Skip to main content

Studying genetics of adaptive variation in model organisms: flowering time variation in Arabidopsis lyrata

  • Chapter

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

Abstract

Arabidopsis thaliana has emerged as a model organism for plant developmental genetics, but it is also now being widely used for population genetic studies. Outcrossing relatives of A. thaliana are likely to provide suitable additional or alternative species for studies of evolutionary and population genetics. We have examined patterns of adaptive flowering time variation in the outcrossing, perennial A. lyrata. In addition, we examine the distribution of variation at marker genes in populations form North America and Europe. The probability of flowering in this species differs between southern and northern populations. Northern populations are much less likely to flower in short than in long days. A significant daylength by region interaction shows that the northern and southern populations respond differently to the daylength. The timing of flowering also differs between populations, and is made shorter by long days, and in some populations, by vernalization. North American and European populations show consistent genetic differentiation over microsatellite and isozyme loci and alcohol dehydrogenase sequences. Thus, the patterns of variation are quite different from those in A. thaliana, where flowering time differences show little relationship to latitude of origin and the genealogical trees of accessions vary depending on the genomic region studied. The genetic architecture of adaptation can be compared in these species with different life histories.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Abbott, R.J. & M.F. Gomes, 1989. Population genetic structure and outcrossing rate of Arabidopsis thaliana (L.) Heynh. Heredity 62: 411–418.

    Google Scholar 

  • Aguadé, M., 2001. Nucleotide sequence variation at two genes of the phenylpropanoid pathway, the FAHl and F3H genes, in Arabidopsis thaliana. Mol. Biol. Evol. 18: 1–9.

    PubMed  Google Scholar 

  • Allard, R.W., S.K. Jain & P. Workman, 1968. The genetics of inbreeding species. Adv. Genetics 14: 55–131.

    Google Scholar 

  • Arabidopsis Genome Initiative, 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.

    Google Scholar 

  • Bergelson, J., E. Stahl, S. Dudek & M. Kreitman, 1998. Genetic variation within and among populations of Arabidopsis thaliana. Genetics 148: 1311–1323.

    PubMed  Google Scholar 

  • Charlesworth, B., M.T. Morgan & D. Charlesworth, 1993. The effect of deleterious mutations on neutral molecular variation. Genetics 134: 1289–1303.

    PubMed  Google Scholar 

  • Charlesworth, D. & B. Charlesworth, 1995. Quantitative genetics of plants: the effect of the breeding system on genetic variability. Evolution 49: 911–920.

    Google Scholar 

  • Clauss, M.J., H. Cobban & T. Mitchell-Olds, 2002. Cross-species microsatellite markers for elucidating population genetic structure in Arabidopsis and Arabis (Brassicaceae). Mol. Ecol. 11: 591–601.

    PubMed  Google Scholar 

  • Clayton, D., 1996. Generalized linear models, pp. 275–301 in Markov Chain Monte Carlo Methods in Practice, edited by W.R. Gilks, S. Richardson & D.J. Spiegelhalter. Chapman and Hall, London.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Hamrick, J.L. & M.J.W. Godt, 1996. Effects of life history traits on genetic diversity in plant species. Phil. Trans. R. Soc. Lond. B 351: 1291–1298.

    Google Scholar 

  • Hanfstingl, U., A. Berry, E.A. Kellogg, J.T. Costa, W. Ruediger & F.M. Ausubel, 1994. Haplotypic divergence coupled with lack of diversity at the Arabidopsis thaliana alcohol dehydrogenase locus: roles for both balancing and directional selection? Genetics 138: 811–828.

    PubMed  Google Scholar 

  • Hudson, R.R., 1990. Gene genealogies and the coalescent process, pp. 1–44 in Oxford Surveys in Evolutionary Biology, edited by D. Futuyma & J. Antonovics. Oxford.

    Google Scholar 

  • Ingvarsson, P.K., 2002. A metapopulation perspective on genetic diversity and differentiation in partially self-fertilizing plants. Evolution 56: 2368–2373.

    PubMed  Google Scholar 

  • Innan, H., F. Tajima, R. Terauchi & N.T. Miyashita, 1996. Intragenic recombination in the Adh locus of the wild plant Arabidopsis thaliana. Genetics 143: 1761–1770.

    PubMed  Google Scholar 

  • Innan, H., R. Terauchi & N. Miyashita, 1997. Microsatellite polymorphism in natural populations of the wild plant Arabidopsis thaliana. Genetics 146: 1441–1731.

    PubMed  Google Scholar 

  • Jansen, R., J. Van Ooijen, P. Starn, 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. Michaels, R. Amasino & C. Dean, 2000. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290: 344–347.

    PubMed  Google Scholar 

  • Jones, B.M.G., 1963 Experimental Taxonomy of the Genus Arabis. University of Leicester, UK, Leicester.

    Google Scholar 

  • Jones, M.E., 1971a. The population genetics of Arabidopsis thaliana. II. Population structure. Heredity 27: 51–58.

    Google Scholar 

  • Jones, M.E., 1971b. The population genetics of Arabidopsis thaliana. I. The breeding system. Heredity 27: 39–50.

    Google Scholar 

  • Kaplan, N.L., R.R. Hudson & C.H. Langley, 1989. The ‘hitchhiking’ effect revisited. Genetics 123: 887–899.

    PubMed  Google Scholar 

  • Kärkkäinen, K., H. Kuittinen, R. van Treuren, C. Vogl, S. Oikarinen & O. Savolainen, 1999. Genetic basis of inbreeding depression in Arabis petraea. Evolution 53: 1354–1365.

    Google Scholar 

  • Karlsson, B.H., G.R. Sills & J. Nienhuis, 1993. Effects of photoperiod and vernalization on the number of leaves at flowering in 32 Arabidopsis thaliana (Brassicaceae) ecotypes. Amer. J. Bot. 80: 646–648.

    Google Scholar 

  • Koch, M., J. Bishop & T. Mitchell-Olds, 1999. Molecular systematics and evolution of Arabidopsis and Arabis. Plant Biol. 1: 529–537.

    Google Scholar 

  • Koch, M., R Haubold & T. Mitchell-Olds, 2001. Molecular systematics of the Brassicaceae: evidence from coding platidic MatK and nuclear CHS. Amer. J. Bot. 88: 534–544.

    Google Scholar 

  • Koch, M.A., B. Haubold & T. Mitchell-Olds, 2000. Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol. Biol. Evol. 17: 1483–1498.

    PubMed  Google Scholar 

  • Koornneef, M., C.J. Hanhart & J.H. van der Veen, 1991. A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol. Gen. Genet. 229: 57–66.

    PubMed  Google Scholar 

  • Kuittinen, H. & M. Aguadé, 2000. Nucleotide variation at the Chalcone Isomerase locus in Arabidopsis thaliana. Genetics 155: 863–872.

    PubMed  Google Scholar 

  • Kuittinen, H., M. Aguadé, D. Charlesworth, A. De Haan, B. Lauga, T. Mitchell-Olds, S. Oikarinen, S. Ramos-Onsins, B. Stranger, P. van Tienderen & O. Savolainen, 2002a. Primers for 22 candidate genes for ecological adaptations in Brassicaceae. Mol. Ecol. Notes 2: 258–262.

    Google Scholar 

  • Kuittinen, H., A. Mattila & O. Savolainen, 1997. Genetic variation at marker loci and in quantitative traits in natural populations of Arabidopsis thaliana. Heredity 79:144–152.

    PubMed  Google Scholar 

  • Kuittinen, H., D. Salguero & M. Aguadé, 2002b. Parallel patterns of sequence variation within and between populations at three loci of Arabidopsis thaliana. Mol. Biol. Evol. 19: 2030–2034.

    PubMed  Google Scholar 

  • Kumar, S., K. Tamura, LB. Jakobsen & M. Nei, 2001. MEGA2: Molecular Evolutionary Genetics Analysis Software. Arizona State University, Tempe, Arizona.

    Google Scholar 

  • Kusaba, M., K. Dwyer, J. Hendershot, J. Vrebalov, J.B. Nasrallah & M.E. Nasrallah, 2001. Self-incompatibility in the genus Arabidopsis: characterization of the S locus in the outcrossing A. lyrata and its autogamous relative A. thaliana. Plant Cell 13: 627–643.

    PubMed  Google Scholar 

  • Lagercrantz, U., 1998. Comparative mapping between Arabidopsis thaliana and Brassica nigra indicates that Brassica genomes have evolved through extensive genome replication accompanied by chromosome fusions and frequent rearrangements. Genetics 150: 1217–1228.

    PubMed  Google Scholar 

  • Lagercrantz, U., J. Putterill, G. Coupland & D. Lydiate, 1996. Comparative mapping in Arabidopsis and Brassica, fine scale genome collinearity and congruence of genes controlling flowering time. Plant J. 19: 13–20.

    Google Scholar 

  • Maloof, J., J. Borevitz, T. Dabi, J. Lutes, R. Nehring, J. Redfern, G. Trainer, J. Wilson, T. Asami, C. Berry, D. Weigel & J. Chory, 2001. Natural variation in light sensitivity of Arabidopsis. Nat. Genet. 29: 441–446.

    PubMed  Google Scholar 

  • Mesicek, J., 1967. The chromosome morphology of Arabidopsis thaliana (L.) Heynh. and some remarks on the problem of Hylandra suecica (Fr.) Love. Folia Geobot. Phytotaxonom. 2: 433–436.

    Google Scholar 

  • Mikola, J., 1982. Bud-set phenology as an indicator of climatic adaptation of Scots pine in Finland. Silva Fennica 16:178–184.

    Google Scholar 

  • Mitchell-Olds, T., 2001. Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution. Trends Ecol. Evol. 16: 693–700.

    Google Scholar 

  • Miyashita, N.T., A. Kawabe & H. Innan, 1999. DNA variation in the wild plant Arabidopsis thaliana revealed by amplified fragment length polymorphism analysis. Genetics 152:1723–1731.

    PubMed  Google Scholar 

  • Napp-Zinn, K., 1957. Untersuchungen zur Genetik des Kältebedurfnisses bei Arabidopsis thaliana. Zeitschrift fur indukt. Abstammungs-und Vererbungslehre 88: 253–285.

    Google Scholar 

  • Nasrallah, M.E., K. Yogeeswaran, S. Snyder & J.B. Nasrallah, 2000. Arabidopsis species hybrids in the study of species differences and evolution of amphiploidy in plants. Plant Physiol. 124: 1605–1614.

    PubMed  Google Scholar 

  • Nei, M. & S. Kumar, 2000. Molecular Evolutionary Phylogenetics. Oxford University Press, Oxford.

    Google Scholar 

  • Nordborg, M. & J. Bergelson, 1999. The effect of seed and rosette cold treatment on germination and flowering time in some Arabidopsis thaliana (Brassicaceae) ecotypes. Am. J. Bot. 86: 470–475.

    PubMed  Google Scholar 

  • Nordborg, M., J.O. Borewitz, J. Bergelson, C. Berry, J. Chory, J. Hagenblad, M. Kreitman, J. Maloof, T. Noyes, P.J. Oefner, E.A. Stahl & D. Weigel, 2002. The extent of linkage disequilibrium in Arabidopsis thaliana. Nat. Genet. 30: 190–193.

    PubMed  Google Scholar 

  • Nordborg, M. & P. Donnelly, 1997. The coalescent process with selfing. Genetics 146: 1185–1195.

    PubMed  Google Scholar 

  • Nordborg, M. & S. Tavaré, 2002. Linkage disequilibrium: what history has to tell us. Trends Genet. 18: 83–90.

    PubMed  Google Scholar 

  • O’Kane, S.L. & LA. AI-Shehbaz, 1997. A synopsis of Arabidopsis (Brassicaceae). Novon 7: 323–327.

    Google Scholar 

  • Pannell, J.R. & B. Charlesworth, 1999. Neutral genetic diversity in a metapopulation with recurrent local extinction and recolonization. Evolution 53: 664–676.

    Google Scholar 

  • Pannell, J.R. & B. Charlesworth, 2000. Effects of metapopulation processes on measures of genetic diversity. Phil. Trans. R. Soc. Lond. B 355: 1851–1864.

    Google Scholar 

  • Pigliucci, M., H. Pollard & M.B. Cruzan, 2003. Comparative studies of evolutionary responses to light environments in Arabidopsis. Amer. Natur 161: 68–82.

    Google Scholar 

  • Pinheiro, J.C. & D.M. Bates, 2000. Mixed Effects Models in Sand S-PLUS. Springer Verlag, New York.

    Google Scholar 

  • Price, R.A., J.D. Palmer & I.A. Al-Shehbaz, 1994. Systematic relationships of Arabidopsis, pp. 7–19 in Arabidopsis, edited by E.M. Meyerowitz & C. Somerville. Cold Spring Harbor Press, Cold Spring Harbor, NY.

    Google Scholar 

  • Putterill, J., F. Robson, K. Lee, R. Simon & G. Coupland, 1995. The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80: 847–857.

    PubMed  Google Scholar 

  • R Development Core Team. 2002. R: a language and environment for statistical computing. Vienna, Austria.

    Google Scholar 

  • Redei, G.P., 1974. Is Hylandra an amphidiploid of Arabidopsis and Cardaminopsis arenosa? Arabidopsis Inf. Servo 11: 5.

    Google Scholar 

  • Saitou & Nei, 1987. The nieghbor-joining method: a new method for constructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.

    PubMed  Google Scholar 

  • Savolainen, O., C.H. Langley, B. Lazzaro & H. Freville, 2000. Contrasting patterns of nucleotide variation at the alcohol dehydrogenase locus in the outcrossing Arabidopsis lyrata and the selfing Arabidopsis thaliana. Mol. Biol. Evol. 17:645–55.

    PubMed  Google Scholar 

  • Schierup, M.H., 1998. The effect of enzyme heterozygosity on growth in a strictly outcrossing species, the self-incompatible Arabis petraea (Brassicaceae). Hereditas 128:21–31.

    Google Scholar 

  • Sharbel, T.F., B. Haubold & T. Mitchell-Olds, 2000. Genetic isolation by distance in Arabidopsis thaliana: biogeography and postglacial colonization of Europe. Mol. Ecol. 9:2109–2118.

    PubMed  Google Scholar 

  • Spiegelhalter, D.J., A. Thomas & N.G. Best, 2000. WinBUGS Version 1.3. User Manual. MRC Biostatistics Unit, Cambridge, UK.

    Google Scholar 

  • Stahl, E.A., G. Dwyer, R. Mauricio, R. Kreitman & J. Bergelson, 1999. Dynamics of disease resistance polymorphism at the Rpml locus of Arabidopsis. Nature 400:667–71.

    PubMed  Google Scholar 

  • Stenóien, H., C. Fenster, H. Kuittinen & O. Savolainen, 2002. Quantifying latitudinal lines to light responses in natural populations of Arabidopsis thaliana (Brassicaceae). Am. J. Bot.

    Google Scholar 

  • Suarez-López, P., K. Wheatley, F. Robson, H. Onouchi, F. Valverde & G. Coupland, 2001. CONSTANS mediates between the cirdacian clock and the control of flowering time in Arabidopsis. Nature 410: 1116–1120.

    PubMed  Google Scholar 

  • Thomas, B. & D. Vince-Prue, 1999. Photoperiodism in Plants. Academic Press, San Diego.

    Google Scholar 

  • Thornsberry, J.M., M.M. Goodman, J. Doebley, S. Kresovich, D. Nielsen & E.S. Buckler, 2001. Dwarf8 polymorphisms associate with variation in flowering time. Nature Genet. 28: 286–289.

    PubMed  Google Scholar 

  • Todokoro, S., R. Terauchi & S. Kawano, 1996. Microsatellite polymorphism in natural populations of Arabidopsis thaliana in Japan. Jpn. J. Genet. 70: 543–554.

    Google Scholar 

  • Van Treuren, R., H. Kuittinen, K. Kärkkäinen, E. Baena-Gonzalez & O. Savolainen, 1997. Evolution of microsatellites in Arabis petraea and A. lyrata, outcrossing relatives of Arabidopsis thaliana. Mol. Biol. Evol. 14: 220–229.

    PubMed  Google Scholar 

  • Wakeley, J. & N. Aliacar, 2001. Gene genealogies in a metapopulation. Genetics 159: 893–905.

    PubMed  Google Scholar 

  • Weiss, K.M. & A.G. Clark, 2002. Linkage disequilibrium and the mapping of complex human traits. Trends Genet. 18: 19–24.

    PubMed  Google Scholar 

  • Westerman, J.M. & M.J. Lawrence, 1970. Genotype-environment interaction and developmental regulation in Arabidopsis thaliana. I. Inbred lines; description. Heredity 25: 609–627.

    Google Scholar 

  • Wright, S.I., B. Lauga & D. Charlesworth, 2002. Rates and patterns of molecular evolution in inbred and outbred Arabidopsis. Mol. Biol. Evol. 19: 1407–1420.

    PubMed  Google Scholar 

  • Yanovsky, M.J. & S.A. McKay, 2002. Molecular basis of seasonal time measurement in Arabidopsis. Nature 419: 308–312.

    PubMed  Google Scholar 

  • Zenker, A.M., 1955. Jarowisationsuntersuchungen an sommerannuellen Arabidopsis Rassen. Beitr. Biol. Pflantz. 32:135–170.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Outi Savolainen .

Editor information

Rodney Mauricio

Rights and permissions

Reprints and permissions

Copyright information

© 2005 Springer

About this chapter

Cite this chapter

Riihimäki, M., Podolsky, R., Kuittinen, H., Koelewijn, H., Savolainen, O. (2005). Studying genetics of adaptive variation in model organisms: flowering time variation in Arabidopsis lyrata. In: Mauricio, R. (eds) Genetics of Adaptation. Georgia Genetics Review III, vol 3. Springer, Dordrecht. https://doi.org/10.1007/1-4020-3836-4_7

Download citation

Publish with us

Policies and ethics