Focusing on TERMINAL FLOWER 1 (TFL1) regulation

by Timo Hytönen
University of Helsinki, Finland

FLOWERING LOCUS T (FT) and TERMINAL FLOWER 1 (TFL1) are small closely related proteins that have a great impact on the production of agricultural and horticultural crops and forest trees. FT functions as a mobile signaling molecule that travels from leaves to shoot meristems to mediate information about the suitable season to induce flowers, produce tubers or set a bud (reviewed by Wickland & Hanzawa, 2015). TFL1, in contrast, is a repressor of flowering that is expressed locally in meristems. In species with indeterminate growth habit, one of the main functions of TFL1 is to maintain indeterminate inflorescence meristem and to allow flower bud development only in the flanks of the meristem. This has a direct effect on yield because it affects the number of seeds or fruits. In some other species with closed inflorescence structures, high TFL1 expression can completely prevent floral development (Costes et al., 2014).

Both FT and TFL1 are transcriptional cofactors that bind with the same transcription factor FD, and there is increasing evidence that the balance of these antagonistic signals determines the developmental output (Hanano & Goto, 2011; Wickland & Hanzawa, 2015). The molecular control of FT has been studied in detail especially in Arabidopsis, but much less is known about factors controlling spatiotemporal expression pattern of TFL1.


Indeterminate inflorescences at the lava desert of El Teide.

In their recent study, Serrano-Mislata et al. (2016) explored cis-regulatory elements of TFL1 using various experimental approaches including mutant complementation, phylogenetic shadowing and promoter::GUS fusion lines. First, they tried to complement tfl1 mutant using a genomic construct containing full 5’ and 3’ intergenic regions and a similar construct lacking introns. Both constructs similarly complemented the mutant phenotype indicating that introns are not needed for the transcriptional regulation of TFL1. Next, using phylogenetic shadowing of TFL1 orthologues of several Brassicaceae species, they found seven conserved blocks that were tested further using genomic constructs of different lengths as well as similar constructs containing GUS reporter in the place of TFL1. Using these constructs the authors successfully dissected the roles of different promoter blocks in controlling TFL1 expression and shoot architecture. They found that 300 bp upstream and 3.3 kb downstream regions are needed to fully complement the defects of tfl1 mutant and to drive similar expression of GUS reporter than the full-length genomic construct. This short 5’ region is needed to maintain high TFL1 expression level, whereas separate 3’ elements control its spatiotemporal expression in different meristems. A 3’ region +2.8-3.3 kb after the stop codon is needed to maintain TFL1 expression in the inflorescence meristem, and another region at +1.6-2.2 kb controls its expression in axillary meristems. Finally, 3’ region between +1.0 and +1.3 is required to control flowering time by affecting TFL1 expression in vegetative meristems as well as its up-regulation following floral transition.


TFL1 promoter elements controlling its spatiotemporal expression pattern (based on Serrano-Mislata et al. (2016).

The authors suggested that a modular structure of TFL1 promoter might facilitate gene evolution to generate different plant architectures as already observed in Leavenforthia crassa. More importantly, the identification of these modules is instrumental for future research focusing on upstream regulators of TFL1 that may control inflorescence architecture and/or flowering time in different species. One important question is what is causing the up-regulation of TFL1 in the vegetative meristem upon flower induction. One of the suggested regulators is a MADS transcription factor XAANTAL2 that shows sequence similarity with SUPPRESSOR OF THE OVEREXPRESSION OF CONSTANS1 (SOC1) (Pérez-Ruiz et al., 2015). Interestingly, also SOC1 is highly expressed in the inflorescence meristem (Immink et al., 2012), and the strawberry orthologue of SOC1 has been shown to up-regulate TFL1 (Mouhu et al., 2013). In addition, an early study indicated that CO may induce the expression of TFL1 (Simon et al., 1996), perhaps through FT. Using tools produced by Serrano-Mislata et al. (2016), time is now ripen to focus on the molecular control of TFL1 expression that may translate to increased crop yields.


Costes E, Crespel L, Denoyes B, Morel P, Demene M, Lauri P & Wenden B. 2014. Bud structure, position and fate generate various branching patterns along shoots of closely related Rosaceae species: a review. Frontiers in Plant Science 5: 666.

Hanano S & Goto K. 2011. Arabidopsis TERMINAL FLOWER1 is involved in the regulation of flowering time and inflorescence development through transcriptional repression. The Plant Cell 23: 3172–3184. http:/​/​dx.​doi.​org/​10.​1105/​tpc.​111.​088641

Immink RGH, Posé D, Ferrario S, Ott F, Kaufmann K, Valentim FL, de Folter S, van der Wal F, van Dijk ADJ, Schmid M & Angenent GC. 2012. Characterization of SOC1’s central role in flowering by the identification of its upstream and downstream regulators. Plant Physiology 160: 433–449. http:/​/​dx.​doi.​org/​10.​1104/​pp.​112.​202614

Mouhu K, Kurokura T, Koskela EA, Albert VA, Elomaa P & Hytönen T. 2013. The Fragaria vesca homolog of SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 represses flowering and promotes vegetative growth. The Plant Cell 25: 3296–3310. http:/​/​dx.​doi.​org/​10.​1105/​tpc.​113.​115055

Pérez-Ruiz RV, García-Ponce B, Marsch-Martínez N, Ugartechea-Chirino Y, Villajuana-Bonequi M, de Folter S, Azpeitia E, Dávila-Velderrain J, Cruz-Sánchez D, Garay-Arroyo A, de la Paz Sánchez M, Estévez-Palmas JM, Álvarez-Buylla ER. 2015. XAANTAL2 (AGL14) is an important component of the complex gene regulatory network that underlies Arabidopsis shoot apical meristem transitions. Molecular Plant 8: 796–813.

Serrano-Mislata A, Fernández-Nohales P, Doménech MJ, Hanzawa J, Bradley J, Madueño F. 2016. Separate elements of the TERMINAL FLOWER 1 cis-regulatory region integrate pathways to control flowering time and shoot meristem identity. Development 143: 3315–3327.

Simon R, Igeño MI, Coupland G. 1996. Activation of floral meristem identity genes in Arabidopsis. Nature 384: 59–62.

Wickland DP & Hanzawa Y. 2015. The FLOWERING LOCUS T/TERMINAL FLOWER 1 gene family: functional evolution and molecular mechanisms. Molecular Plant 8: 983–997.


About Flowering Highlights

Flowering Newsletter published by the Journal of Experimental Botany
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