Changing the spatial pattern of TFL1 expression reveals its key role in the shoot meristem in controlling Arabidopsis flowering architecture

Abstract

Models for the control of above-ground plant architectures show how meristems can be programmed to be either shoots or flowers. Molecular, genetic, transgenic, and mathematical studies have greatly refined these models, suggesting that the phase of the shoot reflects different genes contributing to its repression of flowering, its vegetativeness ('veg'), before activators promote flower development. Key elements of how the repressor of flowering and shoot meristem gene TFL1 acts have now been tested, by changing its spatiotemporal pattern. It is shown that TFL1 can act outside of its normal expression domain in leaf primordia or floral meristems to repress flower identity. These data show how the timing and spatial pattern of TFL1 expression affect overall plant architecture. This reveals that the underlying pattern of TFL1 interactors is complex and that they may be spatially more widespread than TFL1 itself, which is confined to shoots. However, the data show that while TFL1 and floral genes can both act and compete in the same meristem, it appears that the main shoot meristem is more sensitive to TFL1 rather than floral genes. This spatial analysis therefore reveals how a difference in response helps maintain the 'veg' state of the shoot meristem.

Keywords: Architecture; TFL1.; expression; flowering; identity; meristem.

Fig. 1.

Ectopic TFL1 affects plant organ numbers. The number of rosette leaves (RLs), cauline leaves (CLs), I1* structures (shoots without subtending CLs or ap1-like structures), and flowers (Fs) made by the main shoot were recorded for wild-type (WT) Arabidopsis or tfl1-1 mutants containing pANT::TFL1, pLFY::TFL1, or pAP1::TFL1. WT plants containing p35S::TFL1 and ap1-12 mutants were also analysed. Numbers represent the average of 23–54 plants with standard deviations as shown. The solid black bars in (F) in the tfl1 background represent termination of the main shoot by conversion to a flower.

Fig. 2.

Plant architectures due to TFL1 expression. (A–D) Mature plants of Arabidopsis WT (A) or WT containing pANT::TFL1 (B), pLFY::TFL1 (C), or pAP1::TFL1 (D). In (A), the WT phases V, I1, and I2 are indicated. (E, F) Young tfl1-1 mutant plants already bolted with terminal flowers (E) compared with tfl1 containing pAP1::TFL1 at the same age of 16 d (F). (G–I) Mature plants showing tfl1-1 (G) or tfl1-1 containing pLFY::TFL1 (H) or pAP1::TFL1 (I). the insert in (H) shows that these plants eventually make normal flowers and terminate. Insert in (I) shows CLs with axillary ap1-like structures. Scale bars=1cm.

Fig. 3.

Early TFL1 expression patterns in the WT background. (A–E) TFL1 expression in the vegetative phase (6-day-old plants) of the WT (A) or the WT containing pANT::TFL1 (B), pLFY::TFL1 (C), pAP1::TFL1 (D), or p35S::TFL1 (E). For example, in (A), the shoot apical meristem (SAM) and rosette leaves (RL) generated by this meristem are indicated. (F–J) TFL1 expression in early to late I1 phase (10- to 12-day-old plants) of the WT (F) or the WT containing pANT::TFL1 (G), pLFY::TFL1 (H), pAP1::TFL1 (I), or p35S::TFL1 (J). Examples of inflorescence SAM, axillary meristems (AxM) in axils of cauline leaves (CL) and floral meristems (FM) are highlighted. All images were obtained with the same probes and signals developed for the same time. Signal is seen as a purple stain on a pale/pink background. Scale bar=100 μm.

Fig. 4.

Early TFL1/tfl1-1 expression patterns in the tfl1-1 background. (A–D) TFL1/tfl1-1 expression at 6 d in tfl1-1 (A) or tfl1-1 containing pANT::TFL1 (B), pLFY::TFL1 (C), or pAP1::TFL1 (D). The shoot apical meristem is generating rosette leaves (RL). (E–H) TFL1/tfl1-1 expression at 12–14 d in the I1–I2 phase of tfl1-1 (E) or tfl11-1 containing pANT::TFL1 (F), pLFY::TFL1 (G), or pAP1::TFL1 (H). In tfl1, the SAM has already converted to a terminal flower (TF) while the other lines have TFL1/tfl1-1 mRNA in the shoot apical meristems but are still not terminating at this stage. All images were obtained with the same probes and signals developed for the same time. Signal is seen as a purple stain on a pale/pink background. Scale bar=100 μm.

Fig. 5.

TFL1 and floral gene expression patterns in inflorescences in the WT background. (A, B) WT flowering shoots in the I2 phase at 21 d showing expression of TFL1 (A) or AP1 (B). Inserts in TFL1 (A) and LFY (B) at 17 d. (C, D) WT plants containing pLFY::TFL1 at 16 d showing TFL1 (C) and LFY (D) expression. Inserts show another transgenic line at 21 d. (E, F) WT plants containing pAP1::TFL1 at 21 d showing TFL1 (E) and (AP1) expression. Inserts show another line. (G–I) WT plants containing pANT::TFL1. Expression of TFL1 in a young tertiary shoot (G). Expression of TFL1 in an older secondary shoot (H) and AP1 expression (I). Shoot apical meristem (SAM), flower (F), and corresponding mRNA signals seen as a purple stain on pale blue/white tissue background. Scale bar=100 μm.

Fig. 6.

Expression patterns in tfl1 mutant backgrounds. (A, B) Young 10-day-old tfl1 mutants showing tfl1-1 (A) and LFY (B) expression. The insert in (B) shows plants just starting to bolt and ectopically expressing LFY in the shoot. (C, D) Ten-day-old day tfl1 plants containing pLFY::TFL1 showing TFL1/tfl1-1 (C) and absence of LFY (D) expression. (E, F) Older tfl1 plants containing pLFY::TFL1 at 17 d showing TFL1/tfl1-1 (E) and LFY (F) expression. The left insert in (E) shows expression at 20 d in another line in an ap1-like structure. The right insert shows that TFL1 expression is largely limited to the shoot meristem in ap1 mutants. (G, H) At 21 d, tfl1 mutants containing pAP1::TFL1, showing TFL1/tfl1-1 (G) and AP1 (H) expression. Inserts in (G) show other examples. Corresponding mRNA signals seen as a purple stain on pale blue/white tissue background. Scale bars=100 μm.