Significant decrease in yield under future climate conditions: Stabilityand production of 138 spring barley accessions

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ContentslistsavailableatScienceDirect

European

Journal

of

Agronomy

jo u r n al hom e p a g e :w w w . e l s e v i e r . c o m / l o c a t e / e j a

Signiﬁcant

decrease

in

yield

under

future

climate

conditions:

Stability

and

production

of

138 spring

barley

accessions

Cathrine

Heinz

Ingvordsen

a,∗

_,

_Gunter

_Backes

b

_,

_Michael

_Foged

_Lyngkjær

c

_,

Pirjo

Peltonen-Sainio

d

_,

_Jens

_Due

_Jensen

e

_,

_Marja

_Jalli

d

_,

_Ahmed

_Jahoor

e

_,

Morten

Rasmussen

f

_,

_Teis

_Nørgaard

_Mikkelsen

a

_,

_Anders

_Stockmarr

g

_,

Rikke

Bagger

Jørgensen

a

a_Centre_for_Ecosystems_and_{Environmental}_{Sustainability,}_Department_of_Chemical_and_Biochemical_Engineering,_Technical_University_of_Denmark, Frederiksborgvej399,RoskildeDK-4000,Denmark

b_University_of_Kassel,_Faculty_of_Organic_Agricultural_Sciences,_Section_of_Organic_Plant_Breeding_and_{Agrobiodiversity,}_{Nordbahnhofstr.}_1a, WitzenhausenD-37213Germany

c_University_of_Copenhagen,_Department_of_Plant_and_{Environmental}_Sciences,_{Thorvaldsensvej}_40,_{Frederiksberg}_C_DK-1871,_Denmark d_MTT_Agrifood_Research_Finland,_Plant_Production_Research,_Tietotie,_Jokioinen_FI-31600_Finland

e_Nordic_Seed_A/S,_Kornmarken_1,_Galten_DK-8464,_Denmark

f_Nordic_Genetic_Resource_Center,_Smedievägen_3,_Alnarp_SE-230_53,_Sweden

g_Section_for_Statistics_and_Data_Analysis,_Department_of_Applied_Mathematics_and_Computer_Science,_Technical_University_of_Denmark,_Richard_Petersens Plads,Kgs.LyngbyDK-2800,Denmark

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received8April2014 Receivedinrevisedform 27November2014 Accepted1December2014

Keywords:

Carbondioxide

Carbondioxideexploitation Climatechange

Combinedtreatment

Hordeumvulgare

Phenotypes

Productionparameters Ozone

Temperature

a

b

s

t

r

a

c

t

Theresponseinproductionparameterstoprojectedfuturelevelsoftemperature,atmosphericcarbon

dioxide([CO2]),andozone([O3])wasinvestigatedin138springbarleyaccessions.Thecomprehensiveset

oflandraces,cultivars,andbreeder-lines,wereduringtheirentirelifecycleexposedtoatwo-factor

treat-mentofcombinedelevatedtemperature(+5◦Cday/night)and[CO2](700ppm),aswellassingle-factor

treatmentsofelevatedtemperature(+5◦_C_day/night),_[CO₂_]₍₇₀₀_ppm),_and_[O₃_]_(100–150_ppb)._The

controltreatmentwasequivalenttopresentaverageSouthScandinavianclimate(temperature:19/12◦C

(day/night),[CO2]:385ppm).Overallgrainyieldwasfoundtodecrease29%inthetwo-factortreatment

withconcurrentelevationof[CO2]andtemperature,andthisresponsecouldnotbepredictedfromthe

resultsoftreatmentswithelevated[CO2]andtemperatureassinglefactors,wheregrainyieldincreased

16%anddecreased56%,respectively.Elevated[O3]wasfoundtodecreasegrainyieldby15%.Substantial

variationinresponsetotheappliedclimatetreatmentswasfoundbetweentheaccessions.Theresults

revealedlandraces,cultivars,andbreeder-lineswithphenotypesapplicableforbreedingtowardsstable

andhighyieldunderfutureclimateconditions.Further,wesuggestidentifyingresourcesforbreeding

undermultifactorclimateconditions,assingle-factortreatmentsdidnotaccuratelyforecasttheresponse,

whenfactorswerecombined.

1. Introduction

Climatechangealtersgrowthenvironmentsaroundtheworld andchallengesagriculturalproduction.Atthesametimetheworld

∗Correspondingauthor.Tel.:+4528511905;fax:+4545882258.

E-mail addresses: [email protected] (C.H. Ingvordsen), [email protected]

(G. Backes), [email protected] (M.F. Lyngkjær), pirjo.peltonen-sainio@mtt.ﬁ

(P.Peltonen-Sainio),[email protected](J.D.Jensen),marja.jalli@mtt.ﬁ(M.Jalli),

[email protected](A.Jahoor),[email protected](M.Rasmussen),

[email protected] (T.N. Mikkelsen), [email protected] (A. Stockmarr), [email protected]

(R.B.Jørgensen).

populationis growingwiththeneedof anincreased food pro-duction.Unprecedentedclimateconditionsarereportedtooccur around2047(+/−14years;Moraetal.,2013),andalreadybynow actuallevelsoftemperature,andatmosphericconcentrationofthe abundantgreenhousegassescarbondioxide([CO2];400ppm)and ozone([O3];32–62ppb)haveaffectedyieldsofcereals(Lobelland Field,2007;Lobelletal.,2011;Trnkaetal.,2012;Ellermannetal., 2013).Elevatedtemperaturehasbeenfoundtodecreasecropyield e.g.,byclosingofstomatathusavoidingtranspiration,butatthe sametimeinhibitingphotosynthesisandtherebydisrupting anthe-sisandgrainformation(Barnabásetal.,2008).Thenegativeeffectof elevatedtemperatureispossiblyreducedbyincreased[CO2]

boost-http://dx.doi.org/10.1016/j.eja.2014.12.003

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ingphotosynthesis(Longetal.,2006).Ozoneishighlyreactiveand canleadtoreactiveoxygenspeciesdetrimentaltothe photosyn-theticapparatus(FuhrerandBooker,2003).

By the end of the 21stcentury temperature is expected to increaseby3–5◦Caccordingtotheworst-casescenario(RCP8.5) ofIPCC(Collinsetal.,2013).The[CO2]istoreach1415–1910ppm and[O3]toincreaseby25%comparedtotheconcentrations expe-riencedtoday(32–62ppb).ThelatestassessmentreportofIPCC, workinggroup I,also consideredthree otherclimate scenarios withlowerincreaseintheanthropogenicemissionofgreenhouse gasesleadingtolesselevatedtemperature,however,arecentstudy suggeststhattheRCP8.5worst-casescenarioveryprobablyisthe onetoexpect(Sherwoodetal.,2014).Alongwithclimatechange followsincreasein frequencyof extremeeventssuchasﬂoods, heatwaves,droughts,andstormswithgreatriskofadditionalthreat tofutureagriculturalproduction(Collinsetal.,2013;IPCC,2014). Therapidchangesingrowthconditionsinducedbyalteredclimatic conditionsenhancetheneedtodevelopclimateresilientcultivars andapplynewmanagementpractices(Anwaretal.,2013).

Theannualgrowthrateoftheglobalagriculturalproduction wasonaverage2.1%from2003to2012,however,itisexpected todecreaseto1.5%peryearin thecomingdecades(OECD/FAO, 2013).Thelowergrowthrateisduetolimitedexpansionof agricul-turalland,risingproductioncosts,restricteduseofnon-renewable resourcestogetherwithreduceduseoffertilizer,andpestcontrol agentstolimittheirenvironmentalsideeffects(Foleyetal.,2011; OECD/FAO,2013).Plantbreedinghastheenormoustasktoincrease futureprimaryproduction.Inthiscontext,genebankmaterialand exoticaccessionscanpossesstraitstobeexploitedinthe devel-opmentofstableandhighyieldingclimateresilientcultivars.An obstacletotheuseoftheseresourcesisthelimitedinformation onclimatetoleranceofplantaccessions(Ceccarelliet al.,2010; Newtonetal.,2011).Alsothemethodicalcomplexityinthesearch fortolerancetoconditionsnotearlierexperiencedbyanycropis challenging.AsemphasizedbyPowelletal.(2012),theutilization ofgeneticresourceswithtolerancetoclimatefactorsisimpeded bylackofreliableandcostefﬁcientscreeningmethods.

Considerableknowledgeonclimatechangeeffectstocropsare stillneeded toplan bestbreedingstrategies tosecure the pro-duction.Forexamplethefollowingtwotopicshavereceivedlittle attention:Climatechangehasbeenfoundtoaffectvariouscrop speciesdifferently(e.g.,FengandKobayashi,2009;Kimball,1986; Luo,2011; Mills et al.,2007), however, theintraspeciﬁc varia-tion- betweenand withinaccessions- in responseto changes hasreceivedlittlefocus(e.g.,Craufurdetal.,2003;Pleijel,2011; WeigelandManderscheid,2012).Also,instudiesofclimatechange effectsoncropaccessions,ratherfewhaveinvestigatedtheeffects oftreatments,wheremorethanoneclimatefactorwaschanged (Alemayehuetal.,2014;Clausenetal.,2011;Frencketal.,2011; Juknysetal.,2011;Kasurinenetal.,2012;Mitchelletal.,1993;Zhou etal.,2011).

IntheNordiccountries,aroundhalfofthecultivatedarea(9 mil-lionha)isusedforgrowingcerealsandin2012barley(Hordeum vulgareL.)wasthemaincereal(FAOSTAT,2014).AlsointheEU barleyisanimportantcropcultivatedon21%ofthecerealcrop area(EuropeanUnion,2014).Thegrainsareusedformaltandfeed, however,theyieldisstagnating(FAOSTAT,2014).Undermidto highlatitudeconditionsatemperatureincreaseexceeding2◦Cis expectedtoreducecerealyields(IPCC,2014).TheNordic agricul-tureis furtherin riskofsummerdroughtand heavyrainswith changesinprecipitationpatternsleadingtodecreasedgrainyield (Christensenetal.,2011;Högyetal.,2013).

Inthisstudy,theeffectsofelevatedtemperatureandthemost abundantgreenhousegasses,CO2 andO3 wereanalyzedon138 springbarleyaccessions.Theclimatetreatmentswereappliedover theentirecroplifecycleassingle-andtwo-factor(elevated

tem-peratureand[CO2])treatments.Accessionswithphenotypesthat couldalleviateorinhibiteffectsoffutureclimatechangeongrain yieldandharveststabilitywereidentiﬁed.

2. Materialandmethods

2.1. Plantmaterial

The springbarley material tested consisted of48 landraces, 32oldcultivars(1883–1974),53moderncultivars(1978–2013), and 5breeder-lines. The majority ofthe accessionshad Nordic origin,viz.Denmark,Sweden,Norway,andFinland.Eightofthe moderncultivarsand22ofthelandraceshadnon-Nordicorigin (e.g.,Afghanistan,Belgium,Croatia,France,Germany)and8 acces-sions had unknown origin (AppendixA). Modern cultivars and breeder-linesweresuppliedbytheNordicbreedersinthenetwork ‘Sustainable primary production in a changing climate’ (Nord-Forsk)andafewcultivarswerefromtheBAR-OFproject(ICROFS, Denmark).AllotheraccessionsweresuppliedbytheNordicGenetic ResourceCenter(NordGen;http://www.nordgen.org/).

2.2. RERAF,technicaldescription

AllplantswerecultivatedintheRERAFphytotron(Risø Envi-ronmentalRiskAssessmentFacility)attheTechnicalUniversityof Denmark.RERAFhassixidenticalphysicallyseparatedgas-tight chambers(width6m,depth4mandheight3m).Thechambers hadindividualcontroloflight,temperature,humidity,andgasses (chamber atmospheres) and withcontinuous monitoring of all parameters.Airmixingwithinchamberswasensuredbytwowind turbines placed on opposite sides. Humiditywas generated by a humidiﬁer(HumiDisk65,Carel)placed infront of oneofthe windturbines.Thelightwassuppliedby28high-pressuremercury (1000Wor400W)and14halogen(250W)lampsperchamber.The lampscouldbeturnedonoroffindividually,whichwasusedto simulatesunriseandsunset.The[CO2]wassuppliedbyAirLiquide DenmarkA/Sandtheapplicationcontrolledaccordingtothe con-tinuousmeasurements.The[O3]inthechamberswassuppliedby UVPro550A(Crystalairproducts&services,Canada)generators, whichweremanuallyadjusted.FurtherdetailsonRERAFaregiven byAlemayehuetal.(2014)andFrencketal.(2011).

2.3. Growthconditions

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Table1

Setpoint-valuesandexperimentallevelsoftheabioticfactorsappliedinthetreatments.

Treatment Temperature,◦C(day/night) [CO2],ppm [O3],ppb Humidity,%(day/night)

Setpoint Experimental Setpoint Experimental Setpoint Experimental Setpoint Experimental

Ambient 19/12 18.9±1.2/11.8±0.8 385 448.5±81.1 0 1.4±1.4 55/70 55.7±2.5/69.9±1.5

+CO2 19/12 19.0±1.2/12.5±2.1 700 684.7±41.1 0 0.1±1.7 55/70 55.3±5.1/69.4±5.9

+tmp 24/17 23.9±1.4/16.8±0.8 385 448.4±74.4 0 1.9±1.2 55/70 55.9±2.8/69.8±1.6

+tmpandCO2 24/17 23.8±1.3/16.9±0.9 700 688.3±38.2 0 1.5±1.4 55/70 56.0±2.9/69.8±1.8

+O3 19/12 18.9±1.2/11.9±1.0 385 443.1±67.5 100–150ppb 121.1±32.8 55/70 55.7±2.4/69.8±1.7

theplantswererotatedweeklybothbetweenandwithinthe cham-bers.Inpractice,allchambersweresettoambientconditionsbefore rotation;whenambientconditionswerereached,theplantswere movedintoanewchamberandthecorrespondingtreatmentwas continued.Thesetpointsofthetreatmentswerereachedwithin 1h.Rotationwasomittedafter97days,asplantsweretootallto bemovedbetweenchamberswithoutdamagetotheplant mate-rial.Atanygiventime,thepositionsoftheaccessionswereidentical betweentreatments.

The treatments applied in RERAF consisted of four climate treatmentsandonecontroltreatment(Table1).Setpointsofthe ambientcontroltreatmentmimickedaveragepresentSouth Scan-dinavianclimateinthespringbarleygrowingseasonwith19/12◦C (day/night)and385ppm[CO2].Inthefourclimatetreatments fac-torswere manipulatedtothelevelsclosetothoseprojected at theendofthe21stcentury(correspondingtoascenario,where greenhousegasses are emittedin a “business as usual” magni-tude(∼RCP8.5)andconsistedofthreesingle-factortreatmentsand onetwo-factortreatment.Thethreesingle-factortreatmentswere: temperatureelevated+5◦C(day/night),elevated[CO2]at700ppm and[O3]targetedat100–150ppb.Inthetwo-factortreatmentthe elevatedlevelsoftemperatureand[CO2]werecombined.Ozone wasappliedabovetheprojectedaveragelevelsincebarleyhasbeen foundtopossesshighO3-tolerance(Millsetal.,2007).Besides,an [O3]at100–150ppbcanquiteoftenbefoundlocally,whereozone emissionsarehigh(Weietal.,2014).

2.4. Productionparametersanddatatreatment

Plantswereharvestedindividuallyatmaturityandthematerial fromalltreatmentswasdriedunderidenticalconditions(2months at20◦C,continuoushighairﬂow,55%relative humidity)before threshing.Theproduction parameters,grainyield,aboveground vegetativebiomass,andtotalnumberofearsweredeterminedfor theindividualplants.Harvestindex(grainyieldrelativetototal abovegroundbiomass)wascalculated.Numberofseedsperplant wasobtainedfromtheseedweightperplantdividedbytheweight ofanenumeratedsub-sampleof40grains.

Theexperimentalvaluesoftemperatureand[CO2]were mea-suredandtheirdeviationfromsetpointscalculated(Table1).From themeasured[O3]theaccumulatedozoneexposureovera thresh-oldof40ppb(AOT40)wascalculated accordingtoFuhreretal. (1997):

AOT40measured=imax(0,(Ci−40)) (1)

whereCiisthehourlymeanozoneconcentrationinppb aver-agedoverallhourlyvaluesmeasuredinthedaylighthours(inthis case16h)eachdayandforthecentral90daysofthedurationof theexperiment.

ToinvestigatepotentiallyadditivetreatmenteffectsofCO2and temperatureongrainyield(Table1),atwo-wayANOVAwith ran-domizedpoteffectwasapplied.Thepoteffectwasinvestigated throughmaximumlikelihoodestimation,whichconsidered poten-tialwithin-pot-competitioneffects.Themodelwascorrectedfor varyingyieldlevelsoftheindividualaccessionsthroughthe

addi-tionofasystematiceffect.Afterestablishingapositivewithin-pot correlation,theanalysiswascarriedoutwithstandardsoftwarefor mixedeffectsmodels.Theeffectofcultivar’syearofregistration(at theofﬁcialvarietylist)ongrainyieldwasinvestigatedsubjectedto thedifferenttreatments,throughaseriesofregressionmodelswith randomizedpoteffect.ABonferronicorrectionwasappliedtothe testevaluation.Boxplotswereestablishedonaveragedproduction parametersandsigniﬁcancegiventoambientaccordingtoT-test with***p<0.001;**p<0.01;*p<0.05.Allanalyseswerecarriedout usingthesoftwarepackageR,version3.10(RCoreTeam,2014).

2.5. Stabilityanalysis

Astaticyieldstabilityindexwascalculatedaccordingto envi-ronmentalvariance(S2_;_Roemer,₁₉₁₇_):

S2i=˙(Rij−mi)

2

(e₋1) (2)

where,Rijistheobservedyieldoftheaccessioniinthetreatmentj, m_iismeanyieldoftheaccessionacrosstreatments,andeisnumber ofenvironments.Adynamicyieldstabilityindexwascalculated accordingtoWricke’secovalence(W2_;_Wricke,₁₉₆₂_):

W2_i₌₍_R

ij−mi−mj+m)2 (3)

whereRijistheobservedyieldoftheaccessioniinthetreatment j,miismeanyieldoftheaccessionacrosstreatments,mjismean yieldacrosstreatmentjofallaccessionandmisthegrandmean, averageofallmi.Hence,W2statesthestabilitydependentonthe poolofaccessionsstudiedbytakingmeansofallaccessions(mj andm)intoaccount,whereasS2_is_a_function_of_only_the_speciﬁc accessioninquestion.

3. Results

3.1. Experimentalvalues

Theactualvaluesoftemperature,[O3]andhumiditywithinthe treatmentsintheRERAFphytotroncorrespondedtothesetpoints (Table1).Theexperimentallevelof[CO2]wasincreasedby15–16% comparedtothesetpointof385ppm,however,thehigher experi-mentalvaluesof[CO2]wereinagreementoveralltreatmentswith ambient[CO2].Theexperimental[O3]levelresultedinanAOT40 of113ppb/h.

Plantsinthetwo-factortreatmentweretheﬁrsttoreachZadoks growthstage99andwateringwasended104daysaftersowing.In thetreatmentofelevatedtemperaturewateringwasended114 daysaftersowing;intheambientandelevated[CO2]treatments wateringwasended117daysaftersowingandafter120daysin thetreatmentofelevated[O3].

3.2. Overalltreatmenteffects

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Fig.1.Visualcomparisonofspringbarleygrownunderambientconditionsandfourclimatetreatments.(a)Fromlefttorightwithblocksofthreecultivars(1:‘Lysimax’,2: ‘Paavo’,3:‘Linus’):elevated[CO2]andtemperatureincombination(tmpand[CO2]),ambient(amb),elevated[CO2]([CO2]),elevatedtemperature(tmp).(b)Fromleftambient

(amb)andelevated[O3]([O3])withblockofthreecultivars(4:‘Alf’,5:‘Fløya’,6:‘Åsa’).

heightandvigor.Inthetwo-factortreatmentwithcombined ele-vatedtemperatureand[CO2],plantheightandvigourwerevisually similartothoseoftheambienttreatment,butplantsfromthe com-binedtreatmentshowedincreaseddevelopmentalrate,asmaturity wasreachedearlier.Elevated[O3]causednovisualchangesinplant heightand vigour(Fig.1b), but occasionallybrownspots were observed.

Overallgrainyield(Fig.2a)wasstronglyaffectedbytheclimate treatmentsanddecreased28.9%underthetwo-factorclimate sce-narioofelevatedtemperatureand[CO2].Asforthesingle-factor treatments,elevatedtemperaturedecreasedoverallgrainyieldby 55.8%comparedtoambient,andelevated[CO2]increasedtheyield by16.1%.Elevated[O3]wasfoundtodecreasegrainyieldby14.9%, butnumberofgrainsdeclinedwithonly4.4%.Overallnumberof grainsfollowedthepatternofgrainyieldforthedifferent treat-ments,whereasnumberofearswasincreasedforalltreatments comparedtoambient(datanotshown).Overallaboveground

veg-grain yield (g)

tmpCO2 ***

CO2 ***

tmp*** O3 ***

−5

0

5

a

HI (%)

tmpCO₂***

CO2 tmp

*** _O

3 ***

−4

0

−2

00

2

0

40

b

Fig.2. Overallgrainyield(g/plant)a)andHI(%)b)of138springbarleyaccessions grownunderfourclimatetreatments;elevatedtemperatureand[CO2](tmpCO2),

elevated[CO2](CO2),elevatedtemperature(tmp)andelevated[O3](O3).Dashed

line:productionintheambientcontroltreatment(0).Circlesrepresenttheaverage ofoutlieraccessions.Medianindicatedinboldandwhiskersgivequartilegroup1 and4.Signiﬁcanceofthetreatmentstoambient,***p<0.001;**p<0.01;*p<0.05.

etativebiomasswasdecreasedunderelevatedtemperatureand increasedbyelevated[CO2],butnotaffectedbyelevated[O3]and thetwo-factortreatment.However,HIwasdecreasedbothunder elevated[O3]andthetwo-factortreatment(Fig.2b).Onlyinthe treatmentofelevated[CO2]wasoverallHIunaffected(Fig.2b).

Theappliedmodelrejectedanadditiveeffectofelevated[CO2] and temperature in theircombined treatment(p<0.0001), and foundapositiveinteraction,henceoverallgrainyielddecreased lessinthetwo-factortreatmentthancouldbeexpectedfromthe productioninthesingle-factortreatments.

Dividingtheaccessionsintogroupsofcultivarsandlandraces revealedthatthecultivar-groupproducedmoreearsinall treat-ments,exceptforthetwo-factortreatment(Table2).Inthe+5◦C treatmentthegroupofcultivarsproduced37.3%moreearsthanthe groupoflandraces.Anincreaseof11.5%wasfoundfromelevated [CO2]onoverallgrainyieldofthecultivar-group,butnoton above-groundvegetativebiomass,whencomparedtothelandrace-group. Nostatisticallysignificantcorrelationwasfoundbetweenthegrain yieldandtheyearofregistration(attheofficialvarietylist)of cul-tivarsanalysedoveralltreatments(Bonferroni-corrected,p=0.18). However,underelevated[CO2]aborderlinesignificance(p=0.46) wasfoundbetweenyearofregistrationandgrainyield.

Theclimateeffectongrainyield,numberofgrains,aboveground vegetativebiomassandnumberofearsisillustratedwithaheat mapforallaccessionsunderalltreatmentsinAppendixB.

3.3. Accessionspeciﬁceffects

Substantialvariationwasfoundintheresponseofthe acces-sions,withsomeoftheaccessionsreactingdifferently fromthe overalltrend,e.g.,withnoresponsetoelevated[CO2]orincreased grain yield under elevated [O3]. The deviant responses were demonstratedbothbylandracesandcultivars.

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Table2

Difference(%)betweenthegroupofcultivarstothegroupoflandracesforaveragedproductionvaluesunderambientconditions(ambient),elevated[CO2]andtemperaturein

combination(+tmpand[CO2]),elevated[CO2](+[CO2]),elevatedtemperature(+tmp)andelevatedozone(+[O3])assinglefactors.Negativevaluesindicatethattheproduction

ofthecultivargroupislessthanthatofthelandracegroup.

Ambient +tmpand[CO2] +[CO2] +tmp +[O3]

Noofears 19.7** 7.4 23.7*** 37.3*** 23.5***

Grainyield 4.0 2.9 11.5* 13.3 3.5

Abovegroundvegetativebiomass −5.0 −6.6 −3.0 9.5 −5.0

Noofgrains −4.8 −6.6 −2.5 4.5 −5.3

Signiﬁcances:***0.001;**0.01;*0.05.

Fig.3. Grainyieldrelativetoambientof138springbarleyaccessionscultivatedunderelevated[CO2]andtemperatureassingle-factorsandtheirtwo-factorcombination.

Filledblacksymbolsarecultivarsorbreeder-linesandgreyarelandraces.Selectednamesarestated;abbreviationsareColum.:Columbus;Everg.:Evergreen;Gun:Gunnar;

Gries.:Grieschische;Kush.:Kushteki;Mans.:Manschurei;Seb.:Sebastian.

Variationingrainyieldtoelevated[O3]wasfoundwithinthe groupoflandraces,oldandmoderncultivarsaswellas breeder-lines(Fig.4).Thegroupoflandracesapparentlyshowedthelargest

LR

av

era

g

e

g

rai

n

y

iel

d p

er

p

la

n

t (g

)

u

n

der e

le

v

at

ed [O

3

] rel

at

iv

e

to a

mb

ie

n

t

-6 -4 -2 0 2 4 6

old CV modern CV BL

Fig.4.Grainyieldrelativetoambient(0)of138springbarleyaccessionscultivated underelevated[O3].LR:landraces,oldCV:cultivarsfrom1883to1974,modernCV:

cultivarsfrom1978to2013andBL:breeder-lines.

variationin grainyieldrelative toambientunderelevated[O3]. TwooldcultivarsandaFinish landrace,‘Agneta’,‘JuliAbed’and ‘Ylenjoki’,increasedgrainyieldunderelevated[O3].

3.4. Trendsinstabilityofgrainyield

Amongthe40accessionswiththehighestaveragedmeangrain yield acrosstreatments (mi), both old and modern cultivars as wellaslandracesandabreeder-linewerefound(Table3).The40 accessionsrevealedverydifferentscoresforstaticenvironmental variance(S2₎_and_dynamic_Wricke’s_ecovalence₍_W2_)._In_the_set_of 138accessionsS2_for_grain_yield_spanned_from_0.58_to_16.79_and_W2 from0.27to33.60,wherelowvaluesindicatestabilityover envi-ronments(AppendixC).Thecultivar‘Sebastian’wasstaticstable andhighyielding,ranking11thforS2_and_4th_for_average_mean grainyieldacrosstreatments.Furthermore,‘Sebastian’ranked9th forgrainyieldrelativetoambientinthetwo-factortreatment.The lowestS2 _in_Table₃_,_was_found_for_‘Åsa’_(ranked_8th_of_the₁₃₈ accessions),however,miof‘Åsa’ranked40th.

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Table3

Environmentalvariance(Si2)andWricke’secovalence(Wi2)overtheambienttreatmentandfourclimatetreatmentsforthe40springbarleyaccessionswithhighestaveraged

meanyieldacrosstreatments(mi);rankgivenin().

Accessionname NGBno. Cultontype Yearofregistration mi Si2 Wi2

Agneta NGB1508 CV 1978 7.8 7.4 (113) 20.0 (134)

Jacinta NGB16665 CV 1999 7.7 16.8 (138) 33.6 (138)

Linus NGB13482 CV 1997 7.5 7.4 (112) 4.7 (72)

Sebastian CV 2002 7.4 1.4 (11) 4.3 (62)

Laurikka CV 2012 7.3 8.6 (122) 10.8 (116)

Paavo NGB13661 CV 1959 7.2 5.7 (90) 3.0 (40)

Griechische NGB9333 LR 7.1 5.1 (80) 4.4 (65)

Odin NGB16755 CV 1981 7.1 4.4 (65) 5.9 (90)

Stange NGB2109 CV 1978 7.1 7.4 (111) 3.7 (51)

Evergreen CV 2010 7.0 3.9 (52) 2.6 (37)

Columbus CV 2009 7.0 11.6 (132) 10.8 (115)

Brio NGB9327 CV 1924 7.0 6.1 (95) 5.8 (87)

Gaute NGB16732 CV 2000 7.0 6.3 (102) 2.2 (28)

Manschurei NGB9624 LR 7.0 12.0 (136) 13.5 (127)

Amalika CV 2012 6.9 4.9 (75) 5.6 (83)

Iron CV 2007 6.9 3.4 (42) 1.7 (19)

Alliot NGB16757 CV 1999 6.9 4.3 (63) 4.0 (54)

Szeged NGB9478 LR 6.8 4.3 (61) 4.8 (79)

Danpro NGB9659 CV 1969 6.8 11.6 (133) 9.3 (110)

Orthega CV 1997 6.8 11.2 (131) 11.0 (117)

Caruso NGB15059 CV 1991 6.8 3.9 (51) 0.9 (6)

Møyjar NGB2106 CV 1969 6.8 8.2 (116) 4.4 (63)

Brage CV 2010 6.7 6.5 (106) 4.7 (73)

Bjørne NGB9326 LR 6.6 6.8 (107) 3.6 (49)

Freja NGB1485 CV 1941 6.6 4.8 (72) 11.8 (120)

Hannuksela NGB325 LR 6.6 5.8 (92) 3.0 (42)

Prominant NGB15066 CV 1999 6.5 6.4 (104) 5.9 (88)

Bor09801 BL 6.5 2.8 (30) 13.9 (129)

Peruvian NGB8880 LR 6.5 3.4 (40) 1.7 (18)

Birka NGB4712 CV 1981 6.5 4.7 (69) 1.6 (15)

Kushteki NGB6288 LR 6.5 5.3 (83) 5.8 (86)

Sarkalahti NGB27 LR 6.4 9.9 (127) 7.5 (102)

Lysimax NGB15055 CV 1994 6.4 2.8 (28) 2.0 (25)

Trekker CV 2013 6.4 1.4 (12) 4.2 (59)

GrenobleI NGB9378 LR 6.4 4.2 (59) 1.5 (13)

Metz NGB9373 LR 6.3 2.0 (17) 8.5 (107)

Prestige NGB16750 CV 2000 6.3 3.7 (48) 1.6 (14)

Cicero NGB16756 CV 1999 6.3 8.0 (115) 4.5 (67)

Pavia NGB9501 LR 6.2 8.2 (119) 8.0 (104)

Åsa NGB4640 CV 1949 6.2 1.2 (8) 8.8 (108)

CV:cultivar;BL:breeder-line;LR:landrace.

staticstableaccordingtoS2 _but_with_low_mean_grain_yield_were e.g.,‘Moscou’,‘Calisi’,‘Oslo’,and‘SortGlatstakket’(AppendixC).

4. Discussion

Breeding cultivars, which can meet the increased demands forfoodandfeedinthefuture,isjeopardizedbythenumerous unknownsofclimatechangeandthelackingcharacterizationof accessionsundersuchconditions.Someoftheunknownsarethe speedofclimatechange,thefrequencyofextremeweatherevents andwhethersufﬁcientgeneticresourcesareavailable.Modeling studiesandselectionexperimentsindicatethatnaturallyoccurring microevolutionofcropsislikelytobeoverrunbyclimatechange (Alemayehuetal.,2014;RosenzweigandParry,1994;Svenning andSandel,2013).Withpossiblelittlehelpfrommicroevolution,it iscrucialtoidentifyaccessionsthatcanserveinbreedinghighand stableyieldingcultivarsunderclimatechangeconditions.

4.1. Climatechangeeffectsonthebarleyproduction

Published studieson cropproduction under climatechange fromenclosure,open-toporfree-aircarbonenriched(FACE) exper-iments often included only one or few cultivars. This study encompasseda setof138diversespringbarleyaccessions,and theoveralltrendsidentiﬁedinresponsetotheappliedfactorscan thereforebeconsideredrobustforspringbarley.

Thestrongly decreased grainyieldidentified under elevated temperature(Fig.2)issupportedbyearlierfindings(Alemayehu etal.,2014;Clausenetal.,2011;Högyetal.,2013).Mostlikely,the decreasedgrainyieldiscausedbyconcertedelevatedtemperature andwatershortageleadingtooxidativeandosmoticstress. Treat-mentsincludingelevatedtemperaturelikely experiencegreater vaporpressuredeficitandincreaseddemandforwateruptake pos-siblyleadingtodroughtstress(Barnabásetal.,2008;Powelletal., 2012).Additionally,inapotsetup,asinthepresentstudy,soil tem-peratureapproximatesairtemperature,whichfurtherincreased evaporationofsoilwater.

Theidentiﬁedpositiveresponseingrainyieldtoelevated[CO2] waslowerforthelargebarleysetof thisstudythanpreviously reported for fewer accessionsin enclosure studies (Alemayehu etal.,2014;Clausenetal.,2011;Kimball,1986),butinagreement withtheFACEstudyofWeigelandManderscheid(2012)onone cultivarofwinterbarleyinarotationsystem.Theseresults indi-catetheimportanceofanalyzingarepresentativesetofaccessions tobeabletoprovidesolid,generalresults.Thepositiveeffectof ele-vated[CO2]onprimaryphotosynthesisleadingtoincreasedgrain yieldiswellestablished(AinsworthandRogers,2007).

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sin-glefactorstemperatureand[CO2]werenotfoundadditiveintheir combinedtreatment,wearguethatresponseincomplex environ-mentscannoteasilybedepictedfromsinglefactor scenarios.In thepresentstudytheeffectsinthetwo-factorscenariowouldhave beenoverestimatedfromresultsofthesingle-factortreatments. Whensearchingforgeneticresourcesexploitableforproduction underfutureclimatescenarios,wherenumerousabioticfactorsare inplay,itmustbeconsidered,howtheresultsfromscreens per-formedundersingle-factortreatmentscanbeused.Itmighteven bequestioned,ifthetraditionalsetupoftestingfortoleranceto singlefactorsisworththeinvestment,whenresourcesforusein breedingistheaim.

Inthetreatmentsincludingconstantlyelevatedtemperatureas single-factororcombinedwithelevated[CO2],thetotalnumberof earsincreased,whereasnumberofgrainsdecreased.Theimpaired grainformationcanbecausedbyelevatedtemperature disturb-ingseveraldevelopmentalstepsthroughout thelifecycleofthe plant.Heatexposurepriortoanthesishaspreviouslybeenfound toreducethenumberoffloretsandsubsequentlythenumberof grains,whereasheatexposureatanthesisabortsthefloretsatthe primordialstage.Duringthegrainfillingstage,grainweightand alsosizeisdefined,andheatexposurehasbeenfoundtodecrease both(Rajalaetal.,2011; Ugarteetal.,2007).Tomaintaingrain yieldunderelevatedtemperaturebreedingforearlyheadingcould potentiallysecureasufficientperiodforgrainfilling,asitis sug-gestedinwheat(Tewoldeetal.,2006).

The138barleyaccessionswereexposedtoaconstantlyhigh [O3]duetopreviouslyreportedhighO3-toleranceinbarley,e.g., springbarleywasfoundtotoleratea25timeshigherdosethan wheat(Millsetal.,2007).Ourﬁndingsindicatearelativehigher sensitivityto[O3]thanreportedbyMillsetal.,2007however,it mustbekeptinmindthatnomeasurementshavebeenperformed onO3 takenupbytheaccessions.Ozonewasappliedconstantly, whichcanhavecausedacclimatisationwithnearlyclosedstomata andactivationofrepairmechanisms.

4.2. Productivityincultivarsandlandraces

Consideringthatbreedingfordecadeshasaimedatincreased grain yield, it is surprising that the group of cultivars only at elevated[CO2]producedahighergrainyieldthanthegroupof lan-draces.Ithasbeenhypothesizedthatenhancednet-photosynthesis to elevated [CO2] unconsciously has been targeted through breeding.Insupportofthishypothesisthegroupofcultivars out-performedthegroupoflandracesinregardtograinyieldunder increased[CO2]as singlefactor. Though,theeffectofincreased [CO2]wasnotfoundforabovegroundvegetativebiomass,whythe highergrainyieldinthecultivarsmightbefromimproved realloca-tionduringgrainfilling.However,inthecultivar-groupwefounda borderlinecorrelation(p=0.46)betweenyearofcultivar registra-tionattheofficialvarietylistandgrainyieldunderelevated[CO2] indicatingthatenhancednet-photosynthesistoelevated[CO2]has unconsciouslybeentargetedthroughbreedingorbyspontaneous yeartoyearadaptation.Thisfindingiscontrarytoresultsfrom previousstudiesofsixbarleycultivars(ManderscheidandWeigel, 1997)andfourwheatcultivars(Ziskaetal.,2004)whereno corre-lationwasfound.TheseauthorssuggestedCO2-responsivenesto havepotentialin breeding.We foundthata spontaneousoran unconsciousselectiontotherising[CO2]isalreadypresent, how-ever,itispossiblethatadditionalincreaseingrainyieldcouldbe achievedwithamoretargetedselectionofcultivarswithhighCO2 -resonsivenes.

Withregardtoamountofearsproduced,thegroupofcultivars consistentlyproducedmoreearsthanlandracesunderall single-factortreatments(Table2).Hence,thephysiologicalaptitudefor increasedgrainyieldincultivarsis present,butgrainyieldwas

only higher under elevated[CO2]. In thetwo-factor treatment, which wasthemostrealisticfutureclimatescenario,thegroup ofcultivars andgroupoflandracesproduced similaramountof ears.Therefore,itseemsequallymeaningfultosearchforgenetic resourcesforfutureenvironmentsamongoldaswellasmodern accessions.

4.3. Identiﬁcationofhighyieldingandstableaccessions

Theaccessionswithhighgrainyieldandstabilitywerefound amonglandracesaswellascultivars,andtheyoriginatedin dif-ferent countries indicating that suitable resources for climate resilienceareavailablefromdiversesources.TheDanishcultivar ‘Sebastian’hadhighgrainyieldbothunderelevatedtemperature andelevatedtemperatureincombinationwithelevated[CO2]as wellasitpossessedhighS2_for_grain_yield._This_is_in_agreement_with ‘Sebastian’presentlybeingusedinverydiverseclimatesspanning fromUkrainethroughsouth-westernEuropeandChile.Further, ‘Sebastian’hasthroughbreedinggivenrisetothesuccessfulcultivar ‘Quench’,whichalsodemonstratesbroadenvironmental adapta-tionandhighyield(R.Hjortshøj,SejetPlantBreeding,pers.comm.). Thecombinationofsuchhighstaticstabilityandhighyieldwasnot foundinotherofthetestedaccessionsundertheconditionsofthe presentexperiment,butmanyaccessionswithtraitspromisingfor highgrainyieldunderfutureclimateconditionswereidentiﬁed. Allofthemoderncultivars‘Alliot’,’Brage’,‘Fairytale’,‘Gunnar’,and ‘Jacinta’showedhighyieldunderthetwo-factortreatment possi-bleasaneffectofhighCO2-response(Fig.3).Thissuggeststhat breedingfor exploitation of increased[CO2] mighthave poten-tial.Thelandrace‘SortGlatstakket’washighyieldinginbothof thetreatments withelevated temperatureand therefore possi-bly holdingresources for improvement of heat and/ordrought tolerance.

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4.4. Challengesintheidentiﬁcationofplantresourcesforfuture climateconditions

Inalmostallcasesscreeningofplantaccessionsforresponseto futureclimateconditionshastobeperformedinmanipulated set-tings,andtheoutcomewillbearesultoftheappliedconditions.To whichextentresultsobtainedundermanipulatedconditionswill agreewithresultsfromﬁeldconditionswithnaturalroot develop-mentandplant–diseaseinteractionsisuncertain.Despitethelarge phytotronchambers(24m2₎_used_in_the_present_study,_the_authors acknowledgethattheenvironmentwithintheRERAFphytotron withconstanttemperature,noclouds,potsetupandlimitedbiotic stressisnon-natural.Also,resultsaregivenrelativetoanambient treatmentthatforsomeaccessionsmightbefarfromtheirnormal ambientenvironment.ExperimentsinFACEfacilitiesaremore nat-ural,however,themethodsforincreasingtemperaturee.g.,byroof orinfraredreﬂectancetechnologyhastothisdaynotproven capa-bleofelevatingtemperatureregimeswithmorethan2–3◦Corhas resultedinasymmetricwarming(e.g.,Bruhnetal.,2013;Kimball etal.,2008).

5. Conclusion

For thefirst time a comprehensive setof 138spring barley accessionshasbeencultivatedintheirentirelifecycleundera two-factorclimatescenarioofelevated[CO2]andtemperature.Further, staticanddynamicstabilityofgrainyieldoverthetwo-factor treat-ment,and threesingle-factor treatmentsaswellasanambient treatmentwerereported.Wefoundsubstantialvariationamong individualaccessionsunderallappliedtreatments.Aconsiderable decreasedgrainyield of29% inthetwo-factorclimatescenario wasfound, andamixedeffectsmodelconfirmedthatresultsin thiscombinedscenariocouldnotbepredictedfromresultsofits single-factortreatments.Thisfindingemphasizestheneedfor phe-notypingaccessionsunderrealisticmultifactorclimateconditions, assingle-factorexperimentsmightprovidelimitedoreven mis-leadinginformationtotheforecastingofeffects.Further,wehave identifiedpotentialgeneticresourceswithregardtoproduction performanceandstabilityunderfutureclimateconditions.These geneticresourcescouldandshouldbeexploitedinbreeding pro-grammes.

Acknowledgements

We thank the technical staff at DTU-KT, ECO-Risø for help throughoutcultivationandharvestprocedures.Aspecialthanksto ReneH.Petersenforthreshingthe5600individualplants.Thanksto AllanMurphyandEsbenHøjrupfortechnicalassistanceinRERAF. CathrineH.IngvordsenwasfundedbytheNordicCouncilof Minis-tersasamemberofthenetwork,‘Sustainableprimaryproduction inachangingclimate’.COBRA(CoreOrganicII)grantedfundingfor partsoftheexperiments.TheCO2usedinthisstudywasgenerously suppliedbyAirLiquideDenmarkA/S.

AppendixA. Supplementarydata

Supplementarydataassociatedwiththisarticlecanbefound,in theonlineversion,athttp://dx.doi.org/10.1016/j.eja.2014.12.003.

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