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Synchronization of the flowering transition by the tomato TERMINATING FLOWER gene

Abstract

The transition to flowering is a major determinant of plant architecture, and variation in the timing of flowering can have profound effects on inflorescence architecture, flower production and yield. Here, we show that the tomato mutant terminating flower (tmf) flowers early and converts the multiflowered inflorescence into a solitary flower as a result of precocious activation of a conserved floral specification complex encoded by ANANTHA (AN) and FALSIFLORA (FA). Without TMF, the coordinated flowering process is disrupted, causing floral identity genes, such as AN and members of the SEPALLATA (SEP) family, to activate precociously, while the expression of flowering transition genes, such as FRUITFULL (FUL), is delayed. Indeed, driving AN expression precociously is sufficient to cause early flowering, and this expression transforms multiflowered inflorescences into normal solitary flowers resembling those of the Solanaceae species petunia and tobacco. Thus, by timing AN activation, TMF synchronizes flower formation with the gradual reproductive transition, which, in turn, has a key role in determining simple versus complex inflorescences.

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Figure 1: The roles of TMF in shoot organization.
Figure 2: Cloning and expression dynamics of TMF.
Figure 3: Overexpression of TMF promotes vegetative characteristics and branching within tomato inflorescences.
Figure 4: Loss of TMF drives partial precocious activation of floral termination.
Figure 5: AN and FA are required for the tmf phenotype.
Figure 6: Altering the timing of AN transcriptional activation modulates inflorescence architecture.

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Acknowledgements

We thank A. Aharoni for allowing screening of the population from which tmf2-D was derived. We also thank the Tomato Genetics Resource Center (TGRC) at the University of California, Davis, for germplasm, J. Van Eck for generating transgenic plants and DuPont Pioneer for funding. The work in the laboratory of A. Aharoni was supported by European Research Council (ERC) project SAMIT (Framework Programme 7). The tomato TILLING project is supported by funding from the European Union SOL Integrated Project FOOD-CT-2006-016214 to A.B. C.A.M. is a Gordon and Betty Moore Foundation Fellow of the Life Sciences Research Foundation. This research was supported by research grant 1294-10 from the Israel Science Foundation and Binational Agricultural Research & Development Fund IS-4249-09 to Y.E. and a Career Development Award from The International Human Frontier Science Program Organization to Z.B.L.

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Authors

Contributions

C.A.M., S.J.P. and K.J. designed and performed experiments. F.M., A.B. and Y.I. contributed reagents. C.A.M., Y.E. and Z.B.L. designed the research and wrote the manuscript.

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Correspondence to Zachary B Lippman.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Note, Supplementary Figures 1–9 and Supplementary Table 4 (PDF 885 kb)

Supplementary Table 1

TMF interacting proteins (XLSX 12 kb)

Supplementary Table 2

Differentially expressed genes of tmf vs. WT (XLSX 86 kb)

Supplementary Table 3

Primer sequences (XLSX 13 kb)

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MacAlister, C., Park, S., Jiang, K. et al. Synchronization of the flowering transition by the tomato TERMINATING FLOWER gene. Nat Genet 44, 1393–1398 (2012). https://doi.org/10.1038/ng.2465

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