Originally published as Genetics Published Articles Ahead of Print on August 3, 2009.

Genetics, Vol. 183, 723-732, October 2009, Copyright © 2009
doi:10.1534/genetics.109.104984

Cis-regulatory Changes at FLOWERING LOCUS T Mediate Natural Variation in Flowering Responses of Arabidopsis thaliana

Christopher Schwartz^*,,1, Sureshkumar Balasubramanian^,,1, Norman Warthmann^*,, Todd P. Michael^*,**, Janne Lempe^,2, Sridevi Sureshkumar^,3, Yasushi Kobayashi, Julin N. Maloof^*,, Justin O. Borevitz^*,, Joanne Chory^*, and Detlef Weigel^*,,4

^* Plant Biology Laboratory, The Salk Institute for Biological Studies, La Jolla, California 92037, Department of Molecular Biology, Max Planck Institute for Developmental Biology, 72076 Tübingen, Germany, Department of Ecology and Evolution, University of Chicago, Chicago, Illinois 60637, Section of Plant Biology, University of California, Davis, California 95616, Department of Biochemistry, University of Wisconsin, Madison, Wisconsin 53706, ^** Plant Biology and Pathology, Waksman Institute, Rutgers University, Piscataway, New Jersey 08855, The University of Queensland, School of Biological Sciences, St. Lucia, Queensland 4072, Australia and Howard Hughes Medical Institute, The Salk Institute for Biological Sciences, La Jolla, California 92037

⁴ Corresponding author: MPI for Developmental Biology, Spemannstraße 37-39, D-72076 Tübingen, Germany.
E-mail: weigel{at}weigelworld.org

Flowering time, a critical adaptive trait, is modulated by several environmental cues. These external signals converge on a small set of genes that in turn mediate the flowering response. Mutant analysis and subsequent molecular studies have revealed that one of these integrator genes, FLOWERING LOCUS T (FT), responds to photoperiod and temperature cues, two environmental parameters that greatly influence flowering time. As the central player in the transition to flowering, the protein coding sequence of FT and its function are highly conserved across species. Using QTL mapping with a new advanced intercross-recombinant inbred line (AI-RIL) population, we show that a QTL tightly linked to FT contributes to natural variation in the flowering response to the combined effects of photoperiod and ambient temperature. Using heterogeneous inbred families (HIF) and introgression lines, we fine map the QTL to a 6.7 kb fragment in the FT promoter. We confirm by quantitative complementation that FT has differential activity in the two parental strains. Further support for FT underlying the QTL comes from a new approach, quantitative knockdown with artificial microRNAs (amiRNAs). Consistent with the causal sequence polymorphism being in the promoter, we find that the QTL affects FT expression. Taken together, these results indicate that allelic variation at pathway integrator genes such as FT can underlie phenotypic variability and that this may be achieved through cis-regulatory changes.

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