;T0=noseedinoculation;T1=seedinoculationwith
Bacillussp.strain6;T2=seedinoculationwithPseudomonassp.strain6K;T3=seedinoculationwithBacillussp.strain6+Pseudomonassp.strain
6K.
Table2–Effectofplantgrowthpromotingrhizobacteriaonspikeletsperspike,grainsperspike,andbiologicalyieldof twowheatvarieties.
Treatment Spikeletsperspike Grainsperspike Biologicalyield(Mgha−1)
Pasban-90 Inqlab-91 Pasban-90 Inqlab-91 Pasban-90 Inqlab-91
T0 15.7e 16.9cd 37.2e 39.2d 14.1f 15.1d
T1 16.5d 17.5bc 40.3de 41.8c 14.5e 15.4b
T2 16.9cd 17.8ab 40.9cd 44.4b 14.6e 15.6b
T3 17.1c 18.4a 42.1c 46.7a 15.3c 15.9a
LSD(p≤0.05) 0.65 1.45 0.14
Figuresofinteractionsharingthesamecaseletterdonotdiffersignificantlyatp≤0.05;T0=noseedinoculation;T1=seedinoculationwith
Bacillussp.strain6;T2=seedinoculationwithPseudomonassp.strain6K;T3=seedinoculationwithBacillussp.strain6+Pseudomonassp.strain
6K.
Table3–Effectofplantgrowthpromotingrhizobacteriaonstrawyieldandgrainyieldoftwowheatvarieties.
Treatment Strawyield(Mgha−1) Grainyield(Mgha−1)
Pasban-90 Inqlab-91 Pasban-90 Inqlab-91
T0 6.0g 7.6e 3.6h 4.0g
T1 7.3f 8.1c 4.1f 4.2e
T2 7.9d 8.6b 4.4d 4.5c
T3 8.2c 9.0a 4.6b 5.0a
LSD(p≤0.05) 0.12 0.04
Figuresofinteractionsharingthesamecaseletterdonotdiffersignificantlyatp≤0.05;T0=noseedinoculation;T1=seedinoculationwith
Bacillussp.strain6;T2=seedinoculationwithPseudomonassp.strain6K;T3=seedinoculationwithBacillussp.strain6+Pseudomonassp.strain
6K. a d b f c g e g 0 2 4 6 8 10 12
Pasban Inqlab
A p hi d po pu la ti on (t ill er -1) Wheat varieties
Control Bacillus Pseudomonas combination
spike,straw yield(Mgha−1), andgrainyield(Mgha−1)were recordedfollowingFarooqetal.29
Statistical
analysis
Thedatacollectedduringtheexperimentwereanalyzedusing theFisher’sanalysisofvariancetechnique(twowayanova) andthetreatments’ meanswere comparedbyleast signifi-cancedifference(LSD)testat5%probabilitylevel.30Thedata analysiswasperformedusingrandomizedcomplete design infactorialarrangementwiththehelpofstatisticalsoftware ‘Statistics8.1’.
Results
Bothwheatcultivarsdiffersignificantlyforplantheight, pro-ductive tillers,spike length, spikelets per spike,grains per spike,biologicalyield,strawyield,grainyieldandaphid pop-ulation. Likewise, seed inoculation withboth PGPR strains significantlyaffectedtheplantheight,productivetillers,spike length,spikeletsperspike,grainsperspike,biologicalyield, strawyield,grainyieldandaphidpopulation.Theinteraction ofwheatcultivarswithPGPRswasalsosignificantforplant height, productivetillers, spike length,spikelets per spike, grainsperspike,biologicalyield,strawyield,grainyieldand aphidpopulation(Tables1–3).
The aphid population was significantly reduced by the application of PGPR strains. The minimum population of aphid (2.1 aphids per tiller) was recorded in Inqlab-90 whenitwasinoculatedwithmixtureofPGPRstrains
(Bacil-lus+Pseudomonas strains) as seed treatment, and that was statistically similar with Inqlab-90 inoculated with Pseu-domonasstrains.Themaximumaphidpopulation(8.2aphids pertiller)wasrecordedinPasban-90withoutinoculationwith anybacterialstrains(Fig.1).
The interaction of wheat cultivars with PGPR strains showedthatthehighestplantheight,productivetillers,spike length,spikeletsperspike,grainsperspike,biologicalyield, strawyieldandgrainyieldwererecordedinInqalab-91with seed inoculation with both of the bacterial strains
(Bacil-lus+Pseudomonasstrains).Seedinoculationwithbothbacterial strainsenhancedthegrainsperspikeby25.5%thancontrol inInqalab-91.Thegrainyieldwasalsoenhancedby38.9%in Inqalab-91withseedinoculationwithbothbacterialstrains. InPasban-90,thegrain yieldwas increasedby35.5%when seedswereinoculatedwithbothbacterialstrainsthancontrol
(Tables1–3).
Discussion
UseofbothPGPRstrainseitheraloneorincombinationwas veryusefulforthecontrolofaphidpopulation. Indeed,the PGPRincreasetheaccumulationofphenoliccompoundsand phytoalexins,theactivitiesofdefenseenzymes/genes (encod-ing glucanase, chitinase, and peroxidase), transcripts and pathogenesis-relatedproteins,increasethelignificationand
modulatetheethylene-modulatedsignaltransduction path-way,andinducethephysiologicalchangeswithinplants,31–36 whichimprovetheplantsdefenseagainstinsectpestattack. PGPRs alsoinhibitthe croppeststhroughrelease of differ-ent volatileand diffusiblemetabolites(e.g. pyoluteorinand pyrrolnitrin),37 which are toxicto insect pests thus reduc-ingtheirpopulationaswasobservedinthisstudy.Likewise, the improvementin aphid suppression and wheat growth mightbeattributedtotheproductionofsiderophores.16The indirect effectsofPGPRincludetheinductionofsystematic resistancethusenhancingtheresistanceagainstinsectpests by the synthesis of physical and chemical barriers in the host.17–20
Moreover,thePGPRshelpstoimprovethephosphorusand nitrogen uptake and enhance the activity of indole acetic acidwhichhelpsthewheatplanttouptakeandtranslocate themicroandmacronutrients(zinc,iron,nitrogenand man-ganese) ina better way.These nutrients playa significant roleinbiogeochemicalcyclingandincreasestheactivitiesof defenseenzymes againstpathogen.38,39 Several other stud-ies have reported that application ofvarious PGPR strains enhancedtheresistanceagainstinsectpestinfieldand veg-etablecrops.24–27
Better aphid controldue toseed inoculationwith PGPR resultedinbettercropgrowthwhichultimatelyenhancedthe plantgrowthandtheplantheight.Thebettergrowthdueto PGPRapplicationasaresultofaphidcontrolfinallyresulted inbettergrainpartitionwhichenhancedthenumberofgrains per spike. The highest grain yieldin both wheat varieties due toapplication ofthe PGPRmight beattributedto bet-ter grainsperspikeand productivetillers.Itiswell known that the productive tillersand grains per spike are impor-tant yieldcontributingtraitswhich resultedinbettergrain yieldinthisstudy.Inanotherstudy,Hilalietal.40speculated that plantheight and spikeletsper spike wasincreasedin manycropsbymicrobialinoculation.Rodriguezetal.41also observedsignificantincreaseinwheatyieldbythe applica-tion of P solubilizing and N2 fixing Bacillus sp. The better
grainyieldinwheatinthisstudymightbeattributedtothe directeffectofPGPRsonwheatandtheirindirecteffecton aphidsuppression.Besidesuppressingthepests,thePGPRs alsopromote theplant growththrough productionof vari-ousplanthormones(e.g.abscisicacid,ethylene,cytokinins, and auxins), indole-3-acetic acid, indole-3-ethanol and 1-aminocyclopropane-1-carboxylatewhichpromoteshootand root growth.42 Thereisdire needtoextend this study and understand the whole mechanism how the PGPRaffecting defensemechanismandenhancingyieldofbreadwheat.
Inconclusion,combineuseofbothPGPRstrainsviz. Bacil-lussp.strain6+Pseudomonassp.strain6Koffersanattractive optiontoreducetheaphidpopulationandenhancethe pro-ductivityofbreadwheat.
Conflicts
of
interest
r
e
f
e
r
e
n
c
e
s
1.FarooqM,HussainM,SiddiqueKHM.Droughtstressin
wheatduringfloweringandgrain-fillingperiods.CritRev
PlantSci.2014;33:331–349.
2.FAO.FoodandAgricultureOrganization(FAO),UnitedNations;
2010.
3.GovernmentofPakistan.PakistanEconomicSurvey2015–16.
Islamabad:FinanceDivision,EconomicAdvisor’sWing;
2016:28.
4.AfzalA,BanoA.Rhizobiumandphosphatesolubilizing
bacteriaimprovetheyieldandphosphorusuptakeinwheat
(Triticumaestivum).IntJAgricBiol.2008;10:85–88.
5.HussainM,Waqas-ul-HaqM,FarooqS,JabranK,FarooqM.
Theimpactofseedprimingandrowspacingonthe
productivityofdifferentcultivarsofirrigatedwheatunder
earlyseasondrought.ExpAgric.2016;52:477–490.
6.BaskyZ.Biotypicandpeststatusdifferencesbetween
HungarianandSouthAfricanpopulationsofRussianwheat
aphid,Diuraphisnoxia(Kurdjumov)(Homoptera:Aphididae).
PestManageSci.2003;59:1152–1158.
7.KhanAM,KhanAA,AfzalM,IqbalMS.Wheatcropyield
lossescausedbytheaphidsinfestation.JBiofertilBiopestic.
2012;3:122.
8.MicicS.InsecticidesfortheControlofCerealAphids;2017. Availablefrom:
https://www.agric.wa.gov.au/barley/insecticides-control-cereal-aphidsAccessed09.09.17.
9.AktarW,SenguptaD,ChowdhuryA.Impactofpesticidesuse
inagriculture:theirbenefitsandhazards.InterdisciplToxicol.
2009;2:1–12.
10.ElekH,WernerP,SmartL,Gordon-WeeksR,NádasyM,
PickettJ.Aphidresistanceinwheatvarieties.CommunAgric
ApplBiolSci.2009;74:233–241.
11.VejanP,AbdullahR,KhadiranT,IsmailS,NasrulhaqBoyceA.
Roleofplantgrowthpromotingrhizobacteriainagricultural
sustainability—areview.Molecules.2016;21:573.
12.BowenGD,RoviraAD.Therhizosphereanditsmanagement
toimproveplantgrowth.AdvAgron.1999;66:1–102.
13.KennedyIR,ChoudhuryA,KecskésML.Non-symbiotic
bacterialdiazotrophsincrop-farmingsystems:cantheir
potentialforplantgrowthpromotionbebetterexploited?
SoilBiolBiochem.2004;36:1229–1244.
14.HussainM,ZsgherA,TahirM,etal.Bacteriaincombination
withfertilizersimprovegrowth,productivityandnetreturns
ofwheat(TriticumaestivumL.).PakJAgricSci.2016;53:633–645.
15.Persello-CartieauxF,NussaumeL,RobagliaC.Talesfromthe
underground:molecular.PlantCellEnviron.2003;26:189–199.
16.NelsonLM.Plantgrowthpromotingrhizobacteria(PGPR):
prospectsfornewinoculants.CropManage.2004;3:301–305.
17.KloepperJW,RyuCM,ZhangS.Inducedsystemicresistance
andpromotionofplantgrowthbyBacillusspp.
Phytopathology.2004;94:1259–1266.
18.BostockRM.Signalcrosstalkandinducedresistance:
straddlingthelinebetweencostandbenefit.AnnuRev
Phytopathol.2005;43:545–580.
19.StoutMJ,ThalerJS,ThommaBP.Plant-mediatedinteractions
betweenpathogenicmicroorganismsandherbivorous
arthropods.AnnuRevEntomol.2006;51:663–689.
20.TuzunS,BentE.MultigenicandInducedSystemicResistancein
Plants.NewYork:SpringerScience+BusinessMedia,Inc; 2006.
21.BentE.Inducedsystemicresistancemediatedbyplant
growth-promotingrhizobacteria(PGPR)andfungi(PGPF).In:
TuzunS,BentE,eds.MultigenicandInducedSystemicResistance
inPlants.NewYork:SpringerScience;2006:225–259.
22.PozoMJ,Azcón-AguilarC.Unravelingmycorrhiza-induced
resistance.CurrOpinPlantBiol.2007;10:393–398.
23.VleesschauwerD,HöfteM.Rhizobacteria-inducedsystemic
resistance.AdvBotRes.2009;51:223–281.
24.ZehnderG,KloepperJ,TuzunS,etal.Insectfeedingon
cucumbermediatedbyrhizobacteria-inducedplant
resistance.EntomolExpAppl.1997;83:81–85.
25.BoughtonAJ,HooverK,FeltonGW.Impactofchemical
elicitorapplicationsongreenhousetomatoplantsand
populationgrowthofthegreenpeachaphid,Myzuspersicae.
EntomolExpAppl.2006;120:175–188.
26.MurphyJF,ZehnderGW,SchusterDJ,SikoraEJ,PolstonJE,
KloepperJW.Plantgrowth-promotingrhizobacterial
mediatedprotectionintomatoagainsttomatomottlevirus.
PlantDis.2000;84:779–784.
27.KempsterVN,ScottES,DaviesKA.Evidenceforsystemic,
cross-resistanceinwhiteclover(Trifoliumrepens)andannual
medic(Medicagotruncatulavar.truncatula)inducedby
biologicalandchemicalagents.BiocontrolSciTechnol.
2002;12:615–623.
28.StoutMJ,ZehnderGW,BaurME.Potentialfortheuseof
elicitorsofplantdefenseinarthropodmanagement
programs.ArchInsectBiochem.2002;51:222–235.
29.FarooqS,ShahidM,KhanMB,HussainM,FarooqM.
Improvingtheproductivityofbreadwheatbygood
managementpracticesunderterminaldrought.JAgronCrop
Sci.2015;201:173–188.
30.SteelRGD,TorrieJH,DickyDA.PrinciplesandProceduresof
Statistics:ABiometricalApproach.3rded.NY,USA:McGraw
Hill,Inc.BookCo.;1997:352–358.
31.MeenaB,RadhajeyalakshmiR,MarimuthuT,Vidhyasekaran
P,DoraiswamyS,VelazhahanR.Inductionof
pathogenesis-relatedproteins,phenolicsandphenylalanine
ammonia-lyaseingroundnutbyPseudomonasfluorescens.J
PlantDisProt.2000;107:514–527.
32.KavinoM,HarishS,KumarN,etal.Rhizosphereand
endophyticbacteriaforinductionofsystemicresistanceof
bananaplantletsagainstbunchytopvirus.SoilBiolBiochem.
2007;39:1087–1098.
33.RajendranL,SamiyappanR,RaguchanderT,Saravanakumar
D.Endophyticbacteriamediateplantresistanceagainst
cottonbollworm.JPlantInteract.2007;2:1–10.
34.SaravanakumarD,VijayakumarC,KumarN,SamiyappanR.
PGPR-induceddefenseresponsesintheteaplantagainst
blisterblightdisease.CropProt.2007;26:556–565.
35.HarishS,KavinoM,KumarN,SaravanakumarD,
SoorianathasundaramK,SamiyappanR.Biohardeningwith
plantgrowthpromotingrhizosphereandendophytic
bacteriainducessystemicresistanceagainstbananabunchy
topvirus.ApplSoilEcol.2008;39:187–200.
36.VleesschauwerD,DjavaheriM,BakkerPAHM,HofteM.
PseudomonasfluorescensWCS374r-Inducedsystemic
resistanceagainstMagnaportheoryzaeisbasedon
pseudobactin-mediatedprimingforasalicylic
acid-repressiblemultifaceteddefenseresponse.PlantPhysiol.
2008;148:1996–2012.
37.GuttersonN.Microbialfungicides:recentapproachesto
elucidatingmechanisms.CritRevBiotechnol.1990;10:
69–91.
38.RanaA,SaharanB,JoshiM,PrasannaR,KumarK,NainL.
IdentificationofmultitraitPGPRisolatesandevaluating
theirpotentialasinoculantsforwheat.AnnMicrobiol.
2011;61:893–900.
39.PinedaA,ZhengSJ,VanLoonJA,PieterseMJ,DickeM.
Helpingplantstodealwithinsects:theroleofbeneficial
soil-bornemicrobes.TrendsPlantSci.2010;15:
40.HilaliA,PrzvostD,BroughtonWJ,AntounH.Effectsde
I’inoculationavecdessouchesdeRhizobiumleguminosarum
bv.trifoliisurlacroissancedubl’edansdeuxsolsduMarco.
CanJMicrobiol.2001;47:590–593.
41.RodriguezCEA,GonzalesAG,LopezJR,DiCiaccoCA,Pacheco
BJC,ParadaJL.Responseoffield-grownwheattoinoculation
withAzospirillumbrasilenseandBacilluspolymyxainthe
semiaridregionofArgentina.SoilsFertil.1996;59:800.
42.HayatR,AliS,AmaraU,KhalidR,AhmedI.Soilbeneficial
bacteriaandtheirroleinplantgrowthpromotion:areview.
