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PMID: 23311994 Published · ppublish English Comparative Study Journal Article

Genetic architecture of flowering time differentiation between locally adapted populations of Arabidopsis thaliana.

The New phytologist ·Vol. 197 ·No. 4 ·2013-03-00 ·Pages 1321-1331

Grillo MA, Li C, Hammond M, Wang L, Schemske DW

Abstract

To gain an understanding of the genetic basis of adaptation, we conducted quantitative trait locus (QTL) mapping for flowering time variation between two winter annual populations of Arabidopsis thaliana that are locally adapted and display distinct flowering times. QTL mapping was performed with large (n = 384) F(2) populations with and without vernalization, in order to reveal both the genetic basis of a vernalization requirement and that of variation in flowering time given vernalization. In the nonvernalization treatment, none of the Sweden parents flowered, whereas all of the Italy parents and 42% of the F(2)s flowered. We identified three QTLs for flowering without vernalization, with much of the variation being attributed to a QTL co-localizing with FLOWERING LOCUS C (FLC). In the vernalization treatment, all parents and F(2)s flowered, and six QTLs of small to moderate effect were revealed, with underlying candidate genes that are members of the vernalization pathway. We found no evidence for a role of FRIGIDA in the regulation of flowering times. These results contribute to a growing body of evidence aimed at the identification of ecologically relevant genetic variation for flowering time in Arabidopsis, and set the stage for functional studies to determine the link between flowering time loci and fitness.

MeSH Terms
Adaptation, Physiological Arabidopsis/genetics,growth & development,physiology Arabidopsis Proteins/genetics Chromosome Mapping Flowers/genetics,growth & development,physiology Genes, Plant Phenotype Population Dynamics Quantitative Trait Loci Time Factors
Chemicals
Arabidopsis Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Grillo Michael A
Department of Plant Biology, Michigan State University, East Lansing, MI, 48824, USA.
Li Changbao
Department of Plant Biology, Michigan State University, East Lansing, MI, 48824, USA.
Hammond Mark
Department of Plant Biology, Michigan State University, East Lansing, MI, 48824, USA.
Wang Lijuan
Department of Plant Biology, Michigan State University, East Lansing, MI, 48824, USA.
Schemske Douglas W
Department of Plant Biology, Michigan State University, East Lansing, MI, 48824, USA.
References (75)
75 references, click to expand
  1. Adrian J, Farrona S, Reimer JJ, Albani MC, Coupland G, Turck F. 2010. cis-Regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis. Plant Cell 22: 1425-1440.
  2. Ågren J, Schemske DW. 2012. Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range. New Phytologist 194: 1112-1122.
  3. Amasino R. 2004. Vernalization, competence, and the epigenetic memory of winter. Plant Cell 16: 2553-2559.
  4. Amasino R. 2010. Seasonal and developmental timing of flowering. Plant Journal 61: 1001-1013.
  5. Balasubramanian S, Schwartz C, Singh A, Warthmann N, Kim MC, Maloof JN, Loudet O, Trainer GT, Dabi T, Borevitz JO et al. 2009. QTL mapping in new Arabidopsis thaliana advanced intercross-recombinant inbred lines. PLoS ONE 4: e4318.
  6. Barton NH, Keightley PD. 2002. Understanding quantitative genetic variation. Nature Reviews Genetics 3: 11-21.
  7. Bastow R, Dean C. 2003. Plant sciences - deciding when to flower. Science 302: 1695-1697.
  8. Beavis WD. 1998. QTL analyses: power, precision, and accuracy. In: Paterson AH, ed. Molecular dissection of complex traits. Boca Raton, FL, USA: CRC Press, 145-162.
  9. Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O. 2006. CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312: 1040-1043.
  10. Brachi B, Faure N, Horton M, Flahauw E, Vazquez A, Nordborg M, Bergelson J, Cuguen J, Roux F. 2010. Linkage and association mapping of Arabidopsis thaliana flowering time in nature. Plos Genetics 6: e1000940.
  11. Broman KW, Wu H, Sen S, Churchill GA. 2003. R/qtl: QTL mapping in experimental crosses. Bioinformatics 19: 889-890.
  12. Burn JE, Bagnall DJ, Metzger JD, Dennis ES, Peacock WJ. 1993. DNA methylation, vernalization, and the initiation of flowering. Proceedings of the National Academy of Sciences, USA 90: 287-291.
  13. Caicedo AL, Richards C, Ehrenreich IM, Purugganan MD. 2009. Complex rearrangements lead to novel chimeric gene fusion polymorphisms at the Arabidopsis thaliana MAF2-5 flowering time gene cluster. Molecular Biology and Evolution 26: 699-711.
  14. 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.
  15. Clarke JH, Dean C. 1994. Mapping FRI, a locus controlling flowering time and vernalization response in Arabidopsis thaliana. Molecular & General Genetics 242: 81-89.
  16. Clarke JH, Mithen R, Brown JKM, Dean C. 1995. QTL analysis of flowering time in Arabidopsis thaliana. Molecular & General Genetics 248: 278-286.
  17. El-Lithy ME, Bentsink L, Hanhart CJ, Ruys GJ, Rovito DI, Broekhof JLM, van der Poel HJA, van Eijk MJT, Vreugdenhil D, Koornneef M. 2006. New Arabidopsis recombinant inbred line populations genotyped using SNPWave and their use for mapping flowering-time quantitative trait loci. Genetics 172: 1867-1876.
  18. 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.
  19. Gendall AR, Levy YY, Wilson A, Dean C. 2001. The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107: 525-535.
  20. Haley CS, Knott SA. 1992. A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity 69: 315-324.
  21. Hoekstra HE, Coyne JA. 2007. The locus of evolution: evo devo and the genetics of adaptation. Evolution 61: 995-1016.
  22. Izawa T. 2007. Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. Journal of Experimental Botany 58: 3091-3097.
  23. Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C. 2000. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290: 344-347.
  24. Juenger TE, Sen S, Stowe KA, Simms EL. 2005. Epistasis and genotype-environment interaction for quantitative trait loci affecting flowering time in Arabidopsis thaliana. Genetica 123: 87-105.
  25. Kalisz S, Wardle GM. 1994. Life-history variation in Campanula americana (Campanulaceae) - population differentiation. American Journal of Botany 81: 521-527.
  26. Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D. 1999. Activation tagging of the floral inducer FT. Science 286: 1962-1965.
  27. Karlsson BH, Sills GR, Nienhuis J. 1993. Effects of photoperiod and vernalization on the number of leaves at flowering in 32 Arabidopsis thaliana (Brassicaceae) ecotypes. American Journal of Botany 80: 646-648.
  28. Kawecki TJ, Ebert D. 2004. Conceptual issues in local adaptation. Ecology Letters 7: 1225-1241.
  29. Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T. 1999. A pair of related genes with antagonistic roles in mediating flowering signals. Science 286: 1960-1962.
  30. Koornneef M, Alonso-Blanco C, Vreugdenhil D. 2004. Naturally occurring genetic variation in Arabidopsis thaliana. Annual Review of Plant Biology 55: 141-172.
  31. Korves TM, Schmid KJ, Caicedo AL, Mays C, Stinchcombe JR, Purugganan MD, Schmitt J. 2007. Fitness effects associated with the major flowering time gene FRIGIDA in Arabidopsis thaliana in the field. American Naturalist 169: E141-E157.
  32. Lacey EP. 1988. Latitudinal variation in reproductive timing of a short-lived monocarp, Daucus carota (Apiaceae). Ecology 69: 220-232.
  33. 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.
  34. Lee I, Bleecker A, Amasino R. 1993. Analysis of naturally-occurring late flowering in Arabidopsis thaliana. Molecular & General Genetics 237: 171-176.
  35. Lempe J, Balasubramanian S, Sureshkumar S, Singh A, Schmid M, Weigel D. 2005. Diversity of flowering responses in wild Arabidopsis thaliana strains. Plos Genetics 1: 109-118.
  36. Li Y, Roycewicz P, Smith E, Borevitz JO. 2006. Genetics of local adaptation in the laboratory: flowering time Quantitative Trait Loci under geographic and seasonal conditions in Arabidopsis. PLoS ONE 1: e105.
  37. Lister C, Dean C. 1993. Recombinant inbred lines for mapping RFLP and phenotypic markers in Arabidopsis thaliana. Plant Journal 4: 745-750.
  38. Loudet O, Chaillou S, Camilleri C, Bouchez D, Daniel-Vedele F. 2002. Bay-0 × Shahdara recombinant inbred line population: a powerful tool for the genetic dissection of complex traits in Arabidopsis. Theoretical and Applied Genetics 104: 1173-1184.
  39. Lowry DB. 2012. Local adaptation in the model plant. New Phytologist 194: 888-890.
  40. Lu H, Romero-Severson J, Bernardo R. 2002. Chromosomal regions associated with segregation distortion in maize. Theoretical and Applied Genetics 105: 622-628.
  41. March-Diaz R, Garcia-Dominguez M, Florencio FJ, Reyes JC. 2007. SEF, a new protein required for flowering repression in Arabidopsis, interacts with PIE1 and ARP6. Plant Physiology 143: 893-901.
  42. 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.
  43. Michaels SD, He YH, 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.
  44. Mitchell-Olds T, Schmitt J. 2006. Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441: 947-952.
  45. Morgan TJ, Mackay TFC. 2006. Quantitative trait loci for thermotolerance phenotypes in Drosophila melanogaster. Heredity 96: 232-242.
  46. Morris K, Thornber S, Codrai L, Richardson C, Craig A, Sadanandom A, Thomas B, Jackson S. 2010. DAY NEUTRAL FLOWERING represses CONSTANS to prevent Arabidopsis flowering early in short days. Plant Cell 22: 1118-1128.
  47. Napp-Zinn K. 1985. Handbook of flowering. Boca Raton, FL, USA: CRC.
  48. Nordborg M, Bergelson J. 1999. The effect of seed and rosette cold treatment on germination and flowering time in some Arabidopsis thaliana (Brassicaceae) ecotypes. American Journal of Botany 86: 470-475.
  49. Olsson K, Ågren J. 2002. Latitudinal population differentiation in phenology, life history and flower morphology in the perennial herb Lythrum salicaria. Journal of Evolutionary Biology 15: 983-996.
  50. O'Neill CM, Morgan C, Kirby J, Tschoep H, Deng PX, Brennan M, Rosas U, Fraser F, Hall C, Gill S et al. 2008. Six new recombinant inbred populations for the study of quantitative traits in Arabidopsis thaliana. Theoretical and Applied Genetics 116: 623-634.
  51. Orr HA. 1998. The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52: 935-949.
  52. Pigliucci M. 2003. Selection in a model system: ecological genetics of flowering time in Arabidopsis thaliana. Ecology 84: 1700-1712.
  53. Pigliucci M, Marlow ET. 2001. Differentiation for flowering time and phenotypic integration in Arabidopsis thaliana in response to season length and vernalization. Oecologia 127: 501-508.
  54. Ratcliffe OJ, Nadzan GC, Reuber TL, Riechmann JL. 2001. Regulation of flowering in Arabidopsis by an FLC homologue. Plant Physiology 126: 122-132.
  55. Salome PA, Bomblies K, Laitinen RAE, Yant L, Mott R, Weigel D. 2011. Genetic architecture of flowering-time variation in Arabidopsis thaliana. Genetics 188: 421-433.
  56. Schwartz C, Balasubramanian S, Warthmann N, Michael TP, Lempe J, Sureshkumar S, Kobayashi Y, Maloof JN, Borevitz JO, Chory J et al. 2009. Cis-regulatory changes at FLOWERING LOCUS T mediate natural variation in flowering responses of Arabidopsis thaliana. Genetics 183: 723-732.
  57. Scortecci KC, Michaels SD, Amasino RM. 2001. Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant Journal 26: 229-236.
  58. Seymour DK, Filiault DL, Henry IM, Monson-Miller J, Ravi M, Pang AD, Comai L, Chan SWL, Maloof JN. 2012. Rapid creation of Arabidopsis doubled haploid lines for quantitative trait locus mapping. Proceedings of the National Academy of Sciences, USA 109: 4227-4232.
  59. Shindo C, Aranzana MJ, Lister C, Baxter C, Nicholls C, Nordborg M, Dean C. 2005. Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiology 138: 1163-1173.
  60. Shindo C, Bernasconi G, Hardtke CS. 2007. Natural genetic variation in Arabidopsis: tools, traits and prospects for evolutionary ecology. Annals of Botany 99: 1043-1054.
  61. Simpson GG, Dean C. 2002. Flowering - Arabidopsis, the rosetta stone of flowering time? Science 296: 285-289.
  62. Stinchcombe JR, Weinig C, Ungerer M, Olsen KM, Mays C, Halldorsdottir SS, Purugganan MD, Schmitt J. 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.
  63. Strange A, Li P, Lister C, Anderson J, Warthmann N, Shindo C, Irwin J, Nordborg M, Dean C. 2011. Major-effect alleles at relatively few loci underlie distinct vernalization and flowering variation in Arabidopsis accessions. PLoS ONE 6: e19949.
  64. Stratton DA. 1998. Reaction norm functions and QTL-environment interactions for flowering time in Arabidopsis thaliana. Heredity 81: 144-155.
  65. Sung SB, Amasino RM. 2004. Vernalization and epigenetics: how plants remember winter. Current Opinion in Plant Biology 7: 4-10.
  66. Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K. 2007. Hd3a protein is a mobile flowering signal in rice. Science 316: 1033-1036.
  67. Tanksley SD. 1993. Mapping polygenes. Annual Review of Genetics 27: 205-233.
  68. Ungerer MC, Halldorsdottir SS, Modliszewski JL, Mackay TFC, Purugganan MD. 2002. Quantitative trait loci for inflorescence development in Arabidopsis thaliana. Genetics 160: 1133-1151.
  69. Van Ooijen JW, Voorips RE. 2001. Joinmap 3.0: software for the calculation of genetic linkage maps. Wageningen, the Netherlands: Plant Research International.
  70. Weingartner M, Subert C, Sauer N. 2011. LATE, a C2H2 zinc-finger protein that acts as floral repressor. Plant Journal 68: 681-692.
  71. Weinig C, Stinchcombe JR, Schmitt J. 2003. QTL architecture of resistance and tolerance traits in Arabidopsis thaliana in natural environments. Molecular Ecology 12: 1153-1163.
  72. Weinig C, Ungerer MC, Dorn LA, Kane NC, Toyonaga Y, Halldorsdottir SS, Mackay TFC, Purugganan MD, Schmitt J. 2002. Novel loci control variation in reproductive timing in Arabidopsis thaliana in natural environments. Genetics 162: 1875-1884.
  73. Werner JD, Borevitz JO, Uhlenhaut NH, Ecker JR, Chory J, Weigel D. 2005a. FRIGIDA-independent variation in flowering time of natural Arabidopsis thaliana accessions. Genetics 170: 1197-1207.
  74. Werner JD, Borevitz JO, Warthmann N, Trainer GT, Ecker JR, Chory J, Weigel D. 2005b. Quantitative trait locus mapping and DNA array hybridization identify an FLM deletion as a cause for natural flowering-time variation. Proceedings of the National Academy of Sciences, USA 102: 2460-2465.
  75. Westerbergh A, Doebley J. 2002. Morphological traits defining species differences in wild relatives of maize are controlled by multiple quantitative trait loci. Evolution 56: 273-283.
Article Info
Journal
The New phytologist
Abbr.
New Phytol
ISSN
1469-8137
DOI
10.1111/nph.12109
Published
2013-03-00
Epub
2013-00-11
Pages
1321-1331
Language
English
Region
England
NLM ID
9882884
Subset
IM
External Links
PubMed source DOI: 10.1111/nph.12109 View journal details
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