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From Natural Variation to Regulatory Networks

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From Natural Variation to Regulatory Networks ȱ ȱ ȱ GeneticalȱGenomicsȱinȱArabidopsis:ȱ fromȱnaturalȱvariationȱtoȱregulatoryȱnetworksȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ JoostȱKeurentjesȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ Promotoren:ȱȱ ȱ Prof.ȱdr.ȱir.ȱM.ȱKoornneefȱ PersoonlijkȱhoogleraarȱbijȱhetȱLaboratoriumȱvoorȱ Erfelijkheidsleer,ȱWageningenȱUniversiteitȱ ȱ Prof.ȱdr.ȱL.H.W.ȱvanȱderȱPlasȱ HoogleraarȱinȱdeȱPlantenfysiologie,ȱWageningenȱ Universiteitȱ ȱ Copromotor:ȱȱ ȱ Dr.ȱD.ȱVreugdenhilȱ UniversitairȱhoofddocentȱbijȱhetȱLaboratoriumȱvoorȱ Plantenfysiologie,ȱWageningenȱUniversiteitȱ ȱ Promotiecommissie:ȱȱ Prof.ȱdr.ȱW.J.ȱStiekema,ȱWageningenȱUniversiteitȱ Prof.ȱdr.ȱR.G.F.ȱVisser,ȱWageningenȱUniversiteitȱ Prof.ȱdr.ȱJ.C.M.ȱSmeekens,ȱUniversiteitȱUtrechtȱ Prof.ȱdr.ȱM.ȱStitt,ȱMaxȱPlanckȱInstituutȱvoorȱ MoleculaireȱPlantenfysiologie,ȱGolm,ȱDuitslandȱ ȱ ȱ DitȱonderzoekȱisȱuitgevoerdȱbinnenȱdeȱonderzoekschoolȱvoorȱExperimenteleȱ Plantwetenschappen.ȱ ȱ ȱ ȱ ȱ JoostȱKeurentjesȱ ȱ ȱ ȱ ȱ ȱ ȱ GeneticalȱGenomicsȱinȱArabidopsis:ȱ fromȱnaturalȱvariationȱtoȱregulatoryȱnetworksȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ Proefschriftȱ terȱverkrijgingȱvanȱdeȱgraadȱvanȱdoctorȱ opȱgezagȱvanȱdeȱrectorȱmagnificusȱ vanȱWageningenȱUniversiteit,ȱ Prof.ȱdr.ȱM.J.ȱKropff,ȱ inȱhetȱopenbaarȱteȱverdedigenȱ opȱvrijdagȱ7ȱseptemberȱ2007ȱ desȱnamiddagsȱteȱ13:30ȱuurȱinȱdeȱAulaȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ JoostȱJ.B.ȱKeurentjesȱ ȱ GeneticalȱGenomicsȱinȱArabidopsis:ȱfromȱnaturalȱvariationȱtoȱ regulatoryȱnetworksȱ(2007)ȱ ȱ PhDȱthesis,ȱWageningenȱUniversity,ȱWageningen,ȱTheȱNetherlands.ȱ Withȱreferencesȱ–ȱwithȱsummariesȱinȱEnglishȱandȱDutch.ȱ ȱ ISBNȱ978Ȭ90Ȭ8504Ȭ704Ȭ9 CONTENTSȱ ȱ Chapterȱ1ȱ Generalȱintroductionȱ ȱ ȱ ȱ ȱ ȱ ȱȱȱȱ1ȱ ȱ Chapterȱ2ȱ DevelopmentȱofȱaȱNearȬIsogenicȱLineȱpopulationȱofȱȱ ȱȱ17ȱ Arabidopsisȱthalianaȱandȱcomparisonȱofȱmappingȱpowerȱ withȱaȱRecombinantȱInbredȱLineȱpopulationȱ ȱ Chapterȱ3ȱ RegulatoryȱnetworkȱconstructionȱinȱArabidopsisȱbyȱusingȱȱȱ47ȱ genomeȬwideȱgeneȱexpressionȱquantitativeȱtraitȱlociȱ ȱ Chapterȱ4ȱ Theȱgeneticsȱofȱplantȱmetabolismȱȱȱȱȱȱ73ȱ ȱ Chapterȱ5ȱ Integrativeȱanalysesȱofȱgeneticȱvariationȱinȱenzymeȱȱ ȱȱ99ȱ activitiesȱofȱprimaryȱcarbohydrateȱmetabolismȱrevealȱ distinctȱmodesȱofȱregulationȱinȱArabidopsisȱthalianaȱ ȱ Chapterȱ6ȱ Generalȱdiscussionȱȱȱȱȱȱ133ȱ ȱ Summaryȱȱȱȱȱȱȱ143ȱ ȱ Samenvattingȱȱȱȱȱȱȱ147ȱ ȱ Publicationsȱȱȱȱȱȱȱ151ȱ ȱ Curriculumȱvitaeȱȱȱȱȱȱ155ȱ ȱ Nawoordȱȱȱȱȱȱȱ156ȱ ȱ EducationȱStatementȱȱȱȱȱȱ159ȱ ȱ Chapterȱ1ȱ ȱ ȱ Generalȱintroductionȱ ȱ ȱ Naturalȱvariationȱandȱquantitativeȱtraitsȱ Forȱ mostȱ organismsȱ variationȱ betweenȱ individualsȱ canȱ beȱ observedȱ inȱ nature.ȱ Plantsȱareȱnoȱexceptionȱtoȱthisȱandȱnaturallyȱoccurringȱvariationȱcanȱbeȱobservedȱ betweenȱ andȱ withinȱ species.ȱ Althoughȱ partȱ ofȱ theȱ withinȬspeciesȱ variationȱ observedȱinȱnatureȱcanȱbeȱattributedȱtoȱenvironmentalȱinfluences,ȱgeneticȱvariationȱ canȱbeȱobservedȱwhenȱplantsȱofȱdifferentȱoriginsȱareȱgrownȱtogetherȱinȱtheȱsameȱ environmentȱ (Nordborgȱ etȱ al.,ȱ 2005).ȱ Theȱ contributionȱ ofȱ geneticȱ factorsȱ toȱ theȱ totallyȱ observedȱ variationȱ betweenȱ differentȱ genotypesȱ isȱ oftenȱ expressedȱ asȱ theȱ heritabilityȱofȱaȱtrait.ȱ Naturalȱ variationȱ exhibitedȱ byȱ genotypicallyȱ differentȱ accessionsȱ canȱ beȱ classifiedȱ asȱ qualitativeȱ orȱ quantitative.ȱ Qualitativeȱ traitsȱ areȱ characterizedȱ byȱ distinctȱ phenotypicȱ classes,ȱ e.g.ȱ presenceȱ orȱ absenceȱ ofȱ aȱ property,ȱ oftenȱ aȱ resultȱ fromȱ geneticȱ differencesȱ atȱ singleȱ genes.ȱ Suchȱ traitsȱ canȱ relativelyȱ easilyȱ beȱ dissectedȱ geneticallyȱ dueȱ toȱ theirȱ clearȱ segregationȱ patternȱ inȱ theȱ progenyȱ ofȱ crosses.ȱ Quantitativeȱ traitsȱ onȱ theȱ otherȱ hand,ȱ oftenȱ displayȱ aȱ moreȱ continuousȱ variationȱ inȱ phenotypesȱ dueȱ toȱ aȱ multiplicityȱ ofȱ genesȱ involvedȱ andȱ aȱ relativelyȱ largeȱ effectȱ ofȱ environmentalȱ factorsȱ onȱ theȱ expressionȱ ofȱ theȱ trait.ȱ Becauseȱ differentȱ genesȱ canȱ contributeȱ positivelyȱ orȱ negativelyȱ toȱ aȱ quantifiableȱ trait,ȱ recombinationȱofȱgenesȱresultsȱinȱaȱlargeȱnumberȱofȱphenotypicȱclassesȱwhichȱcanȱ notȱ unambiguouslyȱ beȱ associatedȱ withȱ genotypicȱ classesȱ (Kearseyȱ etȱ al.,ȱ 2003;ȱ WeigelȱandȱNordborg,ȱ2005;ȱHolland,ȱ2007).ȱTheȱcomplexityȱofȱquantitativeȱtraitsȱisȱ furtherȱenhancedȱbyȱtheȱpresenceȱofȱepistaticȱinteractionsȱandȱinteractionsȱbetweenȱ genesȱ andȱ theȱ environmentȱ (Carlborgȱ andȱ Haley,ȱ 2004;ȱ Kroymannȱ andȱ MitchellȬ Olds,ȱ2005).ȱ Althoughȱmuchȱmoreȱdifficultȱtoȱdissect,ȱquantitativeȱvariationȱisȱfoundȱforȱ manyȱagronomicalȱimportantȱtraitsȱlikeȱbiomassȱformation,ȱplantȱheight,ȱfloweringȱ time,ȱ reproductiveȱ yieldȱ andȱ seedȱ dormancyȱ (Koornneefȱ etȱ al.,ȱ 2004;ȱ RossȬIbarra,ȱ 2005;ȱ Ashikariȱ andȱ Matsuoka,ȱ 2006;ȱ Semelȱ etȱ al.,ȱ 2006;ȱ Zhaoȱ etȱ al.,ȱ 2006).ȱ Furthermore,ȱ quantitativeȱ naturalȱ variationȱ controlsȱ adaptiveȱ strategiesȱ toȱ copeȱ withȱ bioticȱ andȱ abioticȱ influencesȱ andȱ itsȱ understandingȱ canȱ provideȱ insightȱ inȱ ecologicalȱmechanismsȱandȱtheȱevolutionaryȱhistoryȱofȱplantsȱ(Tonsorȱetȱal.,ȱ2005;ȱ MitchellȬOldsȱandȱSchmitt,ȱ2006).ȱȱ 1ȱ Chapterȱ1ȱ Arabidopsisȱthalianaȱasȱaȱmodelȱplantȱ Theȱstudyȱofȱquantitativeȱtraitsȱisȱoftenȱcontrastedȱwithȱtheȱanalysisȱofȱqualitativeȱ traits,ȱwhichȱareȱmostlyȱrepresentedȱbyȱsingleȱgeneȱmutantsȱorȱsingleȱgeneȱnaturalȱ variants.ȱForȱtheȱstudyȱofȱsuchȱsingleȱgenesȱArabidopsisȱthalianaȱhasȱprovenȱtoȱbeȱaȱ veryȱefficientȱmodelȱplantȱbecauseȱofȱaȱnumberȱofȱbiologicalȱpropertiesȱthatȱmakeȱ geneticȱ analysesȱ veryȱ efficientȱ (Somervilleȱ andȱ Koornneef,ȱ 2002).ȱ Althoughȱ itȱ isȱ selfȬfertilizingȱitȱcanȱeasilyȱbeȱoutȬcrossedȱandȱitȱcombinesȱshortȱgenerationȱtimesȱ withȱ highȱ reproductiveȱ yield.ȱ Moreover,ȱ itȱ containsȱ aȱ fullyȱ sequencedȱ smallȱ genomeȱ(120ȱMbp)ȱmadeȱupȱofȱonlyȱfiveȱchromosomesȱandȱapproximatelyȱ30,000ȱ genesȱ(TheȱArabidopsisȱGenomeȱInitiative,ȱ2000).ȱTheȱaccumulationȱofȱknowledge,ȱ biologicalȱresourcesȱandȱavailableȱmolecularȱtoolsȱaddsȱupȱtoȱtheȱattractivenessȱofȱ Arabidopsisȱasȱaȱmodelȱsystemȱ(AlonsoȱandȱEcker,ȱ2006).ȱ Theseȱ advantagesȱ alsoȱ makeȱ Arabidopsisȱ veryȱ suitableȱ forȱ theȱ geneticȱ analysisȱ ofȱ naturalȱ variation.ȱ Theȱ plantȱ showsȱ aȱ broadȱ globalȱ distributionȱ throughoutȱ theȱ northernȱ hemisphereȱ atȱ differentȱ continents,ȱ includingȱ America,ȱ Africa,ȱ Europeȱ andȱ Asiaȱ (Schmidȱ etȱ al.,ȱ 2006).ȱ Moreoverȱ itȱ isȱ foundȱ atȱ differentȱ latitudesȱandȱaltitudesȱrangingȱfromȱScandinavianȱseaȱlevelȱtoȱhighȱupȱinȱtheȱAsianȱ Himalayas.ȱ Atȱ manyȱ locations,ȱ accessionsȱ orȱ ecotypes,ȱ haveȱ beenȱ collectedȱ displayingȱ aȱ broadȱ spectrumȱ ofȱ naturalȱ variationȱ forȱ numerousȱ traitsȱ (AlonsoȬ BlancoȱandȱKoornneef,ȱ2000;ȱKoornneefȱetȱal.,ȱ2004).ȱManyȱofȱthoseȱaccessionsȱareȱ depositedȱtoȱstockȱcentersȱmakingȱthemȱpubliclyȱavailableȱforȱgeneticȱanalyses.ȱ ȱ Geneticȱanalysisȱofȱquantitativeȱtraitsȱ Despiteȱtheȱcomplexityȱinȱgeneticȱregulationȱofȱquantitativeȱtraitsȱmuchȱprogressȱ hasȱ beenȱ madeȱ overȱ theȱ pastȱ decadesȱ inȱ dissectingȱ theseȱ traitsȱ byȱ theȱ useȱ ofȱ molecularȱ markers.ȱ Theȱ increasingȱ easeȱ byȱ whichȱ molecularȱ markersȱ canȱ beȱ generatedȱ (Borevitzȱ andȱ Chory,ȱ 2004)ȱ inȱ combinationȱ withȱ theȱ applicationȱ ofȱ sophisticatedȱ mappingȱ methodsȱ (Jansen,ȱ 1993)ȱ hasȱ ledȱ toȱ aȱ strongȱ interestȱ inȱ theȱ useȱ ofȱ naturalȱ variationȱ forȱ studyingȱ quantitativeȱ traitsȱ (Slate,ȱ 2005).ȱ Mutantȱ screens,ȱoftenȱdirectedȱtoȱaȱspecificȱtrait,ȱandȱtheȱsubsequentȱmappingȱandȱcloningȱ ofȱtheȱaffectedȱgene,ȱhaveȱbeenȱaȱveryȱeffectiveȱstrategyȱtoȱanalyzeȱtheȱfunctionȱofȱ genesȱ inȱ Arabidopsisȱ (Meinkeȱ etȱ al.,ȱ 2003).ȱ However,ȱ specificȱ advantagesȱ areȱ associatedȱwithȱtheȱstudyȱofȱmultipleȱnaturalȱperturbationsȱinȱtheȱsameȱmappingȱ population.ȱ Thisȱ allowsȱ forȱ theȱ analysisȱ ofȱ anȱ almostȱ infiniteȱ numberȱ ofȱ traitsȱ (Doerge,ȱ 2002).ȱ Forȱ thisȱ typeȱ ofȱ studyȱ soȬcalledȱ immortalȱ mappingȱ populations,ȱ consistingȱinȱmostȱcasesȱofȱhomozygousȱgenotypesȱthatȱcanȱbeȱtestedȱinȱreplicatesȱ andȱinȱdifferentȱexperiments,ȱhaveȱprovenȱveryȱuseful.ȱ Althoughȱ variousȱ typesȱ ofȱ suchȱ mappingȱ populationsȱ haveȱ beenȱ developedȱforȱaȱvarietyȱofȱspeciesȱ(EshedȱandȱZamir,ȱ1995;ȱRaeȱetȱal.,ȱ1999;ȱYoonȱetȱ 2ȱ Generalȱintroductionȱ al.,ȱ2006),ȱtheȱrelativeȱeaseȱofȱgeneratingȱrecombinantȱinbredȱlinesȱ(RILs)ȱhasȱledȱtoȱ theirȱfavorableȱuseȱforȱquantitativeȱtraitȱlocusȱ(QTL)ȱanalysisȱinȱArabidopsisȱandȱ manyȱ otherȱ plantsȱȱ(Jansen,ȱ 2003b).ȱ RILsȱ areȱ producedȱ byȱ crossingȱ twoȱ distinctȱ genotypesȱandȱusingȱsingleȱseedȱdescentȱpropagationȱofȱtheȱinbredȱlinesȱobtainedȱ byȱ selfingȱ aȱ randomȱ setȱ ofȱ F2ȱ individuals.ȱȱWhileȱ theȱ accuracyȱ ofȱ QTLȱ mappingȱ dependsȱ onȱ statisticalȱ factorsȱ suchȱ asȱ theȱ sizeȱ ofȱ theȱ mappingȱ population,ȱ itȱ hasȱ beenȱ shownȱ toȱ beȱ quiteȱ accurateȱ inȱ manyȱ casesȱ (Price,ȱ 2006).ȱ However,ȱ thereȱ isȱ oftenȱ stillȱ aȱ needȱ forȱ confirmationȱ andȱ furtherȱ fineȱ mappingȱ (Paranȱ andȱ Zamir,ȱ 2003;ȱ Weigelȱ andȱ Nordborg,ȱ 2005).ȱ Forȱ theseȱ aspects,ȱ whichȱ areȱ theȱ basisȱ ofȱ theȱ cloningȱ ofȱ genesȱ underlyingȱ QTLs,ȱ nearȱ isogenicȱ linesȱ (NILs)ȱ areȱ oftenȱ usedȱ toȱ isolateȱaȱQTL.ȱAȱsetȱofȱNILsȱconsistsȱofȱlinesȱwithȱidenticalȱgeneticȱbackgroundȱbutȱ differingȱinȱgenotypeȱatȱtheȱpositionȱofȱaȱlimitedȱnumberȱofȱloci.ȱNILsȱareȱgenerallyȱ constructedȱ byȱ introgressingȱ aȱ donorȱ accessionȱ intoȱ theȱ geneticȱ backgroundȱ ofȱ anotherȱ accessionȱ byȱ crossingȱ andȱ repeatedȱ backȬcrossingȱ withȱ theȱ recurrentȱ accession.ȱNILsȱallowȱstudyingȱtheȱeffectȱofȱMendelizedȱQTLsȱandȱcanȱrefineȱtheȱ positionȱofȱaȱQTLȱbyȱvaryingȱpositionȱandȱsizeȱofȱintrogressions.ȱ Despiteȱ theȱ factȱ thatȱ RILȱ populationsȱ haveȱ beenȱ developedȱ
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