Diversity in plant breeding: a new conceptual framework

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Diversity in plant breeding: a new conceptual framework

Isabelle Litrico, Cyrille Violle

To cite this version:

Isabelle Litrico, Cyrille Violle. Diversity in plant breeding: a new conceptual framework. Trends in

Plant Science, Elsevier, 2015, 20 (10), pp.604-612. �10.1016/j.tplants.2015.07.007�. �hal-01214153v3�

Opinion

Diversity

in

Plant

Breeding:

A

New

Conceptual

Framework

Isabelle

Litrico

*

and

Cyrille

Violle

Faced with anacceleratingrate of environmentalchange andtheassociated needforamoresustainable,low-inputagriculture,theurgentnewchallengefor cropscienceistofindwaystointroducegreaterdiversitytocroppingsystems. However,thereisadearthofgenericformalisminprogramsseekingtodiversify crops.Inthisopinion,weproposea newframework,derived fromecological theory,thatshouldenablediversitytargetstobeincorporatedinto plant-breed-ingprograms.Whileecologicaltheoryprovidescriteriaformaintainingdiversity andoptimizingtheproductionofmixtures,suchcriteriaarerarelyfullyrealized innaturalecosystems.Conversely, cropbreedingshouldoptimize both agro-nomicvalueandtheabilityofplantstoperformandlivealongsideoneanother. Thisframeworkrepresentsanopportunitytodevelopmoresustainable crops andalsoaradicalnew waytoapplyecologicaltheorytocroppingsystems.

ANewFrameworkforBreedingDesign

Onequestionhasbeenmuchdebatedinagronomyandecology[1–3]:isitbettertoliveamong strangersorrelatives;inotherwords,areplantmixtures(seeGlossary)moreproductive,more resistanttopestsandpathogens,andmoresustainablecomparedwithplantmonocultures? The answer will have crucial implications for plant-breeding programs. The introduction of geneticand/orspeciesdiversity(geneticheterogeneitysensu lato)tocroppingsystems isa pressingissueinagriculture[4].Therearetwomainchallenges:(i)ageneralneedtooptimizethe multifunctionality of crop systems [5,6]; and (ii) a need to adapt existing crop systems to acceleratingratesofenvironmentalchanges.

Tofacethesechallengeswitharesponseofchoice,ecologicalstudiessuggestthatagricultural systemscontaininghighgeneticheterogeneityshouldbefavored[1,3].Thispathshouldalso favorlow-inputagriculture, which isanotherofthemajorchallenges facedbycrop science today. Compared with a monoculture, the combination of legumes and grasses in sown pasturesisagoodexample ofhowsignificantproductivityimprovements canbeobtained, withouttheinputofexternalnitrogen[7].Nevertheless,despiteimportantongoingeffortsto mergeecologyandagriculturalsciencewithinacommondiscipline(agroecology),the introduc-tionofgeneticheterogeneitytocropsstillpresentsasignificantchallengetobreeders. Intheoreticalecology,diversity(especially,speciesdiversity)hasanimportantroleinthefunctioning andresilienceofecosystems[8–10].Overthepasttwodecades,numerousecologicalexperiments havebeeninitiatedthatexaminethecontrolofecosystemprocessesbybiodiversity.Theseinclude controlofplantproductivity[2,11,12].Despitesometimes-heateddebate,theevidence neverthe-less suggests a positive effect of biodiversity on primary productivity. Strikingly,most crop-breedingprogramsarepersistentlymonospeciesand/or-genotypeculturalintheiroutlook. Themainstreamapproachtocropbreedingisstilltoimprovegenotypesbycultivatingindividuals inpureculture,eitherinmono-genotypicormulti-genotypicpopulationsofasinglespecies.This

Trends

To face societal and environmental challenges, agriculture is changing. Promotingspeciesand/orgenetic het-erogeneityinagronomiccoversisone ofthekeydevelopments.

Mostcropcoverscomprise mono-gen-otype varieties, except synthetic or populationvarietiesthat,through selec-tionstrategy,containsomeresidualand noncontrolledgeneticdiversity. Thereare currentlyfeworno plant-breedingapproachesappliedto agro-nomiccoversthatincorporatemultiple genotypesand/orspecies.

Ecologytheoryprovidesthekeyforthe maintenance and optimized applica-tionofheterogeneouscovers. Wecallforecologicalassemblyrulesto proposea novelparadigmfor plant-breeding programs when selecting foragronomicmixtures.

1

P3FUR004–INRA–LeChêneRD 150,F-86600Lusignan,BP86006, France

2

CEFEUMR5175,CNRS–Université deMontpellier–UniversitéPaul-Valéry Montpellier–EPHE-1919routede Mende,F-34293Montpellier,CEDEX 5,France

*Correspondence:

isabelle.litrico@lusignan.inra.fr

(I.Litrico).

604 TrendsinPlantScience,October2015,Vol.20,No.10 http://dx.doi.org/10.1016/j.tplants.2015.07.007 ©2015ElsevierLtd.Allrightsreserved.

mirrorsthemostcommonstructureofcurrent varieties(Figure1),whosecovercomprises a singlegenotype(purelinesorhybrids)ormultiplegenotypes,inthecaseofsyntheticvarieties. However,evenforsyntheticvarieties,geneticdiversityislowanddirectionalselectionisusedto reducecover-widephenotypicvariance.Competitionexperimentsdescribedintheecological andevolutionaryliteraturehavelongstressedthattheperformanceofagenotypeinpureculture candifferradicallyfromitsperformanceinmixedculture[13].Similarfindingshavebeenreported intheagronomyliterature[14–16].The differenceinperformancesbetween pureandmixed culturesarisesfromlocalselectionpressuresgeneratedbyintra-and/orinterspecificinteraction withneighborsinthemixture[17–20].Therefore,there isanurgentneedforplant-breeding schemestobegintoformalizetheintegrationoftheseinteractions,ratherthanignorethem(with theexceptionofresearchdoneonbi-speciesmixtures;e.g.,[21,22]).

Breedingprogramsusuallyseektooptimizekeyagronomictraits,suchasseedqualityand quantity,biomassproduction,andpestanddiseaseresistance.Clearly,thisobjectiveshould persistwhenacropmixtureisthebreedingtarget,butothertraitsmustalsobeincorporatedand optimized,including,critically,anabilityto‘liveandperformwithothers’.Interestingly, commu-nityecologyhasmadeimportantrecentprogressinthis,helpedbytheoreticaladvancesin trait-basedecology[23–25].Here,webrieflyreviewearlierattemptsinbreedingdesigntoimprove cropmixtures.Wealsoproposeanewframeworkforbreedingdesignthatexplicitlyincorporates geneticheterogeneitythroughtheinclusionofmechanismsderivedfrombiodiversitytheory.

Glossary

Agronomictrait:phenotypicfeature ofaplantthatatleastpartially determinesitsagronomicvalue (biomassproductionand/orseed production).

Artificialselection(orselective breeding):breedingofplantswith thepurposeofimprovingtraitsof particularimportancetohuman beings.

Assemblyrulesinecology:these rulesrefertothesetofprocesses thatexplainsthelocalcoexistenceof species.Thisincludestheroleof bioticinteractionsandabiotic constraintsonspeciesperformance. Thisideaisintroducedhereinthe contextofplantbreeding

programmes,tohelpdevelopasetof rulestoassistbreederstocreate productiveandsustainable multi-species(ormulti-genotype)mixtures (‘Ideomixes’).

Compositemulti-linepopulation: apopulationofhybridsarisingfrom crossesbetweenmultipleinbred lines.

Functionaltrait:anymorphological, physiologicalorphenologicalfeature, measurableatsomelevel(fromcell towhole-organism)withoutreference totheenvironmentoranyotherlevel oforganisation[50].

Inbredline:apoolofindividuals derivingfromasinglehomozygote genotype.

Interactiontrait:phenotypicfeature ofaplantinvolvedinitsinteractions withneighboringconspecificor heterospecificplants. Mixture:amulti-speciesand/or multi-genotypeculture.

Monoculture:single-speciesculture. Herethedefinitionisrestrictedtoa single-genotypeculture.

Multi-lines:amixtureofinbredlines. Resource-usecomplementarity: thetendencyforcompetingspecies toexploredifferentportionsofthe resourcesavailablelocally. Tradional selecon

schemes with genealogic and recurrent selecon Test of the ability of a

variety to perform in ‘associaon’ with

other variees Evoluonary plant

breeding

Increasing genec and species heterogeneity Approaches to plant breeding

One genotype

• Hybrid Fvariety (maize, sunflower…)

• Pure line variety (wheat, soya...) • Clonal culvar (olive, potato…)

=> most common situaon in CA

Several genotypes

• Mix of hybrid F variees (rare situaon in CA)

• Mix of pure line variees (barley, wheat, rare situaon in CA) • Mix of synthec variees (rare situaon in CA, but occurs in

forestry and grasslands)

• Synthec variees (alfalfa, leek, rare situaon in CA, but occurs in

forestry and grasslands)

Single-species cover Bi-species cover

One genotype per species

• Mix of pure lines and/or hybrids from different species (rare situaon in CA but occurs in agroforestry )

Several genotypes per species

• Mix of synthec variees (rare situaon in CA, but occurs in agroforestry or temporary grasslands; e.g., ryegrass and white clover)

Mul-species cover (more than two species)

Several genotypes per species

• Mix of synthec variees (Cocksfoot, Ryegrass, Alfalfa, Clover, …)

(extremely rare in CA but occurs in temporary grasslands)

(C) (D) (E) (F) (G) (J) (I) No development yet _(B)

One genotype per species

• Extremely rare situaon in CA

(A)

(H)

Figure1.DifferentLevelsofSpeciesandGeneticDiversitywithinAgronomicCoversUsedinConventional Agriculture(CA)andtheirRelatedPlant-BreedingApproach.Differentlevelsofdiversitywithinagronomiccoversdo existinCA,fromsingle-genotypeandsingle-speciessituationstomulti-speciesandmulti-genotypessituations.The advancement(green,advanced;orange,weak;red,nodevelopment)inplant-breedingapproachesdependsonthelevelof diversity.Seemaintextformoredetailoneachtypeofplant-breedingapproach.Photos:(A)Multi-speciessowngrassland (LotuscorniculatusL.,Medicagosativa,TrifoliumpratenseL.,TrifoliumrepensL.,Dactylisglomerata,Loliumperenne, Festucaarundinacea);(B)Mixofcereals(TriticosecaleWittm.exA.Camus,AvenasativaL.,Hordeumvulgare)andlegume (PisumsativumL.);(C)Mixofgrass(L.perenne)andlegume(T.repensL.);(D)Mixofcereal(Triticumaestivum)andlegume (PisumsativumL.)(E)Mixinagroforestry(TriticumdurumandhybridJuglans);(F)MixofT.durumcultivars;(G)M.sativaL.; (H)Zeamays;(I)T.durum;(J)OleaeuropaeaL.Reproduced,withpermission,fromD.Denoue(A),C.Maitre(B),B.Cauvin (C),M.C.Lhopital(D),C.Duprax(E),P.Saulas(F),M.Preudhomme(G),J.Niore(H),H.Cochard(I),andJ.Weber(J). CopyrightINRAinallcases.

LivingandPerformingwith Others:TheChallengesofPlant-Breeding Programs

Despitealong-terminterestintheimprovementofmixturesthroughplantbreeding[26],little formalismhasbeendevelopedtodealwiththebreedingofmultiplecroppingandmulti-species mixtures [27]. Untilnow, breeding programs have attemptedto select varieties and create ideotypes basedonan ‘average’ability to perform whengrown in ‘association’ with other varieties[28].Toestimatethisaverageabilitytoperforminassociation,theapproachusedhas beenderivedfromdialleltestswithmaize(Zeamays)forthedeterminationoftheabilityoflinesto hybridize[29,30].Notably, this has beenused to improvemulti-genotype blends, including multi-line[31–33]andmulti-species[29,34,35]mixtures.However,thisapproachhaslimited portabilitybeyondthespecifictestmaterialandinthecontextofaparticularstudy.Tosome extent, these limitations can be offset by using large sample sizes and a broad range of genotypes[28].Nevertheless,evenif‘biodiversity’isrestrictedtotheconsiderationofbinary associations,thelargenumberofdifferentbinarycombinationsrapidlymakestestingthemall difficult[23].Furthermore,usingpairwisecombinationshasoftenbeendescribedinthe eco-logicalliteratureasposinganimpasse,becauseagenotypebehavesdifferentlyinthepresence ofoneormorecompetinggenotypes[23].Thus,McGilletal.[23]callfortheanalysisofthe ‘interactionmilieu’asawhole,toaccountforallkindsofdiffusebioticinteractionoccurringinan assemblage.Italsoavoidsthelogisticproblemofanalyzingapotentiallyvastnumberofpairwise combinations.

Insteadofoptimizingapoolofgenotypesbyestimatingtheiraverageabilitiestoliveandperform with others,a proposed alternative has beento directly exposecrop mixtures to complex selectionpressures[17,36,37].Thisaccountsforthelocalselectionpressuresduetogenotype genotype interactionswithin themixture.This isthemain objectiveofevolutionary plant-breeding methods[28,38,39].Evolutionary plant breeding has beenappliedto composite multi-line populations but never to multi-species mixtures [14,21] The efficiency of this selectionapproachinmulti-linemixturesdependsonpotentialnegativecorrelationsbetween fitnessandagronomicvalueinselectedcoexistingindividuals[40].Tomitigatethe consequen-cesofanegativecorrelation(oralackofone)betweenfitnessandagronomicvalue,artificial selectionmanipulationscanbeusedwithinthesemixturesinparallelwithnaturalselection[41]. Twomajorlimitationsareassociatedwiththisapproach:(i)drifteffects,whichcanleadtotheloss ofgeneticvariability[39];and(ii)thelongperiodrequiredtoallownaturalselectionprocessesto act;thisisespeciallyaproblemiftheselectiontargetsareperennialplants.

Altogether,attemptstoselectplantsforanabilitytoliveandperformwellwithotherplantshave rarelybeenexploredordevelopedatthisstage.Attheveryleast,theyseemratherinefficient waystorespondtoactualagroecologicalneedswhenappliedtomixtureswithmorethantwo components.Here,wearguethattheuseofknowledgebasedonecologicaltheoryshouldbeof assistanceinpromotingwithin-cropcoverdiversity.Thisshouldimprovetheperformanceof mixturesthroughredesignedbreedingprogramsand,atthesametime,maycircumventsome ofthelimitationsofearlierapproaches.

ImprovingthePerformanceofCropMixtures:Insightsfrom Ecological

Theory

Foralongtime,ecologistsandagronomistshavestudiedtheyieldandstabilityofmixturesof genotypesorofspecies[42–46].Overthepast20years,experimentalandtheoretical under-standingshaveconvergedtowardsacceptanceofthegeneralprinciplethatamixtureofspecies or genotypes is inaverage more productive, and its production is more stable with time, comparedwitheachspeciesgrowninisolation[2,47,48].Thisprinciplehascrucial consequen-cesforartificial(crop)mixtures,grownundercontrolledconditions.Akeyunderlyingconceptis thatanecosystemcomprisingseveralspecieseachexploringaportionoftheavailablelocal

resources(resource-usecomplementarity),isexpectedtobemoreefficientintheutilization ofthetotalpoolofavailableresourcesand,thus,shouldbeabletotransformthemintoagreater amountofbiomass[49].Thishypothesishasalsobeenappliedtothetemporalresponseof ecosystems ina fluctuatingenvironment. Interms of composition andyield, aspecies-rich ecosystemisexpectedtobethemoststableovertime[43]because,ateachtimestep,there should beat least one persistent species thatis well adaptedto any given environmental condition[2,44,48].Althoughtheunderlyingmechanismsofthestabilizingroleofbiodiversityare notcompletelyelucidated[45],thediversity–stabilityhypothesisispivotalforthedevelopmentof sustainable crops. Recently, the plus-value of species and genetic diversity for biomass productionanditstemporalstabilityinsowngrasslandshasbeendemonstrated[46].

Inrecentdecades,theriseoftrait-basedecologyhasallowedtestingandquantificationofthe mechanismsofresource-usecomplementarybetweenspeciesand,thus,anunderstandingof thelinks between plant biodiversityand primaryproductivity.A keypostulate isthat some functionaltraits(defined as any morphological, anatomical, physiological,orphenological featuremeasurableattheindividuallevel[50])arerelatedtotheresource-useaxesofthespecies

[51].Inotherwords,measuringthefunctionaltraitsofaplantisexpectedtoreflectthetypeand quantityoftheresourcesitconsumes.Asaconsequence,beyondthesignificanteffectofthe numberofspeciesorgenotypes[2,52,53]ontheperformanceofanecosystem,thereisgrowing consensusthattheroleoffunctionaltraitdiversity(functionaldiversity)iskeytothemaintenance ofaproductiveandstableecosystem[54].Maximizingbetween-speciesfunctionaltrait differ-ences in a particular ecosystem is a way of maximizing ecosystem-level resource-use complementarity.

However, this resource-economics perspective to ecosystems is conditioned by complex between-traitcorrelations,as emphasizedinthenext section.Furthermore,thisperspective ofecosystemfunctioningnecessarilyimpliesafocusonthe‘speciesunit’andadescriptionof speciesby trait averages(the mean-field approach [24]). This approachhas recently been challengedintheecologicalliterature[12,24,55,56],whereitisarguedthatindividualdifferences maybeasimportantasbetween-speciesdifferencesinexplainingthemaintenanceofspecies coexistenceand,subsequently,thecontrolofecosystemfunctioningbybiodiversity.Toquantify resource-usecomplementaritywithinecologicalcommunitiesbytheintraspecific:interspecific phenotypicvarianceratio, Violleetal.[24]usefullyproposed avariance decomposition.This echoestheuseofWright'sstatisticsinpopulationgenetics.Thisapproachisofinterestforplant breeding,whichalreadyquantifiestwodistinctkindsofvariance:geneticandphenotypic.

FromNatural PlantCommunitiesto‘Optimized’SpeciesAssemblagesin

CroppingSystems

Itisstrikingthatthefunctionalrelationswithinnaturalandexperimentalecosystemsareoften verydifferent.Inexperimentalecosystems,therelationsaremostoftenpositiveandsaturating, whereas in natural ecosystems, a range of relation forms are found (positive, neutral, and negative)[57–59]. Onereason for this wouldseem to bea lack ofa true ‘optimization’ of resource-usecomplementaritywithinmanynaturalecosystems.This,inturn,islikelybecause thereare severalkinds oftrade-offwithinorganisms andpopulations [60–62].Asa conse-quence,thediversityeffectonecosystemprocesses,suchasproductivity,isoftenweakunder natural conditions. Conversely,one may expect greater diversity effects inan agronomical context,inparticularunderlow-inputconditions[46,63].Here,weproposethatplant-breeding programscanoptimizecomplementaritybetweengenotypesinamixture,to‘force’thepositive relationbetweendiversityandyield.Thisisthecornerstoneofthenovelframeworkwenow proposeforplantbreeding,wherebybreedersshouldfocusonthetraitsidentifiedasthemajor contributorstoresource-usecomplementarityinecologicalstudies.Asastartingpoint,rooting depth, vegetative architecture, and phenology, including growth rhythms, are particularly

important[64–67].Thesetraitsinvolvedininteractionsbetweengenotypesandspecies,weterm ‘interactiontraits’.Fromniche-basedecologicaltheory,wewouldexpectgreater resource-usecomplementaritybetweenspecies(orgenotypes)whenthebetween-speciesvariance(or between-genotypesvariance)ofinteractiontraitsishighandthewithin-species variance (or within-genotypesvariance) of interactionstraits is low[24,55,68] (Figure 2). A mixture that maximizesdifferencesininteractiontraitvaluesbetweenindividualswillbemoreproductiveand morestable with time [69], especially under suboptimal environmental conditions[46].We suggestthatthisshouldbeakeyobjectiveofthenewgenerationofdiversity-orientedbreeding programs.

Itisimportanttonotethatdifferenttypesofcompetitiveinteractiondoexist[70–72]. Resource-usecomplementaritycanbepromotedwhencompetingspeciesdisplaycontrastingtraitvalues. Conversely, these species can suffer from competitive exclusion in cases of competition hierarchy(if one specieshas acompetitive advantage overanother). This is detrimental in thecaseofcropmixtures,inwhicheachcomponentneedstobemaintainedtoperformwell.As a consequence, those competitive exclusion processes will have to be removed by plant breeding(seebelow).

Beyondtheroleofresource-usecomplementarity(and,thus,between-speciestraitdifferences) inthe regulationofecosystem processes,trait-basedecologyhasalso clearlyidentifiedthe importantroleofdominantspeciesinthecontroloftheoverallyieldofamixture[73].Indeed,the short-termyieldofgrasslandcommunitiesisprimarilyexplainedbythetraitvaluesofthemost abundantspecieswithinthemixtures [74].Inotherwords,ecosystemsthatcontainspecies havingtraitsthatconvergetowardsthetraitsofthemostproductivespeciesofthemixture[75], expressthebestyields[76,77].Hereafter,thetraitsinvolvedinplantyieldaretermed‘agronomic

Trait axis Trait axis Agronomic traits Interacon traits

σ

σ

σ

σ

Figure 2. Variance Partitioning AppliedtoPhenotypicDiversityina MixtureofCropGenotypesor Spe-cies.Consideramixturecontaining multi-plecomponents(genotypesorspecies). Foranyphenotypictrait,thereisa within-componentvariance(sG2

)andatotal var-iance(sM2

)(thevariancebetweenall indi-vidualsinthemixtureirrespectiveoftheir taxonomicorgenotypicidentity).(A)The optimumagronomicvalueofthemixture shouldfirstbemaximized.Todothis,both thewithin-componentvariance(sG2

)and thetotalvariance(sM2

)shouldbe mini-mizedaroundasingleoptimalvaluefor eachofthekeyagronomictraits.(B)Next, resource-use complementarity between thecomponents shouldbe maximized. Todothis,thevarianceofeachinteraction traitshouldbemaximizedbetween com-ponents (divergent selection) and mini-mizedwithin eachcomponent (without overlapbetweenthecurvesforeach com-ponent).Inthisway,thesG2_:sM2

ratiowill be minimized, following the framework proposedbyViolleetal.[24].

traits’.Agronomictraitscanbeeitherdirectmeasuresofyield(e.g.,vegetativebiomass,grain production,orseedquality)orproxiesofyield,asiscommoninfunctionalecology(e.g.,specific leafareaisakeydeterminantofthegrowthrateofaspeciesandecosystemproductivity[74,78]). Plant-breedingprogramsshouldworktooptimizethemeanvalueoftheagronomictraitsofeach ofthecomponentsofamixture,becausethisshouldleadtoagreateryieldforthewholemixture.

FromIdeotypestoIdeomixes

Theincorporationofplantbreedingintoagroecologicalprogramsinsuchawayastobestexploit theadvantagesofmixinggenotypesandspeciesrepresentsthenextmajorstepinagroecology. Indeed,breedingcanbreaktheconstraintsinherenttowildspeciesandnaturalecosystems[79], withtheresultthatseveralfunctionscanbeoptimized.However,thisalsoimpliesaparadigm shift for thinking inplant breeding.Since the green revolution started,plant breedershave focusedonideotyping; thatis, the creationof elite genotypesselected for their agronomic performanceinaparticularartificialenvironment.Giventhegrowingimportance(asdiscussed above)ofusingmixturestomeetthechallengesposedbytheneedforsustainabilityina fast-changingworld,weproposeherethecreationofelitemixtures,whichweterm‘ideomixes’.A criticaladvantageofbreedingisthatitcanovercomethelimitationsandcomplexityofnatural ecosystemsby decouplingvarioustraits(hereinteraction andagronomictraits)bybreaking geneticconstraintsandoptimizingvariousmechanismsviathetraitsthathavebeenfoundto displayantagonistvaluesinthefield(e.g., resource-usecomplementarityversuscompetition hierarchy).Inecology,ithasbeenarguedthatthecurverepresentingtherelationbetweenyield andthenumberofspecies,issaturating[11,80,81](Figure3).Thisisthoughttobebecauseofan increaseinfunctionalredundancyamongspeciesasthenumberofspeciesincreases;thatis,as speciesnumbersincrease,thespeciesaremorelikelytobeecologicallysimilartoeachother (see[82]foranexample).However,theoreticallyatleast,breedingshouldbeabletocreatean artificialmixturehavingnoredundancyandallcomponentsofthemixtureswouldcompletelyfill theecologicalspace.Thesaturationpointcanbeonlyreachedathigherlevelsofdiversitythanks tothe selectionof contrastingandmorespecializedgenotypesand/orspecies, as demon-stratedinmicrobialexperiments[83].Weseeplantbreedingashavingthepotentialtoallow escapefromtheenvelopecurveidentifiedasaconstraintinecology(Figure3).Next,weshow howbreedingcanproduceideomixes.

Genec heterogeneity

Natural ecosystems

Crop mixtures

Funconing

Figure3.HypotheticalGenetic Het-erogeneity Functional Relations in NaturalEcosystems(Gray)andCrop Mixtures(Red).Thegenetic heteroge-neity of an assemblage can increase throughanincreaseineitherthenumber ofspecies(orgenotypes)orinthegenetic distancesbetweenthespecies(or geno-types).Asaturatingcurveisexpectedfor natural ecosystems due to increasing functional redundancy (see main text). Saturationisnotexpectedforcrop mix-tureswherebreedingisabletomaximize the functioning of all components and theirabilitytocohabitandperformwith each other (notably if ‘specialists’ are selected:seemaintextformoredetail). The creation of crop mixtures through breedingrepresentsanewandpromising avenueforagroecologicalresearch.Inthis schema,productivitylevelsforboth nat-uralandartificialmixturesandthe hierar-chy between them are represented diagrammatically.

Optimizationof CropMixtures: TowardsRedesignedBreedingPrograms

Weproposeanovelframeworkforimprovingcropmixturesbybreeding.Basedonideasfrom theoreticalecology,aswellasrecentadvancesintrait-basedecology,weproposethatbreeding programmes be refocused by basing them on the decoupling and optimization of both interactiontraitsandagronomictraits.Thisimpliesthatselectionisdonenotonlyforthemean valuesofagronomictraits(andoccasionallyalso forthevariance,inthecase ofagronomic qualityofmixtures:seebelow),butalsoforthemeansandvariancesofinteractiontraits.The choiceoftargettraitsisacentralelementofthisapproach. Itissuggestedthatthefocusis placedon:(i)asmallsetofmajortraits,suchasvegetativebiomassorgrainproduction(theseare centralagronomictraitsandtheirchoicewilldependontheselectionobjectives);and(ii)three typesofinteractiontrait.Asapioneeringchoiceofinteractiontraitstofocuson,weproposetraits relatedto resourceforaging (e.g., rooting depth), phenology(e.g., the period of vegetative production),andabovegroundarchitecture(e.g.,stembranching).Thesetraitsrelatetospatial resource-usecomplementarity,temporalresource-usecomplementarity,andlightpartitioning withinthecover,respectively.Preliminaryworkiscriticaltochoosethebestcandidateinteraction traitsandthisisbestguidedbyalternatingbetweenthetraditionalapproachesofecologyand cropscience.Indeed,theidentificationofinteractiontraitsisalong-standingquestioninecology

[71,84,85]butremains puzzling[86].Specificecophysiologicalstudiesandrecurrent use of physiologymodelinginagronomycanprovide insightsintothissearch forthemostrelevant interactiontraits.

Thegeneralobjectiveofabreedingprogramrefocusedonamixtureisto:(i)optimizethemean valuesoftheagronomictraitsofthemixturebyforcingallgenotypestoconvergetowardsan optimalvalue(Figure2);and(ii)maximizethevariancebetweenthecomponentsofthemixturefor theinteractiontraitswhilesimultaneouslyminimizingthewithin-componentvariance(Figure2).In thecase where agronomic quality is the targetof selection, the objective can beto select agronomictraits(e.g.,foragechemistry)thatmayormaynotbethesameforeachcomponent ofthemixture.Thus,maximizationofthevariancecanalsobetargetedforagronomictraits.To reachthesegoals,weproposeatwo-stepframework,laidoutindetailbelow.

StepOne(SelectionStep)

Thefirststepreliesonimprovingtheagronomicandinteractiontraitsforeachcomponentofthe mixture.Inthecaseofspeciesmixtures,theideaistoapplyclassicalbreedingschemestoselect specificvaluesofagronomicandinteractiontraitsforeachspeciesseparately.Inmostcases,for agronomictraits,selectiontowardsthesametraitmeansforallspeciesisneeded.Importantly, asdescribedinsteptwo(assemblystep),thevaluesofinteractiontraitshavetodifferamong speciessoastomaintainthediversityofthemixtureandtheabilityofeachspeciestoliveand performwithothers.Thesamelogiccanbeappliedforamixtureofgenotypesofagivenspecies. Overall, thisstepisbasedona multi-traitselection approachand, thus,needs toconsider correlations amongthe traits ofinterest, notably between agronomic andinteraction traits. Severaltypesofcorrelationcanbeencountered,including:(i)Ifagronomicandinteractiontraits aregeneticallyindependent,thesetwodifferenttraitscanbeindependentlyselected(selection ononetraitwithoutcorrelativeresponseoftheother,andpossiblesimultaneousimprovementof both);and(ii)ifagronomicandinteractiontraitsaregeneticallycorrelated,selectionononetrait resultsinacorrelativeresponseoftheother.Ifthecorrelationcanbebrokenusingexisting breeding tools, particularly genetic andchromosome shuffling, selection of agronomic and interactiontraitscouldbedoneseparately.Bycontrast,ifthecorrelationisstrong,especiallyif pleiotropyisinvolved,simultaneousimprovementappearsdifficult.Inthatcase,genetic recom-binationdrivenbybreedingconstraints,suchasindexselection[87,88],canbeused.Thishas beenachievedinmanysituationsbyplantbreeding,suchasthesimultaneousimprovementof yieldandearlinessinmaizeandofforageyieldandseedyieldinforagegrasses.Theprincipleof

indexselectionisamulti-traitselectionaccordingtothevalueofanintegratedindex;thatis,a linearcombination oftheestimated breeding valuesofcandidate traitsbeing selected. The coefficientsoftheindexaredeterminedusingaconstraintsystembasedonexpectationsof geneticgains.

StepTwo(AssemblyStep)

Thisstepreliesonapplyingassemblyrulesfromecologytobuildinselectedgeneticpoolson thebasisoftheconvergencevaluesofagronomictraitsandthedivergencevaluesofthemajor interactiontraits. To evaluate thedegree ofdiversity required for optimalfunctioning ofthe mixture,process-basedmodelscanbeusedtotestandvalidatetherangeandvarianceofthe interactiontraits.Anexampleofthismightbeindividual-basedmodels[89]thataccountfor relationsbetweena genotype,itsenvironment, anditsbioticneighborsto developavirtual platformfortheoptimizationofassemblagesofgenotypesandspecies.Syntheticvarietiescan becreatedwhendealingwithauto-incompatiblespecies.Inthatcase,thissecondstepofour novelschemacanbeavoidedandreplacedbyaselectionontraitvarianceinstepone.Toreach thatgoal,wecanapplyadditionalconstraintstomaintainenoughgeneticvarianceofinteraction traitsintheconstraint systembasedonexpectationsofgenetic gains.Thisimproved index selectionmethod willenablebreeders todeal withthe trade-offbetweenselection towards certaintraitmeansandmaintenanceofdiversityforothertraitswithinagivenspecies.

ConcludingRemarks

Theproposedframeworkforplantbreedersisbasedoninsightsgainedfromecologicaltheory. Bothbreedingtoolsandmodelingapproachescanbeusedtohelpavoidtheinherenttrade-offs betweenagronomicandinteractiontraitsandtodeterminethedegreeoftraitdiversityrequired tomaintainsustainableproduction(seeOutstandingQuestions).Thisplant-breedingframework enables ideomixesto be created that may beused as the reference mixtures required by agroecology.

Acknowledgments

WethankJean-PaulSampouxandPhilippeBarreforhelpfuldiscussions.Wearegratefultoreviewersforconstructive commentsonearlierversionsofthismanuscript.ThisworkwasfundedbytheAgenceNationaldelaRecherche(ANR), France(PRAISE,ANR-13-BIOADAP-0015).C.V.wassupportedbytheEuropeanResearchCouncil(ERC)StartingGrant Project‘Ecophysiologicalandbiophysicalconstraintsondomesticationincropplants’(Grant ERC-StG-2014-639706-CONSTRAINTS).

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