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Epistasis and genotype-environment interaction for quantitative trait loci affecting flowering time in Arabidopsis thaliana

  • Chapter
Genetics of Adaptation

Part of the book series: Georgia Genetics Review III ((GEGR,volume 3))

Abstract

A major goal of evolutionary biology is to understand the genetic architecture of the complex quantitative traits that may lead to adaptations in natural populations. Of particular relevance is the evaluation of the frequency and magnitude of epistasis (gene-gene and gene-environment interaction) as it plays a controversial role in models of adaptation within and among populations. Here, we explore the genetic basis of flowering time in Arabidopsis thaliana using a series of quantitative trait loci (QTL) mapping experiments with two recombinant inbred line (RIL) mapping populations [Columbia (Col) × Landsberg erecta (Ler), Ler × Cape Verde Islands (Cvi)]. We focus on the response of RILs to a series of environmental conditions including drought stress, leaf damage, and apical damage. These data were explicitly evaluated for the presence of epistasis using Bayesian based multiple-QTL genome scans. Overall, we mapped fourteen QTL affecting flowering time. We detected two significant QTL-QTL interactions and several QTL-environment interactions for flowering time in the Ler × Cvi population. QTL-environment interactions were due to environmentally induced changes in the magnitude of QTL effects and their interactions across environments — we did not detect antagonistic pleiotropy. We found no evidence for QTL interactions in the Ler × Col population. We evaluate these results in the context of several other studies of flowering time in Arabidopsis thaliana and adaptive evolution in natural populations.

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References

  • Alonso-Blanco, C., S.E.-D. El-Assal, G. Coupland & M. Koornneef, 1998a. Analysis of natural allelic variation at flowering time loci in the Landsberg erecta and Cape Verde Islands ecotypes of Arabidopsis thaliana. Genetics 149: 749–764.

    PubMed  Google Scholar 

  • Alonso-Blanco, C., A.J.M. Peeters, M. Koornneef, C. Lister, C. Dean, N. van den Bosch, J. Pot & M.T.R. Kuiper, 1998b. Development of an AFLP based linkage map of Ler, Col, and Cvi Arabidopsis thaliana ecotypes and construction of a Ler/Cvi recombinant inbred line population. Plant J. 14: 259–271.

    PubMed  Google Scholar 

  • Agrawal, A.F., E.D. Brodie & L.H. Riesberg, 2001. Possible consequences of genes of major effect: transient changes in the G-matrix. Genetica 112–113: 33–43.

    PubMed  Google Scholar 

  • Barton, N.H & M. Turelli, 1989. Evolutionary quantitative genetics: how little do we know? Ann. Rev. Genet. 23: 337 370.

    PubMed  Google Scholar 

  • Beavis, W.D., 1994. The power and deceit of QTL experiments: lessons from comparative QTL studies, pp. 255–266 in Proc. Corn and Sorghum Industry Research Conference. American Seed Trade Association, Washington DC, USA.

    Google Scholar 

  • Bradshaw, H.D., K.G. Otto, B.E. Frewen, J.K. Mackay & D.W. Schemske, 1998. Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). Genetics 149: 367–382.

    PubMed  Google Scholar 

  • Callahan, H.S. & M. Pigliucci, 2002. Shade induced plasticity and its ecological significance in wild populations of Arabidopsis thaliana. Ecology 83: 1965–1980.

    Google Scholar 

  • Cheverud, J.M. & E.J. Routman, 1995. Epistasis and its contribution to genetic variance components. Genetics 139:1455–1461.

    PubMed  Google Scholar 

  • Cheverud, J.M., E.J. Routman & D.J. Irschick, 1997. Pleiotropic effects of individual gene loci on mandibular morphology. Evolution 51: 2006–2016.

    Google Scholar 

  • Cheverud, J.M., 2000. Detecting epistasis among quantitative trait loci, pp. 58–81 in Epistasis and the Evolutionary Process, edited by Wolf, J.B., E.D. Brodie III and M.J. Wade. Oxford University Press, New York.

    Google Scholar 

  • Clarke, J.H., R. Mithen, J.K.M. Brown & C. Dean, 1995. QTL analysis of flowering time in Arabidopsis thaliana. Mol. Gen. Genet 248: 278–286.

    PubMed  Google Scholar 

  • Donohue, K., 2002. Germination timing influences natural selection on life-history characters in Arabidopsis thaliana. Ecology 83: 1006–1016.

    Google Scholar 

  • Dorn, L., E.H. Pyle & J. Schmitt, 2000. Plasticity to light cues and resources in Arabidopsis thaliana: testing for adaptive value and costs. Evolution 54: 1982–1994.

    PubMed  Google Scholar 

  • El-Assal, S.E-D, C. Alonso-Blanco, A.J.M. Peeters, V. Raz & M. Koornneef, 2001. A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nature Genetics 29: 435–440.

    PubMed  Google Scholar 

  • Falconer, D.S. & T.F.C. Mackay, 1996. Introduction to Quantitative Genetics. (4th Edition). Addison Wesley Longman, Harlow, Essex.

    Google Scholar 

  • Fenster, C.B., F.F. Galloway & L. Chao, 1997. Epistasis and its consequences for the evolution of natural populations. Trends Ecol. Evol. 12: 282–286.

    Google Scholar 

  • Fisher, R.A., 1930. The Genetical Theory of Natural Selection. Oxford University Press, Oxford.

    Google Scholar 

  • Fry, J.D., S.V. Nuzhdin, E.G. Pasyukova & T.F.C. Mackay, 1998. QTL mapping of genotype-environment interaction for fitness in Drosophila melanogaster. Genet. Research 71:133–141.

    Google Scholar 

  • Gurganus, M.C., J.D. Fry, S.V. Nushdin, E.G. Pasyukova, R.F. Lyman & T.F.C. Mackay, 1998. Genotype-environment interaction at quantitative trait loci affecting sensory bristle number in Drosophila melanogaster. Genetics 149:1883–1898.

    PubMed  Google Scholar 

  • Jansen, R.C., J.W. van Ooijen, P. Stam, C. Lister & C. Dean, 1995. Genotype-by-environment interaction in genetic mapping of multiple quantitative trait loci. Theor. Appl. Genet. 91: 33–37.

    Google Scholar 

  • Johanson, U., J. West, C. Lister, S. Micheals, R. Amasino & C. Dean, 2001. Molecular analysis of FRIGIDA a major determinant of natural variation in Arabidopsis flowering time. Science 290: 344–347.

    Google Scholar 

  • Juenger, T., M. Purugganan & T.F.C. Mackay, 2000. Quantitative trait loci for floral morphology in Arabidopsis thaliana. Genetics 156: 1379–1392.

    PubMed  Google Scholar 

  • Kim, S.-C. & L.H. Rieseberg, 1999. Genetic architecture of species differences in annual sunflowers: implications for adaptive trait introgression. Genetics 153: 965–977.

    PubMed  Google Scholar 

  • Koornneef, M., C. Alonso-Blanco, A.J.M. Peeters & W. Soppe, 1998. Genetic control of flowering time in Arabidopsis. Ann. Rev. Plant Phys. Plant Mol. Biol. 49: 345–370.

    Google Scholar 

  • Kowalski, S.P., T.-H. Lan, K.A. Feldmann & A.H. Paterson, 1994. QTL mapping of naturally-occurring variation in flowering time of Arabidopsis thaliana. Mol. Gen. Genet 245: 548–555.

    PubMed  Google Scholar 

  • Kuittinen, H., M.J. Sillanpaa & O. Savolainen, 1997. Genetic basis of adaptation: flowering time in Arabidopsis thaliana. Theor. Appl. Genet. 95: 573–583.

    Google Scholar 

  • Lande, R. 1979. Quantitative genetic analysis of multivariate evolution, applied to brain:body allometry. Evolution 33:402–416.

    Google Scholar 

  • Lande, R. & S. Arnold, 1983. The measurement of natural selection on correlated characters. Evolution 37: 1210–1226.

    Google Scholar 

  • Lander, E.S. & D. Botstein, 1989. Mapping Mendelian factors underlying quantitative traits using RFLP linage maps. Genetics 121: 185–199.

    PubMed  Google Scholar 

  • Lander, E., S. Green, P. Abrahamson, A. Barlow, M. Daley, S. Lincoln & L. Newburg, 1987. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181.

    Article  PubMed  Google Scholar 

  • Levy, Y.Y. & C. Dean, 1998. Control of flowering time. Curr. Opin. Plant Biol. 1: 49–54.

    PubMed  Google Scholar 

  • Lister, C. & C. Dean, 1993. Recombinant inbred lines for mapping RFPL and phenotypic markers in Arabidopsis thaliana. Plant J. 4: 745–750.

    Google Scholar 

  • Littel, R.C., G.A. Milliken, W.W. Stroup & R. D. Wolfinger, 1996. SAS System for Mixed Models. The SAS Institute, Cary, NC, USA.

    Google Scholar 

  • Long, A.D., S.L. Mullaney, L.A. Reid, J.D. Fry, C.H. Langley & T.F.C. Mackay, 1995. High resolution mapping of genetic factors affecting abdominal bristle number in Drosophila melanogaster. Genetics 139: 1273–1291.

    PubMed  Google Scholar 

  • Lynch, M. & B. Walsh, 1998. Genetics and Analysis of Quantitative Traits. Sinauer, Sunderland, MA, USA.

    Google Scholar 

  • Mackay, T.F.C., 1995. The genetic basis of quantitative variation: numbers of sensory bristles in Drosophila melanogaster as a model system. Trends Genet. 11: 464–470.

    PubMed  Google Scholar 

  • Michaels, S.D. & R.M. Amasino, 1999. Flowering locus C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11: 949–956.

    PubMed  Google Scholar 

  • Mitchell-Olds, T. & J.J. Rutledge, 1986. Quantitative genetics in natural plant populations: a review of the theory. Am. Nat. 127: 379–402.

    Google Scholar 

  • Mitchell-Olds, T., 1996. Genetic constraints on life-history evolution: quantitative trait loci influencing growth and flowering in Arabidopsis thaliana. Evolution 50: 140–145.

    Google Scholar 

  • Mauricio, R. & M. D. Rausher, 1997. Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 51: 1435–1441.

    Google Scholar 

  • Mitchell-Olds, T., 1996. Genetic constraints on life history evolution: quantitative-trait loci influencing growth and flowering in Arabidopsis thaliana. Evolution 50: 140–145.

    Google Scholar 

  • Napp-Zinn, K., 1985. Arabidopsis thaliana, pp. 492–503 in Handbook of Flowering, edited by H.A. Halvey. CRC Press, Boca Raton, Florida, USA.

    Google Scholar 

  • Orr, H.A. & J.A. Coyne, 1992. The genetics of adaptation: a reassessment. Amer. Natur. 140: 725–742.

    Google Scholar 

  • Orr, H.A., 1998. The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52: 935–949.

    Google Scholar 

  • Pigliucci, M. & E.T. Marlow, 2001. Differentiation for flowering time and phenotypic integration in Arabidopsis thaliana in response to season length and vernalization. Oecologia 127: 501–508.

    Google Scholar 

  • Routman, E. J. & J.M. Cheverud, 1997. Gene effects on a quantitative trait: two-locus epistatic effects measured at microsatellite markers and at estimated QTL. Evolution 51:1654–1662.

    Google Scholar 

  • Sanda, S.L. & R.M. Amasino, 1996. Interaction of FLC and late-flowering mutations in Arabidopsis thaliana. Mol. Gen. Genet. 251: 69–74.

    PubMed  Google Scholar 

  • Schemske, D.W. & H.D. Bradshaw, Jr., 1999. Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proc. Natl. Acad. Sci. USA 96: 11910–11915.

    PubMed  Google Scholar 

  • Scheiner, S.M. & H.S. Callahan, 1999. Measuring natural selection on phenotypic plasticity. Evolution 53: 1704–1713.

    Google Scholar 

  • Sen, S. & G. Churchill, 2001. A statistical framework for quantitative trait mapping. Genetics 159: 371–387.

    PubMed  Google Scholar 

  • Shook, D.R. & T.E. Johnson, 1999. Quantitative trait loci affecting survival and fertility related traits in Caenorhabditis elegans show genotype-environment interactions, pleiotropy, and epistasis. Genetics 153: 1233–1243.

    PubMed  Google Scholar 

  • Stratton, D.A., 1998. Reaction norm functions and QTL-environment interactions for flowering time in Arabidopsis thaliana. Heredity 81: 144–155.

    PubMed  Google Scholar 

  • Ungerer, M.C., S.S. Halldorsdottir, J.L. Modliszewski, T.F.C. Mackay & M.D. Purugganan, 2002. Quantitative trait loci for inflorescence development in Arabidopsis thaliana. Genetics 160: 1133–1151.

    PubMed  Google Scholar 

  • Via, S., 1987. Genetic constraints on the evolution of phenotypic plasticity, pp. 47–71 in Genetic Constraints on Adaptive Evolution, edited by V. Loeschke. Springer-Verlag, Berlin.

    Google Scholar 

  • Vieira, C., E.G. Pasyukova, Z.-B. Zeng, B. Hackett, R.F. Lyman & T.F.C. Mackay, 2000. Genotype-environment interaction for quantitative trait loci affecting life span in Drosophila melanogaster. Genetics 154: 213–227.

    PubMed  Google Scholar 

  • Wade, M., 1992. Sewall Wright: Gene interaction in the shifting balance theory, pp. 35–62 in Oxford Surveys in Evolutionary Biology, Vol. 8, edited by D. Futuyma & J. Antonovics. Oxford University Press, New York.

    Google Scholar 

  • Wade, M.J., 2000. Epistasis as a genetic constraint within populations and an accelerant of adaptive divergence among them, pp. 213–231 in Epistasis and the Evolutionary Process, edited by J.B. Wolf, E.D. Brodie III & M.J. Wade. Oxford University Press, Oxford, UK.

    Google Scholar 

  • Wade, M.J., 2001. Epistasis, complex traits, and mapping genes. Genetica 112–113: 59–69.

    PubMed  Google Scholar 

  • Weinig, C., M. Ungerer, L. Dorn, N. Kane, Y. Toyonaga, S.S. Halldorsdottir, T.F.C. Mackay, M.,D. Purugganan, & J. Schmitt, 2002. Novel loci control variation in reproductive timing in Arabidopsis thaliana in natural environments. Genetics 162: 1875–1884.

    PubMed  Google Scholar 

  • Westerbergh, A. & J. Doebley, 2002. Morphological traits defining species differences in wild relatives of maize are controlled by multiple quantitative trait loci. Evolution 56:273–283.

    PubMed  Google Scholar 

  • Wolf, J.B., E.D. Brodie & M.J. Wade (eds.), 2000. Epistasis and the Evolutionary Process. Oxford University Press, Oxford, UK.

    Google Scholar 

  • Zeng, Z.-B., C.-H. Kao & C. Basten, 1999. Estimating the genetic architecture of quantitative traits. Genet. Research 74: 279–289.

    Google Scholar 

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Authors and Affiliations

  1. Section of Integrative Biology, University of Texas at Austin, Austin, TX, 78712, USA

    Thomas E. Juenger

  2. Department of Epidemiology and Biostatistics, University of California, San Francisco, San Francisco, CA, 94143-0560, USA

    Sáunak Sen

  3. Department of Integrative Biology, University of California, Berkeley, Berkeley, CA, 94720, USA

    Kirk A. Stowe & Ellen L. Simms

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  1. Thomas E. Juenger
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  2. Sáunak Sen
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  3. Kirk A. Stowe
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  4. Ellen L. Simms
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Rodney Mauricio

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Juenger, T.E., Sen, S., Stowe, K.A., Simms, E.L. (2005). Epistasis and genotype-environment interaction for quantitative trait loci affecting flowering time in Arabidopsis thaliana. In: Mauricio, R. (eds) Genetics of Adaptation. Georgia Genetics Review III, vol 3. Springer, Dordrecht. https://doi.org/10.1007/1-4020-3836-4_9

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