Avoiding lodging in irrigated spring wheat II Genetic variation of stem and root structural properties

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FieldCropsResearch196(2016)64–74

ContentslistsavailableatScienceDirect

Field

Crops

Research

j o ur na l h o me pa g e :w w w . e l s e v i e r . c o m / l o c a t e / f c r

Avoiding

lodging

in

irrigated

spring

wheat.

II. Genetic

variation

of

stem

and

root

structural

properties

F.J.

Pi ˜

nera-Chavez

a,b,∗

,

P.M.

Berry

c

_,

_M.J.

_Foulkes

a

_,

_G.

_Molero

b

_,

_M.P.

_Reynolds

b

a_Division_of_Plant_and_Crop_Sciences,_The_University_of_Nottingham,_Sutton_Bonington_Campus,_{Loughborough,}_{Leicestershire}_LE125RD,_UK

b_CIMMYT,_Int._Apdo._Postal_6-641,₀₆₆₀₀_Mexico,_DF,_Mexico

c_ADAS_High_Mowthorpe,_Malton,_North_Yorkshire_YO178BP,_UK

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received2February2016

Receivedinrevisedform4June2016 Accepted16June2016

Availableonline9July2016

Keywords: Lodging Springwheat Stemstrength Rootplatespread Plantheight

a

b

s

t

r

a

c

t

Lodging-relatedtraitswereevaluatedontheCIMMYTCorespringwheatGermplasmPanel(CIMCOG)in

theYaquiValleyofNorth-WestMexicoduringthreeseasons(2010–2013).Geneticvariationwas

signif-icantforallthelodging-relatedtraitsinthecross-yearanalysis,however,signiﬁcantG×Einteraction

duetorankchangesorchangesintheabsolutedifferencesbetweencultivarswereidentiﬁed.The

incon-sistencesoncultivarperformancesacrossseasonsparticularlyreducedtheheritabilityofkeycharacters

relatedtorootlodgingresistance(anchoragestrength).Targetcharactersrelatedtostemlodging

resis-tance(stemstrength)showedgoodheritabilityvaluesequalorabove0.70.Positivecorrelationsbetween

stemstrengthandstemdiameterandbetweenrootplatespreadandrootstrengthwerefound.

Select-ingforgreaterstemdiameterandwallwidth,greaterrootplatespreadandshorterplantheightcould

enablebreederstoincreaselodgingresistancebyincreasingstemstrength,rootstrengthanddecreasing

plantleverage,respectively.Achievingalodging-proofcropwilldependonﬁndingawiderrootplate

spreadandimplementingnewmanagementstrategies.Geneticlinkagesbetweenlodgingtraitswillnot

constrainthecombinationofthekeylodging-traitdimensionstoachievealodging-proofideotype.

How-ever,strongassociationbetweenstemstrengthandstemwallwidthwillincreasethetotalbiomasscost

neededforlodgingresistance.

license(http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction

Thepredictionofworldpopulationgrowthforthenextdecades entails an urgent need to adapt food crops to ensure global foodsupplydemandsinthefuture(Foulkesetal.,2011).Raising wheatproductivitywillbeafundamentalstrategytoachievethis (Reynoldsetal.,2012).Inthelastyears,breedingeffortshavebeen focussedonincreasingwheatproductionbyraisingyield poten-tial(Acrecheetal.,2008;FischerandEdmeades,2010;Slaferand Araus,2007).Substantialyieldincreaseswillrequireatwo-pronged approachcomposedby:i)increasingphotosyntheticcapacityand above-groundbiomass(Parryetal.,2011)andii)optimizingdry matterpartitioningtograinyieldwhilemaintaininglodging resis-tance(Foulkesetal.,2011).Lodging,thepermanentdisplacement ofstemsfromtheverticalposition,maylimityieldimprovement

∗ _{Corresponding}_author_at:_Division_of_Plant_and_Crop_Sciences,_The_University ofNottingham,SuttonBoningtonCampus,Loughborough,LeicestershireLE125RD, UK.

E-mailaddresses:[email protected],[email protected] (F.J.Pi ˜nera-Chavez).

bytworoutes:i)directlybyreducingphotosyntheticcapacitydue tochangesincanopyarchitecture(BerryandSpink,2012)andii) indirectlythroughbreedingbyincreasingtheamountofdry mat-terthatmustbepartitionedintosupportstructuresattheexpense of spike dry matter growth and yield when lodging resistance isincreased(Berryetal.,2007).Animprovedlodgingresistance achievedthroughcarefuloptimisationofbiomasspartitioningwill berequiredifgeneticgainsinyieldpotentialaretoberealized (Reynoldsetal.,2011).

Lodgingisacomplexphenomenoninfluencedbymanyfactors includingwind, rain,topography, soil type,previous crop, hus-bandry and disease.Thereare two maintypes of lodging;root lodgingcausedbyfailureoftheanchoragesystem,andstem lodg-ingcausedbybucklingofthestem.Conditionspromotingprolific growth,suchasanabundantsupplyofnutrientsand highseed rate, are also frequently associated with lodging (Berry et al., 2004).Irrigationofwheat(e.g.inMexico,India,andAustralia)can causesignificantlodgingastheapplicationofwaterreducesthe soilstrength,weakeningplantanchorage.InNorth-WestMexico (NWM)concurrenceofirrigationeventsandwindyconditionssoon afterorduringfloweringand inearlygrainfillingoftenoccurs.

http://dx.doi.org/10.1016/j.fcr.2016.06.007

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Avoidingthissituationisverydifficultduetotheunpredictable natureofweather (climatechangeincluded) orsimplybecause someirrigationeventsaredifficulttoavoid.Lodging canreduce grainyieldfrom7to80%(AcrecheandSlafer,2011;BerryandSpink, 2012;Eassonetal.,1993;FischerandStapper,1987;Stapperand Fischer,1990;Tripathietal.,2005;WeibelandPendleton,1964), andmayresultinreducedgrainquality,greaterdryingcosts,and slowerharvest(Berry,1998;Berryetal.,2004).Lodginglossesare greatestwhenlodgingoccurssoonafterfloweringandwhenthe angleofstemdisplacementfromtheverticalishigh(Berryand Spink,2012;FischerandStapper,1987)andcanbeasgreatasthose causedbypestanddisease(Pinthus,1974).Forinstance,ithasbeen reportedthatlodgingwithanangleof45◦wouldcauseagrainyield lossof18%(BerryandSpink,2012).Meanwhile,anangleof80◦from theverticalatanthesiswouldcauseagrainyieldlossintherange of7–35%(FischerandStapper,1987),43–61%(AcrecheandSlafer, 2011),and54%(BerryandSpink,2012).Consideringthelodging probleminthecontextofthe76000haofwheatharvestedinthe YaquiValleyinNWMeveryyearalone(SIAP,2016)theeconomic lossinaseverelodgingyearwouldbearoundUS$29million.Thisis assuming40%oftheareaaffectedwithyieldlossesaround50%and US$215pertonneofwheatgrain(Lanticanetal.,2016).Sucha per-centageofwheatareaaffectedwithlodginghasbeenobservedby CIMMYTresearchersinNWM(Tripathietal.,2005).Thepercentage ofyieldlosswouldbetheaverageoftheuppervaluesreportedby theaforementionedresearcherswhenlodgingangleisaround80◦. TheintroductionofdwarfinggenesduringtheGreenRevolution reducedthelodgingsusceptibility(Conway,1997)bydecreasing theleverageexertedonthestembaseandanchoragesystemvia reducingplantheight,whichallowedgreaterratesoffertilisation andthisleveragewasfurtherreducedwiththeuseofplantgrowth regulators (Berry et al., 2004;Crook and Ennos,1995; Pinthus, 1974;Tripathietal.,2004;WebsterandJackson,1993).However, thereissubstantialevidencethatindicatesaminimumplantheight requirementof 0.7mcompatible withhighyields (Allan,1986; BalyanandSingh,1994;Berryetal.,2015;Flinthametal.,1997; Kerteszetal.,1991;MirallesandSlafer,1995;Richards,1992).On theotherhand,importantwheatbreedingprogramssuchasthe onedevelopedbyCIMMYThaveincreasedplantheightofspring wheatcultivarsbyyearforreleasefrom1966(introductionof semi-dwarfcultivars)to2009from0.9to1.0m(Aisawietal.,2015).These observationsindicatethatexploitingplantheighttoreducelodging riskshouldnotbethemainstrategyinbreedingprograms.

Ifthereislimitedscopeforplantbreederstocounterthegreater lodgingriskcausedbyheavieryieldingvarietiesbyfurther short-eningplantsinsomecountries,thenitfollowsthatthebiophysical componentsthatsupporttheplant(stemandanchoragesystem) mustbestrengthened.Thepropertiesofthebiophysicalsupport structures have beenquantified for winter wheat (Berry et al., 2007)andspringwheat(Pi ñera-Chavezetal.,2016)usinga val-idatedmodelofwheatlodgingwhichevaluatestheinteractionof plant,soil(moisture)andwindcharacteristics(Berryetal.,2003b). Genetic variation of lodging-related traits, including stem and anchoragestrength(stemandanchoragefailuremoment)found forwinterwheatcropsgrowinginUKconditions(BerryandBerry, 2015;Berryetal.,2007,2003a),hasdemonstratedthatbreeding forthesecharactersisfeasibleandwillhelptowardsthe achieve-mentof a lodgingproofplantatleast fora period of25 years. Morerecently,Pi ñera-Chavezetal.(2016),havequantifiedthe bio-physicalstructuredimensionsrequiredforacroplodgingreturn periodof25yearsinspringwheatgrowninNWM.These require-mentsincludearootplatespreadof51mmandforthelowestbasal internode,astemstrengthof268Nmm,diameterof4.12–4.76mm, materialstrengthof35–50Mpaandwallwidthof0.65mmfora cropyielding6tha−1_,_with₅₀₀_shoots_m−2_,₂₀₀_plants_m−2 _and cropheightof0.7m.However,thepotentialforplantbreedersto

achievethesetargetsandwhetherthiswouldincuranytrade-offs withothertraitsaffectingyieldisunknown.Previousstudieshave reportedgeneticvariationforlength,diameter,wallwidth(Kelbert etal.,2004;Tripathietal.,2003)andstemstrength(Wiersmaetal., 2011)ofinternodesandshootheightatcentreofgravity(Tripathi etal.,2003)ofspringwheat.However,theseeffortshavenotbeen enoughtofullyunderstandthelodgingissueinspringwheat.For instance,Tripathietal.(2003)andKelbertetal.(2004)evaluated length,diameterandwallwidthofinternodesinNWMexicoand WesternCanada,respectively,butstemstrengthwasnotassessed; and Wiersma et al. (2011)evaluated stem strength in a single cultivar.Dimensionsforanchoragestrengthcharacterswereonly reportedforasinglecultivargrowingundergreenhouseconditions (Ennos,1991a,b).Fromtheaboveitcanbeconcludedthatmore researchshouldbedoneonthefullsetoflodging-relatedtraitson springwheat.

Theaimofthispaperwastoinvestigatethepotentialforplant breeders toimprove lodging resistance in spring wheatgrown in NWM under high yield potential conditions by: a) evaluat-ing thegeneticvariation and heritabilityof thelodging-related traits,particularly,thosestronglyrelatedtothestemand anchor-agestrength;b)assessingtheassociationsofstemandanchorage strengthtraitsandotherkeyphysiologicalcharacters;and,c) eval-uatingthepotentialofachievingalodging-proofideotypeableto resistlodgingduring25yearsdeﬁnedforspringwheatgrownin NWM.

2. Experimentalmethods

2.1. Plantmaterialandexperimentalconditions

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66 F.J.Pi˜nera-Chavezetal./FieldCropsResearch196(2016)64–74

width).Furtherplantpopulationtreatmentswereimposedafter plantemergenceonthelowestseedrate(75seedsm−2₎_treatment toincreasethecontrastbetweenplantdensitiesas:1)sixplants whichwerecompletelyisolatedineachplotwithina1.5m×2.4m areaoftheplot;2)plantpopulationontherestoftheplotwas thinnedto25plantm−2_._For_all_the_experiments_a_conventional agriculturalmanagementwasusedtoensurethecropwasnot defi-cientinwaterandnutrientsoraffectedbyweeds,pestsordiseases. Theirrigationscheduleincludedfivetosixfloodirrigationevents (includingoneatsowing)duringthecycleandthefertilizationwas 200kgha−1_of_N_(25%_before_sowing_and_75%_before_first_irrigation event)and50kgha−1_of_P_(before_sowing)._Plant_growth_regulators werenotappliedinanyoftheexperiments.Plantemergencedates (at50%ofplantsemerged)wererecordedat15ofDecember2010, 16ofDecember2011,02ofDecember2012and01ofDecember 2013forexperiments2011,2012,2013and2014,respectively.

2.2. Weatherconditions

Longtermmeanweatherconditionswereobtainedfromtwo weatherstations,thefirstwaslocatedatCENEB(1–2kmfromthe fieldtrials)whichcollectedallkeyweatherparameters,butonly spannedan18-yearperiodfrom1997to2014,thesecondweather stationwaslocated8–9kmfromthefieldtrialsandcollectedonly temperaturedata,butspanneda40-yearperiodfrom1973to2014. Datawereusedtocalculatethelong-termmeanand compared withdataperexperimentalyear(weatherstationatCENEB)forthe twomajorgrowthperiods:pre-anthesis(December–February)and grainfilling(March–April)(Table1).Meantemperaturesduringthe pre-anthesisperiodfor2011,2012and2013were2◦Ccolderthan theLTMatObregonairport(1973–2014)andsimilartoLTMfrom CENEB.Themeantemperatureduring2014wasinbetweenthe LTMsatObregonairportandCENEB.Solarradiationwassimilarin allcasesforbothgrowthperiods.Accumulatedrainfallwasabsent orverylowduringthewhole2011growingseason.Whilstrainfall wassimilaracross2012,2013and2014andLTMatCENEBforthe pre-anthesisperiod.Rainfallforthegrainfillingperiodofthe2014 seasonwashigherandsignificantlygreaterthantheotherseasons andtheLTMatCENEB.

2.3. Lodgingtraitsmeasurements

Plant measurements were made 20days after anthesis (GS65+20days)(Zadoksetal.,1974)on15plantsperplot dur-ing2011and10plantsperplotduring2012and2013.Theseplants wererandomlyselectedandextractedfromeachplot,avoidingthe outertworowsintheplotandplotborder.Plantextractionwas achievedbypullinguptheplantsafterexcavatingthesurrounding soilwithahandforktorecoverrootstoadepthof10cm.After,the soilwasremovedfromtherootsbypressurewashing. Measure-mentsassociatedwithlodgingresistanceincludedtherootplate spread(mm)andstructuralrootingdepth(mm)oftheplantroot systemandfertileshootnumberperplant.Theremaining mea-surementsweremadeonthemainstemandincludedtheheight totheeartip(mm),heightatcentreofgravity(mm)(withears attachedduring2012and2013andwithoutearsduring2011), nat-uralfrequency(Hz)forthewholeshootand,thediameter(mm), length(mm),wallwidth(mm),breakingstrength(Newtons)and dryweightforinternodes1and2(stembase)withoutleaf-sheath. Internode1wasdeterminedastheﬁrstinternodeofmorethan 10mmoriginatedjustorbelowthesoilsurface(superior intern-odesinthestemwerenumberedinascendingorderandidentifying theuppermostasthepeduncle).Thedetailedmethodsforthese measurementsaredescribedbyBerryetal.(2000)andhavebeen addedinthispaperassupplementarymaterial(TableS2). Intern-odedryweight(g)wasdeterminedbydryingtheinternodesuntil

nofurtherweightlossoccurredat75◦C.Rootdryweight(g)was determinedbytrimmingtherootsatthestembase,washingoff anyremainingsoilanddryingat75◦Cuntilnofurtherweightloss occurred.Measurementstakenonthe2014experiment usedin thispaperincludedonlyrootplatespreadatGS65+20.Natural lodgingforeachcultivarwasevaluatedintermsoftheangleof displacementofplantsfromtheverticalposition(0–90◦),andthe percentageoftheplotarealodged(0–100%).Thesemeasurements wererecordedonce ortwicea weekduringthelodgingperiod (betweentheﬁrstoccurrenceatearlygrainﬁllingandharvest)and usedtogeneratealodgingscore:

Lodgingscore ₌ (%ofplotarealodged)_×(angleoflodgingfromthe

vertical)/90(FischerandStapper,1987)

2.4. Agronomicandphysiologicaltraits

Agronomic and physiological traits measured for this study includedgrainyield(tha−1_),_harvest_index,_thousand_grain_weight (g),strawyield(tha−1_),_chaff_weight_(t_ha−1_),_ears_per_square_meter andheadingandanthesisdates(GS55and65intheZadoksscale, respectively)(Zadoksetal.,1974).Themethodsusedtocollectthe dataforthesetraitswereobtainedfromPasketal.(2012). Mea-surementstakenonthe2014experimentincludedonlygrainyield. Headingandanthesisdatewererecordedwhenmorethan50%of theplotwasattherespectivegrowthstages.Grainyieldwas esti-matedfromtheharvestedareawhichwasdeterminedavoiding bordereffects.Therestofthetraitswereestimatedfroma sub-sampleof100ear-bearingshootstakenfromtheharvestarea.

2.5. Calculatedlodgingparameters

Avalidated modelof lodgingfor winterwheat(Baker etal., 1998;Berryetal.,2003b)wasusedtocalculatethestemfailure moment(stemstrength),stemmaterialstrength,anchorage fail-uremoment(anchoragestrength),thewind-inducedbasebending moment(leverage)oftheshootandplant,andoverallrisktostem and root lodgingon spring wheat(stem and root failure wind speed).Details forthese calculations aregiven in a companion paperbyPi ˜nera-Chavezetal.(2016).

2.6. Statisticalanalysis

IndividualanalysisforeachexperimentwasdoneusingREML andperformedwiththeMIXEDprocedurefromSASInstituteInc. (2004)consideringthecultivarasﬁxedeffectand thereplicate andblockswithinreplicationsasrandomeffects.Combined anal-ysis acrossexperiments (cross-year) wasalso performed using REMLconsidering the effects of experiments, replicateswithin experimentsandgenotypebyenvironment(experiment) interac-tion(G×E)asrandomandgenotypeasﬁxed.Individualanalysis wasdoneaccordingtotheexperimentaldesignwhilecross-year analysiswas doneon27 cultivars (consistent cultivars in each experiment, see TableS1) under a randomised complete block design.Adjustedmeanswereestimatedforeachtraitby experi-mentfromindividualanalysesandcombiningdatafrom2011,2012 and2013experiments(cross-yearmean).Averagestandarderrorof difference(SED)betweencultivarmeansbyexperimentandcross yearmeanwascalculated.Broadsenseheritability(H2₎_was calcu-latedusingEq.(1)foranalysesforindividualexperimentsand2for analysescombinedacrossexperiments(Cooperetal.,1996).

H2₌ ␴2g ␴2

g+␴2e/nr

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Table1

Summaryofweatherconditionsduringpre-anthesisandgrainﬁllingperiodsforexperiments2011,2012and2013attheYaquiValley.

Parameter Growthperiod 2011 2012 2013 2014 LTMa _LTMb

Minimumtemperature(◦_C) Pre-anthesis 6.4 6.4 7.4 9.3 10.6 7.3 Grainfilling 10.2 10.1 9.8 11.4 13.7 9.7 Maximumtemperature(◦C) Pre-anthesis 25.0 25.6 24.1 26.4 25.0 25.1 Grainfilling 30.0 29.4 29.0 30.5 28.9 29.1 Meantemperature(◦_C) _Pre-anthesis _14.8 _15.0 _14.9 _16.7 _17.6 _15.3 Grainfilling 19.7 19.1 18.7 20.2 21.0 18.9 Meansolarradiation(MJm−2₎ Pre-anthesis 18.0 17.0 14.5 14.8 – 15.9 Grainfilling 26.9 24.9 21.6 21.4 – 24.1 Meanaccumulatedrainfall(mm) Pre-anthesis 0.4 14.0 12.9 20.9 – 22.2

Grainﬁlling 0.0 0.3 2.5 15.4 – 2.4

LTMa_,_long_term_mean_for_1973–2014_at_Obregon_Airport;_LTMb_,_long_term_mean_for_1997–2014_at_CENEB.

H2₌ ␴2g

␴2 g+

␴2 ge

ne +

␴2 e

nenr

(2)

where␴g2and␴e2arethegenotypic(cultivar)anderrorvariance,

␴ge2 is theG×E interaction.The number ofenvironments and

numberofreplicatesarerepresentedbyneandnr,respectively.

Phenotypiccorrelations(rp)betweentraitsweresimplePearson

correlations.Geneticcorrelationsamongtraits(rg)werecalculated

forcross-yearmeansusingtheequationfromCooperetal.(1996).

rg= g(jj) g(j)g(j)

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whereg(jj)isthearithmeticmeanofallpairwisegenotypic covari-ancesbetweentraitjandj’andg(j)g(j) isthearithmeticaverage of allpairwise geometricmeansamong the genotypic variance componentsofthetraits.Alltheanalyses,exceptforgenetic corre-lations,weredoneusingthesuiteMETA(MultiEnvironmentTrial Analysis)whichincludes33SASprogramstoanalysemulti- envi-ronmenttrials(Vargasetal.,2013).Geneticcorrelationsweredone usingasuiteofRcodes(META-R)foranalysingmulti-environment trials(Alvaradoetal.,2015).SASversion9.0andR3.2.1wereused torunthesuites.Experiment2014wasanalysedseparatelyusing aPROCMIXEDfromSASforasplitplotdesign.

3. Results

3.1. Variationoflodgingrelatedtraitsduetogeneticand

environmentaleffects

Analysis of variance showed consistent differences (P<0.01–0.001) betweencultivars for most of thetraits across allthreeexperiments.Anchoragestrengthandrootplatespread during2011andplantleverageduring2012weretheonlycases werenostatisticallysigniﬁcantcultivardifferencesweredetected. Reducingthenumberofcultivarsfrom60inthe2011experiment to30in2012and2013didnotaffectthestatisticalsigniﬁcance ofthecultivareffects.Theheightatcentreofgravityoftheshoot measuredin 2011wasless thanin2012and 2013becausethe earwasremovedinthe2011experimentbeforemeasuringthis trait.Thistraitwas,onaverage,60%oftheplantheightin2012 and2013,whileitwas44%ofplantheightin2011.Thecultivar range,expressedasthedifferencebetweentheproportionofthe grandmeanofthesmallestandlargestcultivar,wasgreatestfor anchorage strength, for which the values ranged from 1.39 in 2011to2.93in2012.Formaterialstrengththisproportionranged from0.93 in 2012to1.29in 2013and forplant leveragefrom 0.93in2013to1.25in2011.Thelowestproportionwasfoundfor internode diameter,root plate spread, structural rooting depth andplantheight.Theseproportionsrangedfrom0.30in2011to 0.35in2013forinternodediameter,0.28in2011to0.47in2012

forrootplatespread,0.34in2011to0.45in2012forstructural rootingdepthand0.50in2012to0.39 in2011forplantheight (Table2).

Cross-yearanalysisofdatafromthe27cultivarscommonacross theexperimentsin2011,2012and2013indicatedlargedifferences betweenthecultivars(G)(P<0.001)(Table3)consistentwiththe analysesoftheindividualexperiments(Table2).Environmental effects(E)werefound(P<0.05–0.001)formostofthetraits,except forshootand plantleverageand earnumberperplant.AG×E interaction(P<0.05–0.001)wasobservedforalltraits(Table3).

3.2. Broadsenseheritabilityoflodgingrelatedtraits

Broadsenseheritabilityforplant/shootleverageandstem/root strengthcharactersareillustratedinTable4.Heritabilityvalues estimatedfortraitsassociatedwithstemstrengthineach experi-mentranged0.60–0.86for2011,0.69–0.90for2012and0.74–0.94 for 2013. Despite the G×E interactions observed for all stem strengthtraits(Table3)highvaluesofheritabilityrangingfrom0.70 to0.94weredeterminedforthecross-yearanalysis,exceptfordry weightperunitlength(H2₌_0.38)_which_in_turn_caused_a_low heri-tabilityfordryweightperunitlengthperunitstrength(H2₌_0.33). Stemdiameterwasthemostconsistenttraitandshowedthe high-estheritability (0.93).Root characters related totheanchorage strengthhadthelowestheritabilityvalueswhencomparedwith therest of thecharacters (range0.19–0.61 for 2011,0.66–0.82 for 2012and0.62–0.82 for2013) and forthecross-year values (range0.11–0.48).Plantheighthadthehighestandmost consis-tentheritabilityrangingfrom0.95to0.96fortheindividualand crossyearanalysis.Similarly,traitsstronglyrelatedtoplantheight suchasnaturalfrequency(0.78–0.91)andheightatcentreof grav-ity(0.88–0.94)showedhighconsistentheritabilityvaluesforthe individualandcrossyearanalysis.Heritabilityfortheareaofthe mainshootearrangedfrom0.85–0.93betweenexperimentsand forthecross-yearanalysis.Earnumberperplanthadthelowest heritabilityranging from0.43 to0.56. Shootleverage heritabil-ity was consistent across years and for the combined analysis (H2₌_{0.72–0.92);}_plant_leverage_had_lower_heritability_{(0.36–0.74)} whichprobablyresultedfromthelowheritabilityofcomponent traitearnumberperplant.

3.3. Agronomicandphysiologicaltraits

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Table2

Summaryoftheindividualanalysisforstem(bottominternode1),rootandleveragecharactersassociatedtolodgingresistanceforspringwheatcultivarsgrownatNWM during2011,2012and2013.

Trait 2011a ₂₀₁₂b ₂₀₁₃c

Stem Mean Range SED Mean Range SED Mean Range SED

Diameter(mm) 4.21 3.60–4.87 0.157*** _3.94 _3.31–4.65 _0.165*** _3.74 _3.07–4.37 _0.150***

Wallwidth(mm) 0.80 0.67–1.25 0.059*** _0.86 _0.74–1.04 _0.051*** _0.72 _0.53–0.96 _0.065***

Strength(Nmm) 134 97.9–189 20.3** ₂₀₇ _147–289 _26.0*** ₂₀₆ _137–295 _20.5***

Materialstrength(MPa) 25.1 17.3–40.8 3.82*** _39.0 _28.9–65.2 _3.77*** _49.0 _27.2–90.3 _6.38***

Dryweightperlength(mgmm−1₎ _2.17 _1.54–2.91 _0.208*** _2.88 _2.38–3.56 _0.244** _3.21 _1.89–6.08 _0.373***

Dryweightperlengthperunitstrength(mgmm−1_/N_mm) _0.015 _{0.010–0.021} _0.0021*** _0.014 _{0.012–0.020} _0.0015*** _0.016 _{0.010–0.034} _0.002***

Stemfailurewindspeed(ms−1₎ _11.0 _9.06–16.1 _0.981*** _13.7 _11.6–17.9 _0.879*** _14.0 _11.1–17.6 _0.675***

Rootstrength

Rootplatespread(mm) 33.0 27.9–37.2 2.51ns _37.0 _28.5–45.8 _3.77** _44.3 _40.0–54.7 _2.67**

Structuralrootingdepth(mm) 36.8 31.0–43.4 2.21*** _38.6 _32.6–50.0 _2.55*** _38.9 _31.3–45.8 _1.97***

Rootdryweight(mgplant−1₎ ₃₇₂ _215–550 _78.3** ₃₂₇ _169–566 _74.8*** ₂₄₄ _151–366 _42.0**

Anchoragestrength(Nmm) 232 78.0–400 80ns ₂₆₂ _66.6–835 ₁₁₆*** ₃₉₇ _177–1133 ₁₃₀***

Anchoragefailurewindspeed(ms−1₎ _8.67 _4.63–12.6 _1.47** _8.59 _5.14–14.5 _1.75*** _11.5 _7.98–19.6 _1.39***

Leverage

Plantheight(mm) 1002 727–1120 25.0*** ₉₂₄ _730–1049 _21.5*** ₉₂₁ _716–1047 _19.5***

Heightatcentreofgravity(mm) 383 303–450 11.4*** ₅₆₅ _483–640 _12.2*** ₅₄₂ _446–602 _16.5***

Naturalfrequency(Hz) 1.28 0.97–2.21 0.115*** _1.48 _1.14–2.12 _0.095*** _1.68 _1.28–2.45 _0.130***

Earareaofmainshoot(cm2₎ _20.4 _10.8–27.4 _1.60*** _19.3 _12.8–25.3 _1.24*** _16.3 _10.6–22.1 _0.91***

Earnumberperplant 2.73 1.60–3.50 0.360* _2.69 _2.13–3.39 _0.290** _2.63 _1.97–3.07 _0.250***

Shootleverage(Nmm) 192 66.0–283 20.8*** ₁₈₉ _122–296 _28.6*** ₁₇₉ _89.1–279 _13.4***

Plantleverage(Nmm) 524 165–820 89.7*** ₅₀₆ _359–845 ₁₁₃ns ₄₆₉ _242–677 _63.3***

a₆₀_cultivars. b ₃₀_cultivars.

c ₃₀_cultivars.ns_not_{signiﬁcant.} * _P_<_0.05.

** _P_<_0.01. ***_P_<_0.001.

Table3

Summaryofthecross-yearanalysisforstem(bottominternode),rootandleveragecharactersassociatedtolodgingresistancefor27springwheatcultivars(G)grownat NWMduring2011,2012and2013(E).

Trait Mean Range SED(G) Pvalue(E) Pvalue(G×E)

Stem

Diameter(mm) 3.96 3.35–4.47 0.120*** <0.01 <0.05 Wallwidth(mm) 0.80 0.64–0.92 0.054*** <0.01 <0.01 Strength(Nmm) 184 134–252 20.5*** <0.01 <0.01 Materialstrength(MPa) 37.5 27.4–59.4 6.13*** <0.001 <0.001 Dryweightperlength(mgmm−1₎ _2.78 _1.95–3.85 _0.525*** _<0.01 _<0.001 DW/L/SS(mgmm−1_/N_mm) _0.016 _{0.013–0.023} _0.0025*** _<0.05 _<0.001 Stemfailurewindspeed(ms−1₎ _13.1 _10.8–15.7 _0.792*** _<0.01 _<0.001 Root

Rootplatespread(mm) 38.3 34.4–42.2 2.74*** <0.01 <0.01 Structuralrootingdepth(mm) 38.1 34.4–44.0 2.37*** <0.05 <0.001 Rootdryweight(mgplant−1₎ ₃₁₅ _213–437 _55.9*** _<0.05 _<0.01 Anchoragestrength(Nmm) 302 169–585 0.120*** <0.05 <0.001 Anchoragefailurewindspeed(ms−1₎ _9.84 _7.12–12.8 _1.68*** _<0.01 _<0.001 Leverage

Plantheight(mm) 938 726–1067 20.3*** <0.01 <0.01 Heightatcentreofgravity(mm) 492 410–543 10.9*** <0.001 <0.01 Naturalfrequency(Hz) 1.50 1.22–2.25 0.093*** <0.01 <0.01 Earareaofmainshoot(cm2₎ _18.4 _11.5–24.8 _1.05*** _<0.01 _<0.01 Earnumberperplant 2.65 2.06–3.07 0.227*** ns <0.01 Shootleverage(Nmm) 183 103–283 17.8*** ns <0.05 Planleverage(Nmm) 483 263–643 69.1*** ns <0.05

DW/L/SS,dryweightperunitlengthperunitstrength;***,P<0.001;ns,notsigniﬁcant.

andkeydevelopmentalstages(headingandanthesisdate)(range

0.72–0.98)(Table5).

3.4. Associationamongtraits

Associationsbetweenimportantagronomic,physiologicaland lodging traits for the 27 common cultivars in 2011–2013 are describedinTable6.Thecorrelationscausedbybothgeneticand environmentalfactorscombinedaregivenbyPearsoncorrelation coefﬁcients(upperdiagonal)(rp)forthecross-yearcultivarmeans and correlations caused by genetic factors alone are described bygeneticcorrelationcoefﬁcients(lowerdiagonal)(rg)obtained

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Table4

Broadsenseheritability(H2₎_for_stem_(bottom_internode),_root_and_leverage_characters_associated_to_lodging_resistance_for_spring_wheat_cultivars_grown_at_NWM_during

2011,2012and2013.

Trait 2011a ₂₀₁₂b ₂₀₁₃c _Cross-yeard

Stem

Diameter 0.86 0.87 0.91 0.93

Wallwidth 0.84 0.82 0.74 0.76

Strength 0.60 0.71 0.88 0.78

Materialstrength 0.72 0.90 0.90 0.72

Dryweightperlength 0.72 0.63 0.94 0.38

Dryweightperlengthperunitstrength 0.68 0.69 0.92 0.33

Stemfailurewindspeed 0.71 0.80 0.91 0.82

Root

Rootplatespread 0.19 0.66 0.62 0.11

Structuralrootingdepth 0.61 0.82 0.74 0.40

Rootdryweight 0.54 0.72 0.63 0.48

Anchoragestrength 0.25 0.81 0.76 0.17

Anchoragefailurewindspeed 0.56 0.78 0.82 0.38

Plantandshoot

Plantheight 0.95 0.96 0.96 0.96

Heightatcentreofgravity 0.92 0.94 0.88 0.94

Naturalfrequency 0.78 0.89 0.88 0.91

Earareaofmainshoot 0.85 0.89 0.93 0.92

Earnumberperplant 0.43 0.53 0.56 0.46

Shootleverage 0.85 0.72 0.92 0.87

Plantleverage 0.70 0.36 0.74 0.58

a₆₀_cultivars. b₃₀_cultivars. c ₃₀_cultivars. d ₂₇_cultivars.

Table5

Summaryofcross-yearanalysisofvarianceforagronomicandphysiologicaltraitsofspringwheatcultivars(G)grownatNWMduring2011,2012and2013experiments(E).

Trait Mean Range SED(G) Pvalue(E) Pvalue(G×E) H2

Grainyield(tha−1) 6.68 5.48–7.69 0.254*** <0.05 <0.01 0.82 Harvestindex 0.47 0.43–0.53 0.0088*** <0.01 ns 0.89 Thousandgrainweight(g) 42.8 31.2–51.6 1.12*** <0.05 ns 0.98 Strawyield(tha−1₎ _5.58 _4.77–6.32 _0.263*** _<0.01 _<0.05 _0.86 Chaff(tha−1₎ _1.88 _1.52–2.24 _0.111*** _<0.01 _ns _0.72 Headingdate(DAE) 83 73–93 1.61*** <0.01 <0.001 0.92 Athesisdate(DAE) 88 78–97 1.76*** <0.01 <0.001 0.91

Earm−2 ₃₀₃ _224–375 _15.5*** _ns _<_0.05 _0.93

Lodgingscore 2.28 0–15.7 – – – –

H2_,_broad_sense_{heritability;}_DAE,_days_after_emergence;_***,_P_<_0.001._ns,_not_{signiﬁcant.}

stem dry weightper unitlength withstem diameter(rp=0.27,

notsigniﬁcant;rg=0.48;P<0.05)andstemwallwidth(rp=0.59, rg=0.90;P<0.001)werealsofound.Stemstrengthandits

compo-nentswerealsoassociatedtograinyieldandyieldcomponentsand otherphysiologicaltraits.Forinstance,stemwallwidth,stem diam-eterandstemstrengthwereconsistentlyandnegativelyassociated withthousandgrainweightandearspermetersquared(rp=−0.49

to−0.79,rg=−0.53to−0.78;P<0.01–0.001).Thestrongest

asso-ciationwithgrainyieldwasfoundforstem diameter(rp=0.37, P=0.06; rg=0.41, P<0.05).There werenonegative correlations

betweenstemstrength traitsand grainyield.Material strength

wascorrelated tothedateatgrowthstagesheading(rp=−0.53, rg=−0.57;P<0.01)andanthesis(rp=−0.49,rg=−0.52;P<0.01).

Thisindicatedthatcultivarswithlaterheadingandanthesis devel-opedsmallermaterialstrength.

Anchorage strength was strongly and positively correlated

to its two components namely root plate spread (rp=0.88,

rg=0.88;P<0.001)andstructuralrootingdepth(rp=0.89,rg=0.95; P<0.001),asexpectedgivennatureoftheformularelating

anchor-age strength to its components. Surface root dry weight was

strongly and positivelyrelated toanchorage strength (rp=0.71, rg=0.91;P<0.001).Strongpositiveassociationswerealsofound

withintheanchoragestrengthcomponentsandrootdryweight

(rp=0.70–0.75,rg=0.77–0.94;P<0.001).Rootdryweightwas

posi-tivelycorrelatedtointernodediameter(rp=0.48,P<0.01;rg=0.71,

P<0.001),stemstrength(rp=0.33,ns;rg=0.44,P<0.05)anddry

weightperlength(rp=0.35,ns;rg=0.70,P<0.001)andnegatively

correlatedtointernodematerialstrength(rp=−0.36,ns;rg=−0.58, P<0.001).Additionally,anegativecorrelationbetweenrootplate spreadandstemwallwidth(rg=−0.44,P<0.01)andpositive

asso-ciationbetweenandanchoragestrengthwithstemdryweightper

unitlengthwerefound(rp=0.22,ns;rg=0.93,P<0.001).Genetic

correlation coefﬁcients alsoindicated a signiﬁcantand positive

associationbetween rootdry weight and grainyield, thousand

grainweightandharvestindex(rg=0.44to−0.50;P<0.05–0.01).

Insomecasesinvolvingroottraits,geneticcorrelationcoefﬁcients werenotcalculatedorsimplynoassociationwasidentiﬁeddueto geneticvariancecomponentvaluesequalorclosetozero.

Plantheightasamaincomponentoftheplantleveragewas neg-ativelycorrelatedwiththenaturalfrequency(rp=−0.65,rg=−0.70; P<0.001)andpositivelytotheheightatcentreofgravity(rp=0.85, rg=0.87;P<0.001). Plant height wasalso negatively correlated

tostemdryweightperunitlengthperunitstrength(rp=−0.48, P<0.05;rg=−0.85, P<0.001). Otheragronomic traits related to

plant height were thousand grain weight (rp=0.56, rg=0.58; P<0.01),harvestindex(rp=−0.41,rg=−0.44;P<0.05)andlodging

score(rp=0.30,notsigniﬁcant;rg=0.85;P<0.001).

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Table6

Phenotypic(upperdiagonal)andgenetic(lowerdiagonal)correlationsbetweencross-yearmeansoflodging,agronomicandphysiologicaltraitsof27springwheatcultivarsgrowingatNWMduring2011,2012and2013.

Traits 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22

1.Grainyield 0.41 −0.12 0.15 −0.25 0.04 −0.09 −0.10 0.19 −0.19 0.37 0.24 0.18 0.11 −0.32 0.14 −0.22 0.02 0.05 0.33 0.58 0.01 2.Naturalfrequency 0.50 −0.65 0.23 −0.81 −0.40 −0.12 −0.17 0.14 −0.31 0.18 −0.06 0.20 0.42 −0.37 −0.11 −0.16 0.20 0.25 −0.07 0.36 0.27 3.Plantheight −0.16 −0.70 0.08 0.85 0.27 −0.06 −0.05 −0.09 0.30 0.33 0.12 −0.09 −0.48 0.00 0.33 −0.04 −0.29 −0.25 0.56 −0.41 −0.34 4.Earperplant 0.21 0.43 0.11 −0.25 −0.35 −0.32 −0.58 −0.39 0.11 −0.09 −0.23 −0.25 −0.16 0.04 −0.16 −0.46 −0.50 −0.45 0.23 0.23 0.40 5.Centreofgravity −0.31 −0.87 0.87 −0.42 0.40 0.17 0.28 0.08 0.27 0.10 0.17 −0.06 −0.38 0.20 0.27 0.28 −0.09 −0.10 0.34 −0.44 −0.42 6.Eararea 0.02 −0.42 0.27 −0.57 0.42 0.53 0.48 0.51 0.04 0.37 0.61 0.28 −0.35 −0.07 0.56 0.56 0.01 −0.02 0.54 0.07 −0.82 7.Rootplatespread 0.04 −0.11 −0.12 na 0.61 na 0.79 0.70 −0.14 0.23 0.09 0.23 0.08 −0.20 0.14 0.88 0.23 0.19 0.07 0.15 −0.49 8.Structuralrootdepth −0.06 −0.24 0.00 na 0.55 0.76 0.90 0.75 0.03 0.13 0.07 0.28 0.25 −0.14 0.09 0.89 0.36 0.32 0.00 0.07 −0.48 9.Rootdryweight 0.50 0.29 −0.07 na 0.13 0.77 0.94 0.77 −0.04 0.48 0.30 0.35 0.08 −0.36 0.33 0.71 0.32 0.31 0.31 0.28 −0.65 10.Lodgingscore 0.00 −0.79 0.85 0.41 0.90 0.05 na −0.09 −0.22 0.06 −0.08 −0.05 −0.13 0.04 0.07 −0.04 0.02 0.05 0.14 −0.15 −0.10 11.Stemdiameter 0.41 0.21 0.34 −0.20 0.12 0.35 0.35 0.09 0.71 0.08 0.31 0.27 −0.14 −0.75 0.44 0.15 0.20 0.26 0.59 0.10 −0.51 12.Stemwallwidth 0.37 −0.02 0.16 −0.56 0.21 0.69 −0.44 −0.21 0.23 −0.43 0.32 0.59 −0.28 0.19 0.84 0.14 −0.08 −0.08 0.49 −0.02 −0.64 13.SDWL 0.54 0.51 −0.17 −0.48 −0.12 0.38 Na Na 0.70 −0.54 0.48 0.90 0.45 0.13 0.61 0.22 −0.21 −0.20 0.28 0.19 −0.43 14.SDWLSS 0.30 0.89 −0.85 −0.37 −0.65 −0.65 0.89 0.95 0.18 −0.39 −0.15 −0.67 −0.18 −0.13 −0.41 0.07 0.16 0.14 −0.41 0.26 0.32 15.Stemmaterialstrength −0.36 −0.38 −0.01 0.30 0.22 −0.08 −0.33 0.04 −0.58 0.11 −0.86 0.30 −0.11 −0.34 0.21 −0.12 −0.49 −0.53 −0.16 −0.16 0.08 16.Stemstrength 0.24 −0.10 0.37 −0.26 0.30 0.59 0.07 0.11 0.44 −0.21 0.46 0.97 0.78 −0.71 0.12 0.16 −0.29 −0.25 0.65 −0.04 −0.72 17.Anchoragestrength −0.34 −0.18 −0.01 na 0.72 na 0.88 0.95 0.91 −0.72 0.09 −0.19 0.93 0.55 0.04 0.22 0.38 0.33 0.02 −0.03 −0.52 18.Anthesisdate 0.00 0.20 −0.32 −0.87 −0.10 0.02 0.69 0.56 0.56 0.19 0.22 −0.09 −0.27 0.24 −0.52 −0.25 0.80 0.99 −0.43 −0.26 0.08 19.Headingdate 0.02 0.25 −0.29 −0.77 −0.11 −0.02 0.60 0.48 0.56 0.22 0.28 −0.06 −0.25 0.20 −0.57 −0.22 0.71 1.00 −0.38 −0.28 0.08 20.Thousandgrainweight 0.37 −0.05 0.58 0.39 0.36 0.57 0.21 0.02 0.48 0.40 0.62 0.56 0.49 −0.72 −0.20 0.76 0.10 −0.43 −0.39 0.18 −0.67 21.Harvestindex 0.62 0.42 −0.44 0.35 −0.47 0.05 0.35 0.07 0.44 −0.48 0.08 −0.03 0.30 0.38 −0.10 −0.01 −0.19 −0.32 −0.33 0.19 −0.10 22.Earm−2 ₋_0.06 _0.31 ₋_0.36 _0.57 _−0.46 _−0.88 _na _−0.70 _−0.97 _0.01 _−0.53 _−0.73 _−0.74 _0.46 _0.14 _−0.79 _na _0.05 _0.06 _−0.70 ₋_0.12

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Table7

Analysisofvarianceforrootplatespreadandgrainyieldunderdifferentseedrates (SD)forasubsetofﬁvecultivars(G)fromCIMCOGpanelgrownatNWMduring 2014.

Seedrate Rootplatespread(mm) Grainyield(tha−1₎

Isolatedplants 102.3 – 25seedm−2 _68.7 _6.33 125seedm−2 _48.4 _6.21 175seedm−2 49.2 6.40

SED(SD) 2.65*** _0.173_ns

SED(G) 2.20*** _0.135***

SED(interaction) 4.74*** _0.297_ns

ns,notsigniﬁcant.

***_P_<_0.001.

of0.54(P<0.01)betweengrainyieldandstemdryweightperunit lengthwasfound.Nosigniﬁcantassociationwasfoundforgrain yieldandlodgingscore.Harvestindexwascorrelatedpositivelyto naturalfrequency(rp=0.36;P=0.07,rg=0.42;P<0.05),and neg-ativelycorrelated to theheightat centre of gravity (rp=−0.44,

rg=−0.47;P<0.05)andlodgingscore(rp=−0.15,notsigniﬁcant;

rg=0.48;P<0.05).

Insummary,itcanbeconfirmedthatstemstrengthwas asso-ciatedpositivelywithitsmaincomponents(stemdiameterand stemwallwidth),exceptforstemmaterialstrengthwereno asso-ciationwasfound.Alsowasconfirmedthatthestemstrengthitis tightlyassociatedwiththespecificweightofthetruestem(stem dryweightperunitlength).Ontheotherhand,anchoragestrength, rootplatespread,structuralrootingdepthandrootdryweightwere positivelyinterrelated.Plantheightcorrelatednegativelywith nat-uralfrequencyandpositivelywithcentreofgravityandgrainyield wasassociatedpositivelywithstemdiameter,naturalfrequency androotdryweight.

3.5. Seedrateeffectonrootplatespreadandgrainyield

Asummaryofthestatisticalanalysisperformedonrootplate spreadandgrainyielddatafrom2014experimentindicatedgenetic differencesforbothtraits.Alsorootplatespreaddifferedbetween seedratesandtherewasaninteractionbetweenseedrateand cul-tivar(P<0.001).Theseresultsshowedthatrootplatespreadcould beincreasedfrom49.2mmto68.7mmbyreducingseedratefrom 175to25m−2_without_reducing_grain_yield₍_Table₇_)._{Interestingly} therewasnointeractionbetweenseedrateandgrainyield.

4. Discussion

4.1. Breedingalodging-proofplant

Pi ˜nera-Chavezet al. (2016) estimatedthat for spring wheat yielding6tha−1 _with₅₀₀_shoot_m−2 _and₂₀₀_plants_m−2_grown intheNWMenvironmentalodgingreturnperiodof25yearswill requireamaximumheightof0.7m,aminimumrootplatespread of51mmandaminimumstemstrengthforthebottominternode of268Nmm.Thetargetstemstrengthcouldbeachievedwitha diameterof4.76mmdiameter,andamaterialstrengthof35MPa, orwithadiameterof4.12mmandamaterialstrengthof50MPa, eachwithamaximumwallwidthof0.65mm.Therationalefor havingathininternodewallwidthwastominimisebiomasscost toincrease stem strength based onengineering principles.The cross-yearcultivaranalysisdemonstratedthatnotallofthetarget traits couldpresentlybe achievedby a singlecultivar. Individ-ualtargettraitsthatcouldbeachievedincludedstemdiameter andmaterial strength.Minimumwallwidthobserved inspring

wheatwas0.64mmwhichwasbelowofthemaximum require-mentof0.65mm.MaximumstemstrengthfoundinCIMCOGpanel (252Nmm)was6%belowthetargetrequirement(268Nmm).Root platespreadwasnotachievedbyanyoftheCIMCOGpanelcultivars investigated,withamaximumvalueobservedof42mmwhichwas 17%lessthantherequirementof51mm.Aminimumplantheight of0.73mwasobservedintheCIMCOGpanelwhichwas4%above therequirement(0.70m)(Table8).Coincidentally,thebestvalues observedinwinterwheatcultivarswerealsolowerthanthetarget stemstrengthandrootplatespreadandwithgreaterplantheight thantheestimatedlodgingproofwinterwheatinaUKenvironment (Berryetal.,2007).

Itisimportanttohighlightthatthegeneticrangeforkey lodg-ingtraitsfoundinthisstudyhasimportantimplicationsforlodging risk.Ifthecultivarmeanvaluesofkeycroppropertiesestimatedare usedtocalculatelodgingrisk(intermsoffailurewindspeed),an averagewheatcropforNWMwillhaveastemfailurewindspeed of12.8ms−1_and_anchorage_failure_wind_speed_of_8.5_m_s−1_._This_is farbelowoftheideotyperequirementof22ms−1_and₁₈_m_s−1_to resiststemandrootlodgingforaperiodof25years,respectively.In thiscontext,ifwedecreaseplantheighttotheminimumwhichwas 0.7m,stemandanchoragefailurewindspeedswillbeincreased about1ms−1_._On_the_other_hand,_if_stem_strength_is_increased_to themaximumwhichwas252Nmm,stemfailurewindspeedswill beincreasedabout2ms−1_._Greater_effect_of_about₆_m_s−1_can_be obtainedifanchoragestrengthisincreasedtothemaximumwhich was585Nmm.Thisreinforcetheideathatgeneticrangesfor sev-eralkeylodgingtraitscansubstantiallyaffectlodgingrisk(Berry andBerry,2015).Moreover,acombinationofthesetraitsinasingle cultivarcangivegreaterpositiveeffectsforlodgingresistance.

Correlations betweenlodgingand agronomic traits are rele-vant to inform breederson strategies toimprove resistance to both stem and root lodging, whilstalso increasing grainyield. For instance, spring wheat has showedsignificant associations betweenstem strengthand stem wallwidthand diameterand apositiveweakbutnotsignificantassociationbetweendiameter andwallwidth(Table6).Nosignificantrelationshipwasfoundfor stemstrengthandstemmaterialstrength.Maximisingstem diam-eterandminimizingstemwallwidthwillresultinlessinvestment of biomasstoincreasestem strength(Berryet al.,2007). How-ever,ourresultshavedemonstratedastronglinkagebetweenstem wallwidthandstemstrengthwhichwillbedifficulttobreak.It appearsthenthatthickerwalledstemsshouldbeconsideredfor springwheat.Forexample,toobtainthetargetedstemstrength (268Nmm)withthemaximumstemwalldimensionobservedin springwheatof0.92mm,astemdiameterof3.89mmwitha mate-rialstrengthof50MPawillberequired.Athickerstemwallwill increasethebiomassperunitstrength(Berryetal.,2007)which inturnwilldemandmorebiomassinvestmentforsupport struc-tures.Thisadditionalbiomassinvestmentinthestemmaycompete forresourceswithspikedrymattergrowthandyield determina-tion.However,thismaybeanacceptablecompromiseifitmakes breedingforstrongstemseasierandquicker.

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Table8

Ideotypetargets,geneticrangeandbestcultivarforthekeylodgingtraitsofspringwheat(CIMCOGpanel).Valuesrepresentthemeansof27cultivarsfrom2011to2013.

Trait Ideotypetarget* _Genetic_range _Best_observed_value

Stemdiameter(mm) 4.12–6.03 3.35−4.47 4.47(cv.60)

Stemwallwidth(mm) 0.65 0.64−0.92 0.64(cv.37)

Stemstrength(Nmm) 268 134−252 252(cv.23)

Stemmaterialstrength(MPa) 20−50 27.4−59.4 59.4(cv.45)

Rootplatespread(mm) 51 34−42 42(cv.16)

Height(m) 0.70 0.73−1.07 0.73(cv.9)

* _Lodging_probability_of₁_in₂₅_years,₂₀₀_plants_m−2_,₅₀₀_shoots_m−2_and_grain_yield_of₆_t_ha−1_.

4.2. Heritability

Thisstudyhasobservedlargegeneticvariationinspringwheat forthemajorityofthetraitsinvolvedinthestemstrength, anchor-agestrength,leverageofthestembaseandstructuralbiomassfor plantsupport.Apartfromrootplatespread, anchoragestrength andplantleveragethisvariationhasbeenconsistentforthe individ-ualandcross-experimentanalysisofvariance.Experimentalmeans differedinallcases,exceptforearnumberperplantandshootand plantleverage.Lodging-traitshavebeenreportedtoshowG×E interactionsinwinterwheat(BerryandBerry,2015;Berryetal., 2003a)andourstudyhasconfirmedthesamefindingforspring wheat.Breedingforthesetraitsmaythereforeneedselectionin multipleenvironments.Additionally,repeatabilityofcultivar per-formanceacrossexperimentswillbeaninterestingparameterto checksinceG×Edecreasesbothheritabilityandresponseto selec-tion(Cooperetal.,1996).Thekeytraitsforstemstrength(stem diameter,wallwidthandmaterial strength)and plantleverage (plantheight)haveheritabilityvaluesequalorabove0.70,which make themuseful forbreeding selection.However,for anchor-agestrengthcharacterssuchasrootplatespread andstructural rootingdepthcross-yearheritabilityvalues were0.11and 0.40, respectively.Thus,responsetoselectionwillbemoredifficultfor anchoragecharacters.Intheliteratureitisreportedthatlodging charactersarehighlyheritablewithvaluesintherangeof0.73–0.93 (Berryetal.,2007).Nevertheless,BerryandBerry,(2015)indicated alowerrangefrom0.17–0.90withthelowestvaluesforroot lodg-ingcharacters.(Kelleretal.,1999)indicatedheritabilityvaluesin therangeof0.51–0.93fortraitssuchasstemdryweightperlength, stemdiameter,stemwallwidthandnaturalfrequency,although, exceptforstemdryweightperlength,theirtraitassessmentwas usingscorenumbersratherthanactuallymeasuringthetraits.

4.3. Implicationsforselectionofimprovedlodgingresistant cultivars

Theinvestmentofadditionalstructuralbiomassinroots and stems required for greater lodging resistance has been fully explainedbyBerryetal.(2007)andPi ˜nera-Chavezetal.(2016) and is oneof the challenges of improvedlodgingresistance in wheat.Thestrongpositivecorrelationsbetweenstemdryweight perunitlengthandstemstrength,androotplatespreadwithroot surfacebiomassindicatedinTable6supportsthispremise. How-ever,evenwithgreaterbiomass,carefuloptimizationofyieldand lodgingtraitswillberequiredtominimizetheinevitable trade-offsbetweengrainyield-formationtraitsandlodging-relatedtraits thatdevelopatthesametime.Thestronggeneticlinkagefound betweenstemstrengthandstemwallwidthislikelyto compro-misethestrategyofminimisingthebiomassinvestedinthestem bybreedingforwidethinwalledstems,aswasdonebyBerryetal. (2007).Acomparisonbetweenthinwalledstemswitha dimen-sionof0.65mmandthickwalledstemswith0.92mm(maximum dimensionobservedinthecross-yeargeneticrange)hasindicated thatstembiomassinvestmentinsupportstructureswouldincrease byapproximately1.0tha−1_with_thicker_walled_stems.

Reducingplantheighttoa0.7mmightdecreaseoverallstem biomassandthestoragecapacityofstems.Thiswillrepresenta trade-offforyieldiflodging-resistantideotypeisachieved. Nev-ertheless,tocounteractthissituationothertraitssuchasfruiting efﬁciency(i.e.thenumberofgrainssetperunitofspikedryweight at anthesis)can beimproved. Improvingfruiting efﬁciency has beenproposedasoneofthestrategiestoraisegrainyieldthrough increasinggrainnumber per unit areain cultivars that already reachedtheoptimumheight(0.7–1.0m)(Slaferetal.,2015).

Findinggermplasmwiththerootplatespreadtargetdimension willbedifficultbasedontheknowngeneticrangesofwinterand springwheat.Lowrepeatabilitywilllimittheresponsefor selec-tionofimprovedlodgingresistanceofthistrait.Rootdryweight mayplayanimportantroleforanchoragestrengthimprovements anditwasfoundtobemoreheritable.Possiblestrategiestofind material withthetarget dimensionwill include screeningnew germplasmorevenwildrelativesandimprovingthistraitby man-agement.Forinstance,reducingtheplantpopulationincreasesroot lodgingresistance(Berryetal.,2007,2004)byincreasing anchor-agestrength (Berry etal.,2000).Presentresultsfromthe2014 experimenthavealsoindicatedthatrootplatespreaddimensions identified at 213–292 seedsm−2 _(experiments_2011,₂₀₁₂ _and 2013)couldbeenhancedbyreducingseedratewhilemaintaining highgrainyields(Table7).Additionally,plantsarranged equidis-tantlyorwithvariationsintheplantarrangementunderthesame seedratecouldbefurtherinvestigatedforeffectsonroot anchor-age.Eassonetal.(1993)indicatedthatplotswithseedratesinthe rangeof50–100seedsm−2 _yielded₁₀_t_ha−1_in_Northern_Ireland whichisahighyieldperformance.Similarly,ourresultshave indi-catedthatwithlowseedrates,highyieldscanbeobtainedinNWM. Tilleringcouldexplainthisgrainyieldsinceallcultivarsusedfor 2014experimentrespondedbycompensatingforthelowplant populationwithmorefertiletillers.Fertileshootsperplantat har-vestrangedfrom9.5to12.5and2.9to4.1for25and175seeds m−2_,_{respectively.}_This _response_of _tillering _to_low _plant popu-lationfromall2014cultivars canalsoexplainthelack ofG×E interactionbetweenseedrateandgrainyield.Whaleyetal.(2000) statedthatcropsgrownatlowdensitiesincreasedgreenareaper plantwithalongertilleringperiodandconcludedthatgrainyield ismaintainedevenwithlargereductionsinplantdensity.More recently,Aisawi(2011)indicatednodifferencesingrainyieldfor seedratesat50,150and450seedsm−2_for_experiments_under NWMgrowingconditions.Thisdemonstratesthegreatpotentialfor improvinganchoragestrengthbyestablishinglowerplant popula-tionswithoutaffectinggrainyield,assumingarelativelyuniform standestablishmentcanbeachievedonfarm.However,usinglower seedratesdoesruntheriskofestablishingasub-optimalplant pop-ulationforyieldwhenplantestablishmentconditionsarepoorand mayincreaseweedgrowthbetweenmorewidelyspacedplants.

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num-berofcultivars.Asubsequentpaperusingdatafromthisstudywill estimatetheminimumplantsamplesizewhilemaintaining reli-abilityinidentifyinggeneticdifferencesandareducednumberof traitsthatenablesthelodgingmodeltoestimatecultivarlodging susceptibilityperformances.

Theabsenceofrapid lodgingscreeningmethodologies could alsobecounteracted bythe implementationofmoleculartools toimprovelodgingresistanceof wheat.QTLs(quantitative trait loci)orothertrait-markerassociationsrelatedtolodgingresistance traitsmustbeidentiﬁedtodevelopgeneticmarkersfor marker-assistedselectionthatcanacceleratebreedingforthesecharacters. SeveralstudieshaveidentiﬁedQTLslinkedtostemdiameter(Berry andBerry,2015;Hai etal.,2005;Kelleretal.,1999),stem wall width(BerryandBerry,2015;Haietal.,2005),stemstrength,stem materialstrength,rootplatespread androotplatedepth(Berry andBerry,2015).GeneTaCM,involvedinthebiosynthesisoflignin, wasassociatedtothestemstrengthandlodgingindex(Ma,2009). Moreover,ithasbeenfoundthatseveralQTLinthewheatgenome arelinkedtobothyieldandstrawbiomass(Berryetal.,2008;Li etal.,2014)whichmightbeusefulonincreasingyieldandlodging resistancesimultaneously.

5. Conclusion

The present study hasidentified geneticvariation in spring wheatelitegermplasmforlodgingrelatedtraits.However, signifi-cantG×Einteractionshavealsobeenfoundaffectingconsistency acrossexperimentsand resulting in lowheritability for several characters.Targetstemstrengthtraitshadgoodheritabilityvalues equalorabove0.70.Themajoranchoragestrengthtrait(rootplate spread)wasstronglyaffectedbyG×Einteractionandthishada lowheritabilityof0.11.Thisstudyhasindicatedthatlodging-proof ideotyopetargetsfordiameter,materialstrengthandwallwidth ofthestemscanbeachievedinspringwheat,butnotyetinthe samecultivar.Stemstrengthandplantheightwere6and4 per-centbelowtherequireddimensionsanddonotrepresentadifficult challenge.However,newgermplasmandmanagementstrategies shouldbeimplementedtoachievethetargetrootplatespreadsince thiswassignificantlybelowtheideotypetarget.Linkagesbetween lodgingtraitsdonotrepresentasignificantchallengetoachievethe lodging-proofideotypethroughbreeding,althoughstrong associ-ationbetweenstemstrengthandstemwallwidthwillincreasethe biomasscostforstrongerstems.Theseresultswillhelpbreeders to(i)selectpotentialparentsforstrategiccrosses,(ii)focusonthe mostimportanttraitsthatdeterminegeneticvariationinlodging riskand(iii)indirectlyselectforstemlodgingrelatedtraitsduring theearlysegregatinggenerationswhenyieldtestsarenotyetbeing conducted.

Acknowledgements

Theauthorsacknowledgethesupportgiven byCIMMYTand SAGARPAthroughtheMasAgroInitiative,andCONACYTfor pro-vidingapostgraduatescholarshiptoF.J.P.C.Wearealsograteful totheWheatPhysiologyGroupfromtheGlobalWheatProgramat CIMMYT.

AppendixA. Supplementarydata

Supplementarydataassociatedwiththisarticlecanbefound,in theonlineversion,athttp://dx.doi.org/10.1016/j.fcr.2016.06.007.

References

Acreche,M.M.,Slafer,G.A.,2011.Lodgingyieldpenaltiesasaffectedbybreedingin Mediterraneanwheats.FieldCropsRes.122,40–48,http://dx.doi.org/10.1016/ j.fcr.2011.02.004.

Acreche,M.M.,Brice ˜no-Félix,G.,MartínSanchez,J.A.,Slafer,G.A.,2008. PhysiologicalbasesofgeneticgainsinMediterraneanbreadwheatyieldin Spain.Eur.J.Agron.28,162–170,http://dx.doi.org/10.1016/j.eja.2007.07.001. Aisawi,K.A.B.,Reynolds,M.P.,Singh,R.P.,Foulkes,M.J.,2015.Thephysiological

basisofthegeneticprogressinyieldpotentialofCIMMYTspringwheat cultivarsfrom1966to2009.CropSci.,http://dx.doi.org/10.2135/cropsci2014. 09.0601.

Aisawi,K.A.B.,2011.PhysiologicalProcessesAssociatedwithGeneticProgressin YieldPotentialofWheat(Ph.D.thesis).TheUniversityofNottingham,UK,333 pp.

Allan,R.E.,1986.Agronomiccomparisonsamongwheatlinesnearlyisogenicfor threereduced-heightgenes.CropSci.26,707–710.

Alvarado,G.,Lopez-Cruz,M.A.,Vargas,M.,Pacheco,A.,Rodriguez,F.,Burgue ˜no,J., Crossa,J.,2015.META-R(MultiEnvironmentTrialAnalysiswithRfor Windows).Version5.0.CIMMYT,Mexico,D.F.

Baker,C.J.,Berry,P.M.,Spink,J.H.,Sylvester-Bradley,R.,Grifﬁn,J.M.,Scott,R.K., Clare,R.W.,1998.Amethodfortheassessmentoftheriskofwheatlodging.J. Theor.Biol.194,587–603,http://dx.doi.org/10.1006/jtbi.1998.0778. Balyan,H.S.,Singh,O.,1994.PleiotropiceffectsofGA-insensitiveRhtgeneson

grainyieldanditscomponentcharactersinwheat.CerealRes.Commun.22, 195–200.

Berry,P.M.,Berry,S.T.,2015.Understandingthegeneticcontrolof

lodging-associatedplantcharactersinwinterwheat(TriticumaestivumL.). Euphytica,http://dx.doi.org/10.1007/s10681-015-1387-2.

Berry,P.M.,Spink,J.,2012.Predictingyieldlossescausedbylodginginwheat.Field CropsRes.137,19–26,http://dx.doi.org/10.1016/j.fcr.2012.07.019.

Berry,P.M.,Grifﬁn,J.M.,Sylvester-bradley,R.,Scott,R.K.,Spink,J.H.,Baker,C.J., Clare,R.W.,2000.Controllingplantformthroughhusbandrytominimise lodginginwheat.FieldCropsRes.67,59–81.

Berry,P.M.,Spink,J.H.,Gay,A.P.,Craigon,J.,2003a.Acomparisonofrootandstem lodgingrisksamongwinterwheatcultivars.J.Agric.Sci.141,191–202,http:// dx.doi.org/10.1017/S002185960300354X.

Berry,P.M.,Sterling,M.,Baker,C.J.,Spink,J.,Sparkes,D.L.,2003b.Acalibrated modelofwheatlodgingcomparedwithﬁeldmeasurements.Agric.For. Meteorol.119,167–180,http://dx.doi.org/10.1016/S0168-1923(03)00139-4. Berry,P.M.,Sterling,M.,Spink,J.H.,Baker,C.J.,Sylvester-Bradley,R.,Mooney,S.J., Tams,A.R.,Ennos,A.R.,2004.Understandingandreducinglodgingincereals. Adv.Agron.84,217–271,http://dx.doi.org/10.1016/S0065-2113(04)84005-7. Berry,P.M.,Sylvester-Bradley,R.,Berry,S.,2007.Ideotypedesignfor

lodging-resistantwheat.Euphytica154,165–179,http://dx.doi.org/10.1007/ s10681-006-9284-3.

Berry,P.M.,Berry,S.T.,Spink,J.H.,2008.Identiﬁcationofgeneticmarkersfor lodgingresistanceinwheat.Home-GrownCereal.Auth.Res.Proj.No.441 HGCA14pp.

Berry,P.M.,Kendall,S.,Rutterford,Z.,Orford,S.,Grifﬁths,S.,2015.Historical analysisoftheeffectsofbreedingontheheightofwinterwheat(Triticum aestivum)andconsequencesforlodging.Euphytica203,375–383,http://dx. doi.org/10.1007/s10681-014-1286-y.

Berry,P.M.,1998.PredictingLodginginWheat.(Ph.D.thesis).TheUniversityof Nottingham,UK,210pp.

Conway,G.,1997.Thedoublygreenrevolution.In:FoodforAllinthe21st Century.PenguinGroup,London,England.

Cooper,M.,DeLacy,I.H.H.,Basford,K.E.E.,1996.Relationshisamonganalytical methodsusedtoanalysegenotypicadaptationinmulti-environmenttrials.In: Cooper,M.,Hammer,G.L.(Eds.),PlantAdaptationandCropImprovement.CAB International,Wallingford,UK,pp.193–224.

Crook,M.J.,Ennos,A.R.,1995.Theeffectofnitrogenandgrowthregulatorsonstem androotcharacteristicsassociatedwithlodgingintwocultivarsofwinter wheat.J.Exp.Bot.46,931–938,http://dx.doi.org/10.1093/jxb/46.8.931. Easson,D.L.,White,E.M.,Pickles,S.J.,1993.Theeffectsofweather,seedrateand

cultivaronlodgingandyieldinwinterwheat.J.Agric.Sci.121,145,http://dx. doi.org/10.1017/S0021859600077005.

Ennos,A.R.,1991a.ThemechanicsofanchorageinwheattriticumaestivumL.:II. anchorageofmaturewheatagainstlodging.J.Exp.Bot.42,1607–1613. Ennos,A.R.,1991b.ThemechanicsofanchorageinwheattriticumaestivumL.:I

theanchorageofwheatseedlings.J.Exp.Bot.42,1601–1606,http://dx.doi.org/ 10.1093/jxb/42.12.1601.

Fischer,R.A.,Edmeades,G.O.,2010.Breedingandcerealyieldprogress.CropSci. 50,S-85–S-98,http://dx.doi.org/10.2135/cropsci2009.10.0564.

Fischer,R.A.,Stapper,M.,1987.Lodgingeffectsonhigh-yieldingcropsofirrigated semidwarfwheat.FieldCropsRes.17,245–258.

Flintham,J.E.,Borner,A.,Worland,A.J.,Gale,M.D.,1997.Optimizingwheatgrain yield:effectsofRht(gibberellin-insensitive)dwarﬁnggenes.J.Agric.Sci.128, 11–25.

Foulkes,M.J.,Slafer,G.a.,Davies,W.J.,Berry,P.M.,Sylvester-Bradley,R.,Martre,P., Calderini,D.F.,Grifﬁths,S.,Reynolds,M.P.,2011.Raisingyieldpotentialof wheatIII.Optimizingpartitioningtograinwhilemaintaininglodging resistance.J.Exp.Bot.62,469–486,http://dx.doi.org/10.1093/jxb/erq300. Hai,L.,Guo,H.,Xiao,S.,Jiang,G.,Zhang,X.,Yan,C.,Xin,Z.,Jia,J.,2005.Quantitative

(11)

populationofwheat(TriticumaestivumL.).Euphytica141,1–9,http://dx.doi. org/10.1007/s10681-005-4713-2.

Kelbert,A.J.,Spaner,D.,Briggs,K.G.,King,J.R.,2004.Theassociationofculm anatomywithlodgingsusceptibilityinmodernspringwheatgenotypes. Euphytica136,211–221,http://dx.doi.org/10.1023/B:EUPH.0000030668. 62653.0d.

Keller,M.,Karutz,C.,Schmid,J.E.,Stamp,P.,Winzeler,M.,Keller,B.,Messmer, M.M.,1999.Quantitativetraitlociforlodgingresistanceinasegregatingwheat xspeltpopulation.TAG98,1171–1182.

Kertesz,Z.,Flintham,J.E.,Gale,M.D.,1991.EffectsofRhtdwarﬁnggenesonwheat grainyieldanditscomponentsundereasterneuropeanconditions.CerealRes. Commun.19,297–304.

Lantican,M.A.,Braun,H.J.,Payne,T.S.,Singh,R.P.,Sonder,K.,Baum,M.,vanGinkel, M.,Erenstein,O.,2016.ImpactsofInternationalWheatImprovementResearch, 1994–2014.CIMMYT,Mexico,D.F.

Li,Z.K.,Jiang,X.L.,Peng,T.,Shi,C.L.,Han,S.X.,Tian,B.,Zhu,Z.L.,2014.Mapping quantitativetraitlociwithadditiveeffectsandadditivexadditiveepistatic interactionsforbiomassyield,grainyield,andstrawyieldusingadoubled haploidpopulationofwheat(TriticumaestivumL.).Genet.Mol.Res.13, 1412–1424.

Ma,Q.-H.,2009.Theexpressionofcaffeicacid3-O-methyltransferaseintwowheat genotypesdifferinginlodgingresistance.J.Exp.Bot.60,2763–2771,http://dx. doi.org/10.1093/jxb/erp132.

Miralles,D.J.,Slafer,G.A.,1995.Yield,biomassandyieldcomponentsindwarf: semi-dwarfandtallisogeniclinesofspringwheatunderrecommendedand latesowingdates.PlantBreed.114,392–396.

Parry,M.a.J.,Reynolds,M.,Salvucci,M.E.,Raines,C.,Andralojc,P.J.,Zhu,X.-G.,Price, G.D.,Condon,A.G.,Furbank,R.T.,2011.RaisingyieldpotentialofwheatII. Increasingphotosyntheticcapacityandefﬁciency.J.Exp.Bot.62,453–467, http://dx.doi.org/10.1093/jxb/erq304.

Pask,A.,Pietragalla,J.,Mullan,D.,Reynolds,M.P.,2012.PhysiologicalBreedingII:a FieldGuidetoWheatPhenotyping.CIMMYT,Mexico,D.F.

Pi ˜nera-Chavez,F.J.,Berry,P.M.,Foulkes,M.J.,Jesson,M.A.,Reynolds,M.P.,2016. AvoidinglodginginirrigatedspringwheatI.Stemandrootstructural requirements.FieldCropsRes.,inPress.

Pinthus,M.J.,1974.Lodginginwheat,barley,andoats:thephenomenonitscauses, andpreventivemeasures.Adv.Agron.25,209–263.

Reynolds,M.,Bonnett,D.,Chapman,S.C.,Furbank,R.T.,Manès,Y.,Mather,D.E., Parry,M.J.a.,2011.RaisingyieldpotentialofwheatI.Overviewofaconsortium approachandbreedingstrategies.J.Exp.Bot.62,439–452,http://dx.doi.org/ 10.1093/jxb/erq311.

Reynolds,M.,Foulkes,J.,Furbank,R.,Grifﬁths,S.,King,J.,Murchie,E.,Parry,M., Slafer,G.,2012.Achievingyieldgainsinwheat.PlantCellEnviron.35, 1799–1823,http://dx.doi.org/10.1111/j.1365-3040.2012.02588.x. Richards,R.A.,1992.Theeffectofdwarﬁnggenesinspringwheatindry

environments.I.Agronomiccharacteristics.AustJ.AgricRes43,517–527.

SASInstituteInc,2004.SASSystemforWindows.SASInstitute,Inc.Cary,NC,USA (Version9.1.).

SIAP,2016.ServicioDeInformacionAgroalimentariayPesqueraWheatHarvest Area2014,Availableat:www.siap.gob.mx(accessed05.08.16).

Sayre,K.D.,Rajaram,S.,Fischer,R.A.,1997.Yieldpotentialprogressinshortbread wheatsinNorthwestMexico.CropSci.37,37–36.

Slafer,G.A.,Araus,J.L.,2007.Physiologicaltraitsforimprovingwheatyieldundera widerangeofconditions.In:Spiertz,P.C.S.,vanLaar,H.H.(Eds.),Scaleand ComplexityinPlantSystemsResearch:Gene–Plant–CropRelations.Springer Dordrecht,TheNetherlands,pp.147–156.

Slafer,G.A.,Elia,M.,Savin,R.,García,G.A.,Terrile,I.I.,Ferrante,A.,Miralles,D.J., González,F.G.,2015.Fruitingefﬁciency:analternativetraittofurtherrise wheatyield.FoodEnergySecur.4,92–109,http://dx.doi.org/10.1002/fes3.59. Stapper,M.,Fischer,R.A.,1990.Genotype,sowingdateandplantspacinginﬂuence

onhigh-yieldingirrigatedwheatinsouthernNewSouthWalesIII.Potential yieldsandoptimumﬂoweringdates.Aust.J.Agric.Res.41,1043–1056,http:// dx.doi.org/10.1071/AR9901043.

Tripathi,S.C.,Sayre,K.D.,Kaul,J.N.,Narang,R.S.,2003.Growthandmorphologyof springwheat(TriticumaestivumL.)culmsandtheirassociationwithlodging: effectsofgenotypesNlevelsandethephon.FieldCropsRes.84,271–290, http://dx.doi.org/10.1016/S0378-4290(03)00095-9.

Tripathi,S.,Sayre,K.,Kaul,J.,Narang,R.,2004.Lodgingbehaviorandyieldpotential ofspringwheat(TriticumaestivumL.):effectsofethephonandgenotypes. FieldCropsRes.87,207–220,http://dx.doi.org/10.1016/j.fcr.2003.11.003. Tripathi,S.C.,Sayre,K.D.,Kaul,J.N.,2005.Plantingsystemsonlodgingbehavior

yieldcomponents,andyieldofirrigatedspringbreadwheat.CropSci.45, 1448–1455,http://dx.doi.org/10.2135/cropsci2003-714.

Vargas,M.,Combs,E.,Alvarado,G.,Atlin,G.,Mathews,K.,Crossa,J.,2013.Meta:a suiteofsasprogramstoanalyzemultienvironmentbreedingtrials.Agron.J. 105,11–19,http://dx.doi.org/10.2134/agronj2012.0016.

Webster,J.R.,Jackson,L.F.,1993.Managementpracticestoreducelodgingand maximizegrainyieldandproteincontentoffall-sownirrigatedhardred springwheat.FieldCropsRes.33,249–259, http://dx.doi.org/10.1016/0378-4290(93)90083-Y.

Weibel,R.O.,Pendleton,J.W.,1964.Effectofartiﬁciallodgingonwinterwheat grainyieldandquality.Agron.J.56,487–488.

Whaley,J.M.,Sparkes,D.L.,Foulkes,M.J.,Spink,J.H.,Semere,T.,Scott,R.K.,2000. Thephysiologicalresponseofwinterwheattoreductionsinplantdensity. Ann.Appl.Biol.137,165–177.

Wiersma,J.J.,Dai,J.,Durgan,B.R.,2011.Optimumtimingandrateof

trinexapac-ethyltoreducelodginginspringwheat.Agron.J.103,864–870, http://dx.doi.org/10.2134/agronj2010.0398.