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. 2005 Oct;17(10):2661-75.
doi: 10.1105/tpc.105.035766. Epub 2005 Sep 9.

The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves

Paula Teper-Bamnolker  1 , Alon Samach
Affiliations

The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves

Paula Teper-Bamnolker et al. Plant Cell. 2005 Oct.

Abstract

The transition to flowering involves major changes in the shoot apical meristem and in the fate of existing leaf primordia. Transcripts of the Arabidopsis thaliana flowering-promoting gene FLOWERING LOCUS T (FT) are present in leaf tissue but can also promote flowering when artificially introduced into the meristem. FT may normally act in the leaf and/or the meristem, initiating or constituting a mobile flower-promoting signal. We studied FT-dependent events in the rosette leaf, some of which might precede or mimic events in the meristem and its primordia. We show FT-dependent transcript accumulation of the MADS box transcription factors FRUITFULL (FUL) and SEPALLATA3 (SEP3) in leaves. Abnormally high levels of FT further increase the expression of these genes, leading to morphological changes in the leaves. Loss of the flowering-time gene FD, as well as environmental conditions that delay flowering, reduce FT's effect on leaves via reduced activation of its targets. FUL, SEP3, and APETALA1 accumulation in the meristem is associated with and contributes to the transition to flowering. We propose that FT functions through partner-dependent transcriptional activation of these and as-yet-unknown genes and that this occurs at several sites. Organ fate may depend on both degree of activation and the developmental stage reached by the organ before activation occurs.

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Figures

Figure 1.
Figure 1.
Leaf Phenotypes of Pro35S:FT/TFT Plants. (A) to (C) Growth conditions affect leaf phenotypes of Pro35S:FT plants. Wild-type and Pro35S:FT plants were grown in a long-day growth room (A1 in Table 1; 23-d-old plants; [A]), a blue long-day chamber (A3 in Table 1; 18-d-old plants; [B]), and a short-day growth chamber (A4 in Table 1; 23-d-old plants; [C]). (D) Phenotypes of independent 22-d-old transgenic plants homozygous for Pro35S:TFT. All lines are early-flowering and small with very curled leaves. (E) A cauline leaf and the terminal inflorescence meristem of one of the transgenic Pro35S:TFT plants viewed by a scanning electron microscope. Note the severe leaf curling and the termination of the meristem. Dashed lines within panels border between different genotypes, grown together under identical conditions, and photographed separately at the same age. Bars = 1 cm in (A) to (D) and 2 mm in (E).
Figure 2.
Figure 2.
SEP3 and FUL Are Activated by FT in Leaves. Expression was measured by quantitative real-time RT-PCR (see Methods). Expression of each gene was calculated relative to β-TUBULIN (AT5G62690). Bars in (B) to (D) show standard error of the mean of three biological repeats. The experiment in (A) was performed at least twice, with similar results (see Supplemental Figure 3 online). (A) Comparison of 6-d-old seedlings from different genotypes grown under blue long days (A3 in Table 1). (B) Expression in rosette leaves of 30-d-old wild-type and Pro35S:FT plants grown under long days (A2 in Table 1). (C) Expression in rosette leaves of 30-d-old wild-type, ft-2, or fd-1 plants grown under long days (A2 in Table 1). Expression of AP1 is not shown due to low levels and high variance among samples. (D) Expression in rosette leaves of 30-d-old Pro35S:FT plants with or without a mutation in FD, grown under long days at 18°C (A2 in Table 1) or Pro35S:FT plants grown at 12°C.
Figure 3.
Figure 3.
Interaction of Pro35S:FT/TFT Plants with fd-1. (A) The fd-1 mutation suppresses leaf phenotypes of Pro35S:FT/TFT plants. Phenotypes of 21-d-old plants grown under white (top row, A4 in Table 1) or blue (bottom row, A5 in Table 1) short days (SDs). Dashed lines within panels border between different genotypes, grown together under identical conditions, and photographed separately at the same age. Bar = 1 cm. (B) to (D) Flowering time of Pro35S:FT plants and Pro35S:TFT#3 plants in a wild-type or fd-1 homozygous mutant background. The different growth conditions, blue long days (LDs; A3), white short days (A4), and blue short days (A5), are depicted in each panel. Total leaf number of wild-type plants (data not shown) is 7 in A3 (see Figure 6C) and >30 in A4 (Table 2; see Supplemental Table 1 online) and A5. Under all conditions, a mutation in FD suppresses early flowering by 0.5 to 1.5 leaves. The major effect of FD is on rosette leaf number. The difference between the Pro35S:FT and Pro35S:TFT#3 plants becomes more clear under white short days, perhaps due to lack of internal FT under these conditions. Flowering time is measured by counting rosette (gray) and cauline (black) leaves. Mean leaf number is shown ± se (n = 5 to 22).
Figure 4.
Figure 4.
Effect of Growth Temperature on FT/TFT Function. (A) and (B) Plants of different genotypes were grown at 23°C (A) or at 12°C (B) under otherwise similar short-day growth conditions (Table 1, B treatments). While low temperatures slightly increased leaf size of wild-type (Ler) plants, it severely increased leaf size and eliminated leaf curling of Pro35S:FT, Pro35S:TFT#3, and Pro35S:TFT#7. Note that cold temperatures had no noticeable effect on Pro35S:TFT#3 in fd-1 plants, besides a reduction in petiole length. Plants in (A) are 21 d old, and in (B), they are 26 d old. Dashed lines within panels border between different genotypes, grown together under identical conditions, and photographed separately at the same age. Bar = 1 cm. (C) Flowering time of Pro35S:FT and Pro35S:TFT#3 plants at different temperatures. Flowering time is measured by counting rosette (gray) and cauline (black) leaves. Both genotypes responded to lower temperatures by an increase in rosette leaf number. Since no corresponding reduction in cauline leaf number occurred in Pro35S:FT plants, flowering was significantly delayed. #, repeat number of experiment. Mean leaf number is shown ± se (n = 5 to 22).
Figure 5.
Figure 5.
SEP3 Is the Rate-Limiting Factor in FT/TFT-Dependent Leaf Curling. (A) Phenotypes of 14-d-old F1 plants grown under blue long days (A3 in Table 1) from a cross between Pro35S:FT and sep3-2 (in Col-0) or Col-0. Loss of leaf phenotypes are noticed in both rosette (left) and cauline (right) leaves. (B) Phenotypes of 14-d-old F1 plants grown under the same conditions as in (A), from a cross between Pro35S:TFT#7 and sep3-2 or Col-1. Note the complete absence of leaf curling by losing one allele of SEP3 under conditions that normally cause strong curling. (C) Phenotypes of 35-d-old plants grown under short days (A4 in Table 1) homozygous for Pro35S:TFT#7 or Pro35S:TFT#7 in sep3-2. (D) Phenotypes of 15-d-old F1 plants grown under short days (A4 in Table 1). Note the increase in curling in the cross to Pro35S:SEP3. Dashed lines within panels border between different genotypes, grown together under identical conditions, and photographed separately at the same age. All bars = 1 cm.
Figure 6.
Figure 6.
Flowering-Time Phenotypes Caused by Mutations in SEP3 and FUL. (A) Flowering time under blue long days (A3 in Table 1) of segregating F2 populations from a cross of Pro35S:TFT#7 to Col-0 or to sep3-2. Graph shows percentage of plants flowering with different amounts of rosette leaves. Segregation of both Ler and Col-0 is shown as a line graph. Arrow shows that all Pro35S:TFT#7 (in Ler) plants flowered with two rosette leaves. In the segregating F2 population of the control cross to Col-0, 55%, rather than the expected 75%, of the plants flowered with less than three rosette leaves (see Supplemental Table 3 online). A recessive suppressor should reduce the ratio of early-flowering plants to 56% [0.75(Pro35S:TFT+/+;+/−) × 0.75(Ler +/+;+/−)]. Above the noise created by the Col-0 background, loss of SEP3 clearly affected flowering time of the segregating Pro35S:TFT population. The percentage of plants that flowered with less than three rosette leaves was reduced from 55 to 36%. The average number of rosette leaves increased by 1.5 leaves in the whole population and from 2.36 to 3.37 in the earliest 75th percentile (likely including at least one copy of Pro35S:TFT). (B) Flowering time of a line homozygous for both Pro35S:TFT#7 and sep3-2 under short days (A4 in Table 1). Plants are late-flowering compared with Pro35S:TFT#7. See Figure 5C for picture of plants. (C) A mutation in FUL delays flowering in a wild-type and Pro35S:FT background. Flowering time of wild-type, ful-1, Pro35S:FT, or F2 plants from a cross of Pro35S:FT to ful-1. Early-flowering plants containing at least one copy of Pro35S:FT (+/) were separated to those containing (+/) or not containing (−/−) an intact FUL allele. The latter were identified by their distinct ful-1 silique phenotype and verified by PCR. Plants were grown under the same conditions as in (A). See Figure 7D for additional phenotypes of these plants. Mean leaf number is shown ± se (n = 5 to 46).
Figure 7.
Figure 7.
Interactions with AP1 and FUL. (A) Phenotypes of 35-d-old F3 plants grown under short days (A4 in Table 1) from a cross between Pro35S:TFT#7 and ap1-7. Both plants are early-flowering, and the plant on the left is homozygous for ap1-7 (see floral phenotype). Leaves of both plants are curled. (B) Phenotypes of 23-d-old plants grown under similar conditions. The inflorescence meristem in Pro35S:TFT#7 × Pro35S:AP1 F1 plants is completely transformed into a single flower, and leaves are severely curled. (C) GUS staining of first rosette leaves from 19-d-old plants (containing the ful-1 allele) grown under blue long days (A3 in Table 1). Overexpression of FT causes higher expression of the FUL promoter in leaves. (D) Phenotypes of 18-d-old plants grown under blue long days. The ful-1 mutation causes late flowering and abnormally large cauline leaves in a wild-type and Pro35S:FT background. Dashed lines within panels border between different genotypes, grown together under identical conditions, and photographed separately at the same age. Bars = 1 cm.
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