Standing genetic variation in FRIGIDA mediates experimental evolution of flowering time in Arabidopsis

Molecular Ecology

Volumn 18, Issue 9, 2009, Pages 2039-2049

  Scarcelli, Nora ^a,b   Kover, Paula X ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

Arabidopsis thaliana; Bolting time; Parallel evolution; QTL; Response to selection

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; FLF PROTEIN, ARABIDOPSIS; FRI PROTEIN, ARABIDOPSIS; MADS DOMAIN PROTEIN; PLANT DNA;

ALLELE; ARABIDOPSIS; ARTICLE; DNA SEQUENCE; FLOWER; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; HAPLOTYPE; MOLECULAR EVOLUTION; PHYSIOLOGY; PLANT GENE; SEASON;

ALLELES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA, PLANT; EVOLUTION, MOLECULAR; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENE FREQUENCY; GENES, PLANT; GENETIC VARIATION; HAPLOTYPES; MADS DOMAIN PROTEINS; SEASONS; SELECTION (GENETICS); SEQUENCE ANALYSIS, DNA;

EID: 65549130876     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2009.04145.x     Document Type: Article

References (62)

1. Balasubramanian S, Sureshkumar S, Agrawal M et al 2006) The PHYTOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana. Nature Genetics, 38, 711 715. (Pubitemid 43927316)
2. Barrett RDH, Schluter D (2008) Adaptation from standing genetic variation. Trends in Ecology & Evolution, 23, 38 44.
3. Beck JB, Schmuths H, Schaal BA (2008) Native range genetic variation in Arabidopsis thaliana is strongly geographically structured and reflects Pleistocene glacial dynamics. Molecular Ecology, 17, 902 915.
4. Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell, 16, S18 S31. (Pubitemid 38774214)
5. Bradshaw WE, Holzapfel CM (2001) Genetic shift in photoperiodic response correlated with global warming. Proceedings of the National Academy of Sciences, USA, 98, 14509 14511. (Pubitemid 33121422)
6. Bull JJ, Badgett MR, Wichman HA et al 1997) Exceptional convergent evolution in a virus. Genetics, 147, 1497 1507. (Pubitemid 27525448)
7. Caicedo AL, Schaal BA, Kunkel BN (1999) Diversity and molecular evolution of the RPS2 resistance gene in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA, 96, 302 306. (Pubitemid 29036094)
8. Caicedo AL, Stinchcombe JR, Olsen KM, Schmitt J, Purugganan MD (2004) Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proceedings of the National Academy of Sciences, USA, 101, 15670 15675. (Pubitemid 39473546)
9. Charlesworth B, Charlesworth D, Barton NH (2003) The effects of genetic and geographic structure on neutral variation. Annual Review of Ecology, Evolution, and Systematics, 34, 99 125. (Pubitemid 38171415)
10. Colosimo PF, Hosemann KE, Balabhadra S et al 2005) Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science, 307, 1928 1933. (Pubitemid 40404697)
11. Cunningham CW, Jeng K, Husti J et al 1997) Parallel molecular evolution of deletions and nonsense mutations in bacteriophage T7. Molecular Biology and Evolution, 14, 113 117.
12. Donohue K (1996) Germination timing influence natural selection on life-history characters in Arabidopsis thaliana. Ecology, 83, 1006 1016.
13. Falconer DS, Mackay TFC (1996) Introduction to Quantitative Genetics, 4th edn. Longman, England.
14. Filiault DL, Wessinger CA, Dinneny JR et al 2008) Amino acid polymorphisms in Arabidopsis phytochrome B cause differential responses to light. Proceedings of the National Academy of Sciences, USA, 105, 3157 3162.
15. Frankham R, Ballou J, Briscoe D (2002) Introduction to Conservation Genetics, p. 617. Cambridge University pres, Cambridge, UK.
16. Gallais A, Moreau L, Charcosset A (2007) Detection of marker-QTL associations by studying change in marker frequencies with selection. Theoretical and Applied Genetics, 114, 669 681. (Pubitemid 46214064)
17. Gazzani S, Gendall AR, Lister C, Dean C (2003) Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiology, 132, 1107 1114. (Pubitemid 36715107)
18. Hagenblad J, Tang C, Molitor J et al 2004) Haplotype structure and phenotypic associations in the chromosomal regions surrounding two Arabidopsis thaliana flowering time loci. Genetics, 168, 1627 1638. (Pubitemid 40007374)
19. IPCC (2001) Climate change 2001: the scientific basis. In : Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change (eds Houghton JT, Ding Y, Griggs DJ et al.), p. 881. Cambridge University Press, Cambridge, UK and New York.
20. Johanson U, West J, Lister C et al 2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science, 290, 344 347.
21. Kimura M, Crow JF (1978) Effect of overall phenotypic selection on genetic change at individual loci. Proceedings of the National Academy of Sciences, USA, 75, 6168 6171. (Pubitemid 9100968)
22. Koornneef M, Alonso-Blanco C, Peeters AJM, Soppe W (1998) Genetic control of flowering time in Arabidopsis. Annual Review Plant Physiology and Plant Molecular Biology, 49, 345 370. (Pubitemid 28514496)
23. Korves TM, Schmid KJ, Caicedo AL et al 2007) Fitness effects associated with the major flowering time gene FRIGIDA in Arabidopsis thaliana in the field. American Naturalist, 169, E141 E157.
24. Le Corre V, Roux F, Reboud X (2002) DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: Extensive nonsynonymous variation is consistent with local selection for flowering time. Molecular Biology and Evolution, 19, 1261 1271.
25. Lempe J, Balasubramanian S, Sureshkumar S et al 2005) Diversity of flowering responses in wild Arabidopsis thaliana strains. PLoS Genetics, 1, e6.
26. Lynch M, Walsh B (1998) Genetics and Analysis of Quantitative Traits 980. Sinauer & Associates Inc., Sunderland, Massachusetts.
27. Maloof JN, Borevitz JO, Dabi T et al 2001) Natural variation in light sensitivity of Arabidopsis. Nature Genetics, 29, 441 446. (Pubitemid 34326695)
28. Mckay JM, Richards JH, Mitchell-Olds T (2003) Genetics of drought adaptation in Arabidopsis thaliana. I. Pleiotropy contributes to genetic correlations among ecological traits. Molecular Ecology, 12, 1137 1151. (Pubitemid 36573116)
29. Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell, 11, 949 956.
30. Michaels SD, Amasino RM (2001) Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell, 13, 935 941. (Pubitemid 32375911)
31. Michaels SD, He Y, Scortecci KC, Amasino RM (2003) Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proceedings of the National Academy of Sciences, USA, 100, 10102 10107. (Pubitemid 37087074)
32. Napp-Zinn K (1985) Arabidopsis thaliana. In : CRC Handbook of Flowering, Vol. 1, (ed Halevy AH), pp. 492 503. CRC Press, Boca Raton, Florida. (Pubitemid 32451907)
33. Olsen KM, Halldorsdottir SS, Stinchcombe JR et al 2004) Linkage disequilibrium mapping of Arabidopsis CRY2 flowering time alleles. Genetics, 167, 1361 1369. (Pubitemid 39045642)
34. Pickert M (1988) In vitro germination and storage of trinucleate Arabidopsis thaliana (L.) pollen grains. Arabidopsis Information Service, 26. Available from URL : http://www.arabidopsis.org/ais/1988/picke-1988-aadeg.html.
35. Protas ME, Hersey C, Kochanek D et al 2006) Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nature Genetics, 38, 107 111. (Pubitemid 43011890)
36. Przeworski M, Coop G, Wall JD (2005) The signature of positive selection on standing genetic variation. Evolution, 59, 2312 2323. (Pubitemid 41752645)
37. Putterill J, Laurie R, Macknight R (2004) It's time to flower: the genetic control of flowering time. Bioessays, 26, 363 373. (Pubitemid 38461617)
38. Reboud X, Le Corre V, Scarcelli N et al 2004) Natural variation among accessions of Arabidopsis thaliana: beyond the flowering date, what morphological traits are relevant to study adaptation? In : Plant Adaptation: Molecular Genetics and Ecology. Proceedings of an International Workshop Held December 11-13, 2002, in Vancouver, British Columbia, Canada. (eds Cronk QCB, Whitton J, Ree RH, Taylor IEP pp. 135 142. NRC Research Press, Ottawa, Ontario, Canada.
39. Riehle MM, Bennett AF, Long AD (2001) Genetic architecture of thermal adaptation in Escherichia coli. Proceedings of the National Academy of Sciences, USA, 98, 525 530. (Pubitemid 32105075)
40. Roff DA (1997) Evolutionary Quantitative Genetics, p. 516. Chapman & Hall, New York.
41. Roux F, Touzet P, Cuguen J, Le Corre V (2006) How to be early flowering: an evolutionary perspective. Trends in Plant Science, 11, 375 381. (Pubitemid 44108711)
42. Scarcelli N, Cheverud JM, Schaal BA, Kover PX (2007) Antagonistic pleiotropic effects reduce the potential adaptive value of the FRIGIDA locus. Proceedings of the National Academy of Sciences, USA, 104, 16986 16991. (Pubitemid 350210977)
43. Schmitz RJ, Amasino RM (2007) Vernalization: a model for investigating epigenetics and eukaryotic gene regulation in plants. Biochimica et Biophysica Acta - Gene Structure et Expression, 1769, 269 275. (Pubitemid 46855946)
44. Sheldon CC, Burn JE, Perez PP et al 1999) The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell, 11, 445 458.
45. Sheldon CC, Finnegan EJ, Rouse DT et al 2000) The control of flowering by vernalization. Current Opinion in Plant Biology, 3, 418 422.
46. Shindo C, Aranzana MJ, Lister C et al 2005) Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiology, 138, 1163 1173. (Pubitemid 43793190)
47. Simões P, Santos J, Fragata I et al 2008) How repeatable is adaptive evolution? The role of geographical origin and founder effects in laboratory adaptation. Evolution, 62, 1817 1829.
48. Simpson GG, Dean C (2002) Arabidopsis, the rosetta stone of flowering time? Science, 296, 285 289. (Pubitemid 34303671)
49. Stinchcombe JR, Caicedo AL, Hopkins R et al 2005) Vernalization sensitivity in Arabidopsis thaliana (Brassicaceae): the effects of latitude and FLC variation. American Journal of Botany, 92, 1701 1707. (Pubitemid 41426906)
50. Stinchcombe JR, Weinig C, Ungerer M et al 2004) A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proceedings of the National Academy of Sciences, USA, 101, 4712 4717. (Pubitemid 38437476)
51. Stockwell CA, Hendry AP, Kinnison MT (2003) Contemporary evolution meets conservation biology. Trends in Ecology & Evolution, 18, 94 101. (Pubitemid 36072684)
52. Tenaillon MI, Tiffin PL (2008) The quest for adaptive evolution: a theoretical challenge in a maze of data. Current Opinion in Plant Biology, 11, 110 115.
53. van Tienderen PH, Hammad I, Zwaal FC (1996) Pleiotropic effects of flowering time genes in the annual crucifer Arabidopsis thaliana (Brassicaceae). American Journal of Botany, 83, 169 174. (Pubitemid 2620542)
54. Toomajian C, Hu TT, Aranzana MJ et al 2006) A nonparametric test reveals selection for rapid flowering in the Arabidopsis genome. PLoS Biology, 4, e137. (Pubitemid 43748220)
55. Weinig C, Ungerer MC, Dorn LA, Kane NC et al 2002) Novel Loci Control Variation in Reproductive Timing in Arabidopsis thaliana in Natural Environments. Genetics, 162, 1875 1884. (Pubitemid 36114670)
56. Weinig C, Dorn LA, Kane NC et al 2003) Heterogeneous selection at specific loci in natural environments in Arabidopsis thaliana. Genetics, 165, 321 329. (Pubitemid 37204077)
57. Werner JD, Borevitz JO, Uhlenhaut NH et al 2005) FRIGIDA-independent variation in flowering time of natural Arabidopsis thaliana accessions. Genetics, 170, 1197 1207. (Pubitemid 41105475)
58. Whitlock MC, Phillips PC, Wade MJ (1993) Gene interaction affects the additive genetic variance in subdivided populations with migration and extinction. Evolution, 47, 1758 1769. (Pubitemid 2097329)
59. Wood TE, Burke JM, Rieseberg LH (2005) Parallel genotypic adaptation: when evolution repeats itself. Genetica, 123, 157 170. (Pubitemid 40466126)
60. Wood R, Schneider D, Winkworth CL, Riley MA, Lenski RE (2006) Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proceedings of the National Academy of Sciences, USA, 103, 9107 9112. (Pubitemid 43902541)
61. Wright SI, Gaut BS (2005) Molecular population genetics and the search for adaptive evolution in plants. Molecular Biology and Evolution, 22, 506 519. (Pubitemid 40299500)
62. Zhao K, Aranzana MJ, Kim S et al 2007) An Arabidopsis example of association mapping in structured samples. PLoS Genetics, 3, e4. (Pubitemid 46168834)