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Interaction of LEAFY, AGAMOUS and TERMINAL FLOWER1 in maintaining floral meristem identity in Arabidopsis

François Parcy1,2,*, Kirsten Bomblies1,*,{dagger} and Detlef Weigel1,3,{ddagger}

1 Plant Biology Laboratory, The Salk Institute for Biological Studies, La Jolla, CA 92037, USA
2 Institut des Sciences du Végétal, CNRS, 91198 Gif-sur-Yvette Cedex, France
3 Department of Molecular Biology, Max Planck Institute for Developmental Biology, D-72076 Tübingen, Germany
* These authors contributed equally to this work
{dagger} Present address: Department of Genetics, University of Wisconsin, Madison, WI, USA



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  		Fig. 1. Floral reversion in ag-1 mutant backgrounds. (A) Wild-type flower with sepals (se), petals (pe), stamens (st) and carpels (ca) forming the central gynoecium. (B) LFY:VP16, intermediate phenotype. The outer whorl is occupied by carpelloid organs. Organs in whorl 2 are missing or replaced by stamens. (C) LFY:VP16, strong phenotype. The number of floral organs is reduced further. All of them are carpelloid, and no whorled structure is apparent. (D) ag-1. Stamens in whorl 3 are replaced by petals, and the central gynoecium by an internal flower that repeats the pattern of the primary flower. (E-G) LFY:VP16 ag-1, strong phenotype. Young flowers are similar to those of ag mutants and include petaloid sepals (E). In older flowers, a new inflorescence (inf) emerges from the center (F,G). (H) lfy-6/+ ag-1 flower from a plant grown in short days. After a few whorls of floral organs had formed, the flower reverted to an inflorescence. All plants were grown in long days except (H). Scale bars 1 mm.

 


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  		Fig. 2. Scanning electron micrographs of developing mutant and transgenic flowers. The top row shows inflorescence shoot apices (meristem indicated with an asterisk) surrounded by developing flowers. Numbers indicate floral stages (Smyth et al., 1990Go). (A,E,I,M) Wild type. (E) Stage 5 flower, with two sepals (se) dissected away to reveal the developing stamens (st) and the floral meristem (fm), which has begun to form the central gynoecium consisting of congenitally fused carpels. (I) Stage 7 flower, in which the floral meristem has terminated with the formation of carpels (ca). (M) Mature flower with four whorls or organs, including sepals, petals (pe), stamens and carpels. (B,F,J,N) Strong LFY:VP16 line. Note supernumerary organs in the first whorl (1st) of developing flowers (F). The floral meristem is enlarged compared to that of the wild type and is beginning to produce another set of four organ primordia. (J) Three partially fused carpels are found in the center, which appear to have almost spiral phyllotaxy. A floral meristem is still visible in the center. (N) A mature flower that consists of several carpels and carpelloid organs that lack a clear whorled arrangement. (C,G,K,O) ag-1. The floral meristem persists and produces many whorls of organs that develop into sepals and petals. The floral meristem is indicated by an asterisk in (O). (D,H,L,P) LFY:VP16 ag-1. After the meristem has produced several whorls of organs, it reverts to an inflorescence meristem (indicated by an asterisk) that produces secondary flowers (sf). Note the enlarged floral meristem in H. Scale bars 50 µm (A-D, I-L), 20 µm (E-H), and 500 µm (M-P).

 


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  		Fig. 3. Phenotypic effects of LFY:VP16 are dependent on endogenous LFY. Structures shown are ‘single flowers’ from a weak LFY:VP16 line. (A) In an otherwise wild-type background, the flowers of this line are similar to those of wild type. (B) In LFY:VP16 lfy-12, each flower consists only of congenitally fused carpels. (C,D) In LFY:VP16 lfy-12 /+ ag-1, single flowers are replaced by structures consisting of flower buds interspersed with floral organs. The first-whorl organs of the flower shown in C have fallen off; only secondary flowers remain. (E,F) In LFY:VP16 lfy-12 ag-1, only a small number of floral organs were produced before the floral meristem reverted to produce only floral buds. Scale bars 1 mm (A-C,F), and 3 mm (D,E).

 


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  		Fig. 4. Expression of AP1 RNA in sections of inflorescence apices of wild-type (A), strong LFY:VP16 (B), ag-1 (C), and strong LFY:VP16 ag-1 (E) plants (meristems indicated by asterisks). Numbers indicate floral stages (Smyth et al., 1990Go). (D,F) Sections of individual ag-1 (D) and LFY:VP16 ag-1 (F) flowers. In wild type AP1 is activated as soon as flowers arise and expressed throughout floral primordia until stage 2. In ag mutants, AP1 expression persists in the center of floral meristems (arrowhead in D). (E,F) In LFY:VP16 ag plants, AP1 RNA is eliminated from the center of floral meristem after only a few whorls of organs have formed (arrows). Note secondary flowers (sf) in F. The inset in F shows the central meristem in a fully reverted flower, with a pattern of AP1 expression similar to that of a wild-type inflorescence apex. Scale bar in F represents 50 µm for all panels, except for the inset in F (24 µm).

 


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  		Fig. 5. Expression of AG RNA in wild type (A,B), strong LFY:VP16 (C,D), ag-1 (E,F) and strong LFY:VP16 ag-1 (G,H). Left column shows sections of shoot apices with inflorescence meristems (indicated by asterisks) surrounded by young flowers. Right column shows sections of individual flowers. Numbers indicate floral stages (Smyth et al., 1990Go). AG is activated precociously and ectopically in LFY:VP16. (F,G) Mutant AG RNA persists in the center of ag-1 and LFY:VP16 ag-1 flowers (arrowheads). (H) Mutant AG RNA disappears from the center of LFY:VP16 ag-1 flowers only at a late stage, after the reverted meristem has begun to produce secondary flowers (inset in H, compare with inset in F, arrows). Scale bar in H represents 50 µm for all panels, except for insets in F and H (24 µm).

 


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  		Fig. 6. Expression of TFL1 RNA in wild type (A-C) and strong LFY:VP16 (D-F) plants. Left column shows sections of shoot apices with inflorescence meristems (indicated by asterisks). Middle and right columns show sections of individual flowers. Numbers indicate floral stages (Smyth et al., 1990Go). In wild type, TFL1 RNA is restricted to a group of subapical cells in the inflorescence meristem, and absent from flowers (arrowhead in A). In LFY:VP16 flowers, there is ectopic TFL1 expression, initially in a pattern similar to that in the shoot apical meristem (arrowheads in D,E). In the more advanced flower in (F), there is weak TFL1 expression at the tip of the gynoecium (arrow). Occasionally, as in this flower, there is also a small group of TFL1-expressing cells at the base of the central gynoecium (arrowhead), possibly indicating a group of persisting meristematic cells. Scale bar in F represents 50 µm (A,C,D,F), and 24 µm (B,E).

 


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  		Fig. 7. A mutation in TFL1 attenuates floral reversion in LFY:VP16 ag-1 plants. (A) tfl1-1 ag-1 inflorescence. The inflorescence has terminated with a single flower. Note that the most basal flower has formed in the axil of a leaf. (B) The floral phenotype of tfl1-1 ag-1, including that of this terminal flower, is the same as in ag-1 flowers. (C,D) Flowers from a strong LFY:VP16 ag-1 plant (either tfl1-1/TFL1 or TFL1/TFL1; not genotyped). After the flower has produced a variable number of whorls of organs, the floral meristem reverts to an inflorescence meristem (im), which produces only floral buds. (E-G) Modified flowers from a strong LFY:VP16 ag-1 tfl1-1 plant. Reversion to a true inflorescence that produces only secondary flowers is never observed, although the floral meristem produces many flowers interspersed with floral organs. In old flowers, fasciation is sometimes observed (G). Scale bars 1 mm (B,G,F), and 5 mm (A,C-E).

 


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  		Fig. 8. Two scenarios for LFY action during maintenance of floral meristem identity. Diagrams show levels of LFY activity and expression levels of shoot identity genes along with levels of an intermediate regulator. If LFY’s primary activity in this process is as a transcriptional activator, LFY:VP16 should be more potent than wild-type LFY, and reversion should not occur, because levels of shoot identity genes remain low. If LFY’s primary activity is as a transcriptional repressor, LFY:VP16 should have the opposite effect of wild-type LFY, and cause elevated shoot identity gene expression, similar to a reduction in LFY activity in lfy heterozygotes. In the latter case, a scenario without an intermediate activator is formally equivalent.

 

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