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What Has Natural Variation Taught Us about Plant Development, Physiology, and Adaptation?

Carlos Alonso-Blanco, Mark G.M. Aarts, Leonie Bentsink, Joost J.B. Keurentjes, Matthieu Reymond, Dick Vreugdenhil, Maarten Koornneef
Carlos Alonso-Blanco
aCentro Nacional de Biotecnología, Consejo Superior de Investigaciones Científicas, Departamento de Genética Molecular de Plantas, Cantoblanco 28049 Madrid, Spain
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Mark G.M. Aarts
bLaboratory of Genetics, Wageningen University, 6700 AH Wageningen, The Netherlands
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Leonie Bentsink
cMolecular Plant Physiology Group, Institute of Environmental Biology, Utrecht University, 3584 CH Utrecht, The Netherlands
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Joost J.B. Keurentjes
bLaboratory of Genetics, Wageningen University, 6700 AH Wageningen, The Netherlands
dLaboratory of Plant Physiology, Wageningen University, 6700 AR, Wageningen, The Netherlands
eCentre for Biosystems Genomics, 6708 PB Wageningen,The Netherlands
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Matthieu Reymond
fDepartment of Plant Breeding and Genetics, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany
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Dick Vreugdenhil
dLaboratory of Plant Physiology, Wageningen University, 6700 AR, Wageningen, The Netherlands
eCentre for Biosystems Genomics, 6708 PB Wageningen,The Netherlands
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Maarten Koornneef
bLaboratory of Genetics, Wageningen University, 6700 AH Wageningen, The Netherlands
fDepartment of Plant Breeding and Genetics, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany
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Published July 2009. DOI: https://doi.org/10.1105/tpc.109.068114

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    Figure 1.

    Gene Networks Involved in Natural Variation for Flowering Responses to Vernalization and Photoperiod signals in A. thaliana, Wheat, and Rice.

    Diagrams do not represent full molecular models of flowering regulation, but they show gene network components and branches known to contribute to the natural intraspecific variation existing in these species. Yellow color represents genes that contribute to the variation in a single species, which do not present known homologous genes contributing to natural variation in other species. Green color depicts homologous genes that contribute to the variation in several species. Blue and purple indicate genes accounting for the variation in one species, which show homologous protein domains with genes contributing to the variation in another species. Given their large functional homology, CO, FT, and AP1 homologs of the three species are included in the three diagrams, with small circles depicting genes that do not contribute to natural variation. See text for further details.

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    Table 1.

    Genes and Funtional Polymorphisms Involved in Natural Variation for Different Traits and Species

    Functional Nucleotide PolymorphismAllelic Dysfunction
    Plant SpeciesLocus/GenePhenotypic EffectsMolecular FunctionGene PositionMutationReferences
    A. thalianaDOG1Seed dormancy, sugar sensingUnknownPromoterUnknownMEBentsink et al. (2006)
    Thale cressFRIFloweringUnknownPromoter, codingIns, Del, nonsense SubsTP, MEJohanson et al. (2000); Shindo et al. (2005)
    FRL1FloweringFRI-likeCodingNonsense SubsTPSchläppi (2006)
    FRL2FloweringFRI-likeCodingMissense SubsAPSchläppi (2006)
    FLCFloweringMADS TFIntron, codingTE insertion, nonsense SubsME, TPMichaels et al. (2003); Werner et al. (2005a)
    FLW1/FLMFloweringMADS TFPromoter + codingGene DelNull expressionWerner et al. (2005b)
    ART1/HUA2Flowering, shoot morphologyRNA processing factorCodingNonsense and missense SubsTP, APDoyle et al. (2005); Wang et al. (2007)
    EDI/CRY2Flowering, seedling growth, fruit sizePhotoreceptorCodingMissense SubsAPEl-Assal et al. (2001, 2004)
    PHYDFlowering, seedling growthPhotoreceptorCodingDelTPAukerman et al. (1997)
    PHYCFlowering, seedling growthPhotoreceptorCodingNonsense SubsTPBalasubramanian et al. (2006)
    PHYASeedling growthPhotoreceptorCodingMissense SubsAPMaloof et al. (2001)
    PHYBSeedling growthPhotoreceptorCodingMissense SubsAPFiliault et al. (2008)
    TZP/Light5Seedling growthZn knuckle proteinCodingInsTPLoudet et al. (2008)
    CALFlower morphologyMADS TFCodingMissense SubsAPKempin et al. (1995)
    IIL1Leaf morphologyLeu biosynthesis enzymeIntronIns, DelMESureshkumar et al. (2009)
    GL1Trichome formationMyb TFCodingDelMEHauser et al. (2001)
    PUB8Self-incompatibilityU box proteinPromoterUnknownMELiu et al. (2007)
    MUM2Seed mucilageGalactosidaseCodingDelMEMacquet et al. (2007)
    BRXRoot growthNovel TFCodingNonsense SubsTPMouchel et al. (2004)
    LPR1Root growth response to PMulticopper oxidasePromoterDelMESvistoonoff et al. (2007)
    INVSugar composition, root growthInvertaseUnknownUnknownUnknownSergeeva et al. (2006)
    Small effect QTLBiomass accumulationProtein kinaseUnknownUnknownUnknownKroyman and Mitchell-Olds (2005)
    DM1Hybrid incompatibility, disease resistanceNB-LRR proteinsPromoter + codingNonsense Subs, DelAPBomblies et al. (2007)
    QTL3Hybrid incompatibility, disease resistanceNB-LRR proteinsUnknownUnknownUnknownAlcázar et al. (2009)
    LD1. 1Genetic incompatiblity, embryogenesisHis biosynthesis enzymePromoter, codingNonsense SubsME, TPBikard et al. (2009)
    LD1.5Genetic incompatiblity, embryogenesisHis biosynthesis enzymePromoter + codingGene DelNull expressionBikard et al. (2009)
    APR2Sulfate accumulationSulfate reductaseCodingNonsense SubsAPLoudet et al. (2007)
    MOT1Mo accumulationSulfate transporterPromoterDelMEBaxter et al. (2008)
    HMA5Cu toxicityCu ATPase transporterCodingMissense SubsAPKobayashi et al. (2008)
    HKT1Na accumulationNa+ transporterPromoterDelMERus et al. (2006)
    A. lyrataFRIFloweringFRI-likeCodingIndelAPKuittinen et al. (2008)
    B. rapaBrFLC1FloweringMADS TFUnknownUnknownUnknownKole et al. (2001)
    TurnipBrFLC2FloweringMADS TFUnknownUnknownUnknownSchranz et al. (2002)
    S. lycopersicumSUNFruit shapeIQ67 domain proteinCoding + promotorGene duplicationMEXiao et al. (2008)
    TomatoOVATEFruit shapeNuclear proteinCodingNonsense SubsTPCong et al. (2002)
    FASFruit shapeYabby TFIntronInsMECong et al. (2008)
    Fw2.2Fruit sizeCell cycle controlPromoterSubs, indelMEFrary et al. (2000)
    Sw4. 1Seed sizeTransporterUnknownUnknownUnknownOrsi and Tanksley (2009)
    Brix9-2-5/LIN5Fruit sugar contentInvertaseCodingMissense SubsAPFridman et al. (2004)
    CnrFruit ripeningSBP TFPromoterDNA methylationMEManning et al. (2006)
    Pisum sativumLF/PsTFL1cFloweringTFL1-like proteinPromoter, codingGene DelNull expressionFoucher et al. (2003)
    PeaRSeed composition and morphologyStarch branching enzymeCodingTE insertionTP, MEBhattacharyya et al. (1990)
    Lynaria vulgarisLcycFlower simetryTCP TFPromoter + codingDNA methylationMECubas et al. (1999)
    Toadflax
    T. aestivumVRN1FloweringAP1-like MADS TFPromoter, intronDel, InsMEYan et al. (2003)
    Bread wheatVRN3FloweringFT-like proteinPromoterTE insertionMEYan et al. (2006)
    QSeed free-thressingAP2-like TFCodingMissense SubsAPSimons et al. (2006)
    RhtB1, RhtD1Plant and leaf sizeGAI-like proteinCodingNonsense SubsTPPeng et al. (1999)
    Gpc-B1/NAM-B1Senescence; Zn, Fe, and protein contentNAC TFCodingDel, gen DelTPUauy et al. (2006)
    Triticum monococumVRN1FloweringAP1-like MADS TFPromoterDelMEYan et al. (2003)
    Einkorn wheatVRN2FloweringCCT domain proteinPromoter, codingMissense SubsAPYan et al. (2004a)
    H. vulgareVRN2FloweringCCT domain proteinPromoter + codingGene DelNull expressionYan et al. (2004a)
    BarleyVRN3FloweringFT-like proteinIntronSubsMEYan et al. (2006)
    Ppd1FloweringResponse regulatorCodingMissense SubsAPTurner et al. (2005)
    NudSeed free-threshingERF TFPromoter + codingGene DelNull expressionTaketa et al. (2008)
    Vrs1Seed number, ear morphologyHD TFCodingInsTPKomatsuda et al. (2007)
    Bot1Boron toxicity toleranceBoron efflux transporterPromoter + codingGene duplicationMESutton et al. (2007)
    O. sativaqLTG3GerminationUnknownCodingDelMEFujino et al. (2008)
    RiceRcGermination, seed colorbHLH TFCodingDelTPSweeney et al. (2006)
    Hd1FloweringCO-like TFCodingDel, TE insertionTP, MEYano et al. (2000); Doi et al. (2004)
    Hd3aFloweringFT-like proteinUnknownUnknownMEKojima et al. (2002)
    Hd6FloweringProtein kinase CK2CodingNonsense SubsTPTakahashi et al. (2001)
    Ehd1FloweringResponse regulatorCodingMissense SubsAPDoi et al. (2004)
    Ghd7Flowering, plant height, seed yieldCCT domain proteinCodingGene Del, nonsense SubsNull expressionXue et al. (2008)
    sh4ShatteringMyb TFCodingMissense SubsAPLi et al. (2006)
    qSH1ShatteringHD TFPromoterMissense SubsMEKonishi et al. (2006)
    qSW5Seed sizeUnknownCoding, promoterDelMEShomura et al. (2008)
    GW2Seed sizeRING proteinCodingDelTPSong et al. (2007)
    GS3Seed sizeUnknownCodingMissense SubsTPFan et al. (2006)
    Gn1aSeed numberCK oxidase/dehydrogenasePromoterDelMEAshikari et al. (2005)
    WxSeed starch compositionStarch biosynthesis enzymeIntronSplice site SubsTPIsshiki et al. (1998)
    SKC1Salt toleranceHKT transporterCodingMissense SubsAPRen et al. (2005)
    Z. maysVgt1FloweringAP2-like TFPromoter enhancerTE insertion, indelMESalvi et al. (2007)
    Maizetb 1Inflorescence architectureTCP TFPromoter enhancerUnknownMEDoebley et al. (1997)
    tga1Seed morphologySBP TFCodingMissense SubsAPWang et al. (2005)
    WxStarch compositionStarch biosynthesis enzymePromoter, intron, codingTE insertionMEVaragona et al. (1992)
    • TF: Transcription factor; TE: Transposable element; Subs: substitution; Ins: insertion; Del: deletion; TP: truncated protein; AP: altered protein; ME: Misexpression

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What Has Natural Variation Taught Us about Plant Development, Physiology, and Adaptation?
Carlos Alonso-Blanco, Mark G.M. Aarts, Leonie Bentsink, Joost J.B. Keurentjes, Matthieu Reymond, Dick Vreugdenhil, Maarten Koornneef
The Plant Cell Jul 2009, 21 (7) 1877-1896; DOI: 10.1105/tpc.109.068114

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What Has Natural Variation Taught Us about Plant Development, Physiology, and Adaptation?
Carlos Alonso-Blanco, Mark G.M. Aarts, Leonie Bentsink, Joost J.B. Keurentjes, Matthieu Reymond, Dick Vreugdenhil, Maarten Koornneef
The Plant Cell Jul 2009, 21 (7) 1877-1896; DOI: 10.1105/tpc.109.068114
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  • Article
    • Abstract
    • INTRODUCTION
    • DEVELOPMENTAL PROCESSES
    • VEGETATIVE GROWTH AND PHYSIOLOGY
    • REVEALING THE VARIOUS LEVELS OF PHENOTYPIC REGULATION: NATURAL VARIATION FOR MOLECULAR TRAITS
    • MOLECULAR TARGETS OF SELECTION FOR PLANT ADAPTATION: CURRENT AND FUTURE PROSPECTS
    • Acknowledgments
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The Plant Cell Online: 21 (7)
The Plant Cell
Vol. 21, Issue 7
July 2009
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