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. 2004 Jul;167(3):1361–1369. doi: 10.1534/genetics.103.024950

Linkage disequilibrium mapping of Arabidopsis CRY2 flowering time alleles.

Kenneth M Olsen 1, Solveig S Halldorsdottir 1, John R Stinchcombe 1, Cynthia Weinig 1, Johanna Schmitt 1, Michael D Purugganan 1
PMCID: PMC1470957  PMID: 15280248

Abstract

The selfing plant Arabidopsis thaliana has been proposed to be well suited for linkage disequilibrium (LD) mapping as a means of identifying genes underlying natural trait variation. Here we apply LD mapping to examine haplotype variation in the genomic region of the photoperiod receptor CRYPTOCHROME2 and associated flowering time variation. CRY2 DNA sequences reveal strong LD and the existence of two highly differentiated haplogroups (A and B) across the gene; in addition, a haplotype possessing a radical glutamine-to-serine replacement (AS) occurs within the more common haplogroup. Growth chamber and field experiments using an unstratified population of 95 ecotypes indicate that under short-day photoperiod, the AS and B haplogroups are both highly significantly associated with early flowering. Data from six genes flanking CRY2 indicate that these haplogroups are limited to an approximately 65-kb genomic region around CRY2. Whereas the B haplogroup cannot be delimited to <16 kb around CRY2, the AS haplogroup is characterized almost exclusively by the nucleotide polymorphisms directly associated with the serine replacement in CRY2; this finding strongly suggests that the serine substitution is directly responsible for the AS early flowering phenotype. This study demonstrates the utility of LD mapping for elucidating the genetic basis of natural, ecologically relevant variation in Arabidopsis.

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Selected References

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  1. Alonso-Blanco C., El-Assal S. E., Coupland G., Koornneef M. Analysis of natural allelic variation at flowering time loci in the Landsberg erecta and Cape Verde Islands ecotypes of Arabidopsis thaliana. Genetics. 1998 Jun;149(2):749–764. doi: 10.1093/genetics/149.2.749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ardlie Kristin G., Kruglyak Leonid, Seielstad Mark. Patterns of linkage disequilibrium in the human genome. Nat Rev Genet. 2002 Apr;3(4):299–309. doi: 10.1038/nrg777. [DOI] [PubMed] [Google Scholar]
  3. Borevitz Justin O., Nordborg Magnus. The impact of genomics on the study of natural variation in Arabidopsis. Plant Physiol. 2003 Jun;132(2):718–725. doi: 10.1104/pp.103.023549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Clarke J. H., Mithen R., Brown J. K., Dean C. QTL analysis of flowering time in Arabidopsis thaliana. Mol Gen Genet. 1995 Aug 21;248(3):278–286. doi: 10.1007/BF02191594. [DOI] [PubMed] [Google Scholar]
  5. El-Din El-Assal S., Alonso-Blanco C., Peeters A. J., Raz V., Koornneef M. A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nat Genet. 2001 Dec;29(4):435–440. doi: 10.1038/ng767. [DOI] [PubMed] [Google Scholar]
  6. Falush Daniel, Stephens Matthew, Pritchard Jonathan K. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics. 2003 Aug;164(4):1567–1587. doi: 10.1093/genetics/164.4.1567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fu Y. X., Li W. H. Statistical tests of neutrality of mutations. Genetics. 1993 Mar;133(3):693–709. doi: 10.1093/genetics/133.3.693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fullerton S. M., Clark A. G., Weiss K. M., Nickerson D. A., Taylor S. L., Stengârd J. H., Salomaa V., Vartiainen E., Perola M., Boerwinkle E. Apolipoprotein E variation at the sequence haplotype level: implications for the origin and maintenance of a major human polymorphism. Am J Hum Genet. 2000 Sep 13;67(4):881–900. doi: 10.1086/303070. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gazzani Silvia, Gendall Anthony R., Lister Clare, Dean Caroline. Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol. 2003 May 22;132(2):1107–1114. doi: 10.1104/pp.103.021212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Guo H., Yang H., Mockler T. C., Lin C. Regulation of flowering time by Arabidopsis photoreceptors. Science. 1998 Feb 27;279(5355):1360–1363. doi: 10.1126/science.279.5355.1360. [DOI] [PubMed] [Google Scholar]
  11. Johanson U., West J., Lister C., Michaels S., Amasino R., Dean C. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science. 2000 Oct 13;290(5490):344–347. doi: 10.1126/science.290.5490.344. [DOI] [PubMed] [Google Scholar]
  12. Johnson G. C., Esposito L., Barratt B. J., Smith A. N., Heward J., Di Genova G., Ueda H., Cordell H. J., Eaves I. A., Dudbridge F. Haplotype tagging for the identification of common disease genes. Nat Genet. 2001 Oct;29(2):233–237. doi: 10.1038/ng1001-233. [DOI] [PubMed] [Google Scholar]
  13. Koornneef M., Hanhart C. J., van der Veen J. H. A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet. 1991 Sep;229(1):57–66. doi: 10.1007/BF00264213. [DOI] [PubMed] [Google Scholar]
  14. Le Corre Valérie, Roux Fabrice, Reboud Xavier. DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: extensive nonsynonymous variation is consistent with local selection for flowering time. Mol Biol Evol. 2002 Aug;19(8):1261–1271. doi: 10.1093/oxfordjournals.molbev.a004187. [DOI] [PubMed] [Google Scholar]
  15. Long A. D., Lyman R. F., Langley C. H., Mackay T. F. Two sites in the Delta gene region contribute to naturally occurring variation in bristle number in Drosophila melanogaster. Genetics. 1998 Jun;149(2):999–1017. doi: 10.1093/genetics/149.2.999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Michaels Scott D., He Yuehui, Scortecci Katia C., Amasino Richard M. Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc Natl Acad Sci U S A. 2003 Aug 6;100(17):10102–10107. doi: 10.1073/pnas.1531467100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mouradov Aidyn, Cremer Frédéric, Coupland George. Control of flowering time: interacting pathways as a basis for diversity. Plant Cell. 2002;14 (Suppl):S111–S130. doi: 10.1105/tpc.001362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Neff Michael M., Turk Edward, Kalishman Michael. Web-based primer design for single nucleotide polymorphism analysis. Trends Genet. 2002 Dec;18(12):613–615. doi: 10.1016/s0168-9525(02)02820-2. [DOI] [PubMed] [Google Scholar]
  19. Nordborg Magnus, Borevitz Justin O., Bergelson Joy, Berry Charles C., Chory Joanne, Hagenblad Jenny, Kreitman Martin, Maloof Julin N., Noyes Tina, Oefner Peter J. The extent of linkage disequilibrium in Arabidopsis thaliana. Nat Genet. 2002 Jan 7;30(2):190–193. doi: 10.1038/ng813. [DOI] [PubMed] [Google Scholar]
  20. Nordborg Magnus, Tavaré Simon. Linkage disequilibrium: what history has to tell us. Trends Genet. 2002 Feb;18(2):83–90. doi: 10.1016/s0168-9525(02)02557-x. [DOI] [PubMed] [Google Scholar]
  21. Rozas J., Rozas R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics. 1999 Feb;15(2):174–175. doi: 10.1093/bioinformatics/15.2.174. [DOI] [PubMed] [Google Scholar]
  22. Rozen S., Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 2000;132:365–386. doi: 10.1385/1-59259-192-2:365. [DOI] [PubMed] [Google Scholar]
  23. Sharbel T. F., Haubold B., Mitchell-Olds T. Genetic isolation by distance in Arabidopsis thaliana: biogeography and postglacial colonization of Europe. Mol Ecol. 2000 Dec;9(12):2109–2118. doi: 10.1046/j.1365-294x.2000.01122.x. [DOI] [PubMed] [Google Scholar]
  24. Tajima F. Evolutionary relationship of DNA sequences in finite populations. Genetics. 1983 Oct;105(2):437–460. doi: 10.1093/genetics/105.2.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. doi: 10.1093/genetics/123.3.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Thornsberry J. M., Goodman M. M., Doebley J., Kresovich S., Nielsen D., Buckler E. S., 4th Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet. 2001 Jul;28(3):286–289. doi: 10.1038/90135. [DOI] [PubMed] [Google Scholar]
  27. Ungerer Mark C., Halldorsdottir Solveig S., Modliszewski Jennifer L., Mackay Trudy F. C., Purugganan Michael D. Quantitative trait loci for inflorescence development in Arabidopsis thaliana. Genetics. 2002 Mar;160(3):1133–1151. doi: 10.1093/genetics/160.3.1133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ungerer Mark C., Halldorsdottir Solveig S., Purugganan Michael D., Mackay Trudy F. C. Genotype-environment interactions at quantitative trait loci affecting inflorescence development in Arabidopsis thaliana. Genetics. 2003 Sep;165(1):353–365. doi: 10.1093/genetics/165.1.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Yoshida Kentaro, Kamiya Taku, Kawabe Akira, Miyashita Naohiko T. DNA polymorphism at the ACAULIS5 locus of the wild plant Arabidopsis thaliana. Genes Genet Syst. 2003 Feb;78(1):11–21. doi: 10.1266/ggs.78.11. [DOI] [PubMed] [Google Scholar]

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