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
Present address: Department of Genetics, University of Wisconsin, Madison, WI, USA
Author for correspondence (e-mail: weigel{at}weigelworld.org)
Accepted 22 February 2002
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SUMMARY |
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Key words: Arabidopsis thaliana, Flower development, Meristem identity, LEAFY, Floral reversion
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INTRODUCTION |
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In many species, including Arabidopsis, a floral inductive stimulus is required only transiently to cause a stable transition from vegetative to reproductive development. In contrast, a floral inductive stimulus is required continuously in several other species, and its absence can cause either inflorescence or floral reversion. In inflorescence reversion, a shoot ceases to produce flowers and reverts to the formation of leaves with axillary vegetative shoots. In floral reversion, individual flowers stop producing floral organs and initiate vegetative organs (Anthony et al., 1996; Battey and Lyndon, 1984
; Battey and Lyndon, 1986
; Battey and Lyndon, 1988
; Battey and Lyndon, 1990
; Pouteau et al., 1997
; Pouteau et al., 1998
). The latter observation indicates that floral meristem identity not only needs to be established, but also maintained.
Both inflorescence and floral reversion are rare in wild-type Arabidopsis (Bowman, 1994; Laibach, 1951
), but floral reversion has been described in several mutant backgrounds (e.g., Bowman et al., 1993
; Clark et al., 1993
; Mizukami and Ma, 1997
; Okamuro et al., 1996
). While these instances of floral reversion differ in details, they all have in common that the flowers do not revert to a leaf-producing vegetative shoot meristem, but to a flower-producing inflorescence meristem.
In contrast to the establishment of floral meristem identity, its maintenance has received relatively little attention. It is particularly intriguing that LFY, a cardinal factor in establishing floral meristem identity, is also required for its maintenance (Okamuro et al., 1996). It is unclear how direct this effect of LFY is, especially since LFY is a direct activator of the homeotic gene AGAMOUS (AG), which itself is required for stable floral meristem identity (Busch et al., 1999
; Mizukami and Ma, 1997
; Okamuro et al., 1996
). lfy mutants are of limited use in studying this process, because, in these plants, floral meristem identity is not properly established in the first place. Here, we use a combination of mutants and transgenic plants to dissect the role of LFY in the maintenance of floral meristem identity. First, we show that LFY maintains floral meristem identity independently of homeotic gene activation. Second, we provide evidence that LFY is likely to perform this function by acting as a transcriptional repressor of shoot identity genes.
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MATERIALS AND METHODS |
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Wild type was either Landsberg erecta (Ler) or Columbia (Col-0, Col-7). ag-1 and lfy-6 mutants in Ler (Bowman et al., 1989; Weigel et al., 1992
), and tfl1-1 and lfy-12 mutants in Col-0 have been described previously (Huala and Sussex, 1992
; Shannon and Meeks-Wagner, 1991
). LFY:VP16 lines DW245.2.7 and DW245.2.25 (strong phenotype as homozygotes), and DW245.2.37 (weak phenotype) were in the Col-7 background (Parcy et al., 1998
). Additional transgenic plants were generated by vacuum infiltration of Col-7, using vectors pDW245 (for LFY:VP16) and pFP17 (for LFY:mVP16) (Bechtold et al., 1993
; Parcy et al., 1998
). dCAPS genotyping of ag-1 heterozygotes has been described elsewhere (Neff et al., 1998
). lfy-6 and lfy-12 heterozygous and homozygous plants were identified by CAPS genotyping (Konieczny and Ausubel, 1993
) as described previously (Blázquez et al., 1997
) (http://www.weigelworld.org).
Plant analysis
Methods for in situ hybridization, scanning electron microscopy and light microscopy were according to Parcy and colleagues (Parcy et al., 1998). The TFL1 probe was derived from p129D7 (Bradley et al., 1997
).
Any flower that produced secondary flowers interior to the first whorl of organs was considered to be reverting. Partially reverted flowers continued to produce floral organs, while completely reverted flowers did not, and produced only secondary flowers.
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RESULTS |
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The floral phenotype of LFY:VP16 plants is mostly due to ectopic AG expression and consists of reduced floral organs and conversion of petals to stamens and sepals to carpels (Fig. 1A-C) (Parcy et al., 1998). Because there are no obvious signs of floral reversion in mature LFY:VP16 flowers, we studied developing LFY:VP16 flowers using the scanning electron microscope. Initiation of floral meristems in LFY:VP16 plants was similar to wild type, but deviated from wild type subsequently. Instead of initiating four first-whorl organs in a cruciform manner, LFY:VP16 produced an irregular number of first-whorl organs, often more than four (Fig. 2A,B,F). In wild type, the formation of the first whorl is followed by the initiation of petal primordia in the second whorl and stamen primordia in the third whorl (Smyth et al., 1990
). Between the stamen primordia, floral meristem development is terminated by formation of the domed gynoecium primordium, which gives rise to the congenitally fused carpels (Fig. 2E,I). In LFY:VP16, there was no evidence of second- or third-whorl primordia demarcating the gynoecial dome (Fig. 2F,J). Instead, the meristem continued to grow apically, and new, fused primordia were initiated in a pattern that was at least partially spiral (Fig. 2J). These primordia eventually fused to produce an abnormal gynoecium that had an excess of style tissue at the expense of valve tissue (Fig. 2M,N). The abnormal early development of LFY:VP16 flowers, with continued proliferation of the floral meristem and partially spiral phyllotaxis, suggests a meristem defect in these flowers. Specifically, the floral meristem may have partial shoot identity.
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Scanning electron microscopy of developing LFY:VP16 ag flowers revealed that the number of first-whorl organs was irregular, as with LFY:VP16 AG+ flowers, and often greater than four (Fig. 2C,D). In contrast to LFY:VP16 AG+ or non-transgenic ag flowers, only a few whorls of floral organs were produced, before the floral meristem reverted to a shoot meristem and produced new floral primordia on its flanks (Fig. 2G,H,K,L). Second-order flowers repeated the pattern of the primary flowers, with a few whorls of floral organs followed by the production of higher-order floral primordia (Fig. 2L,P).
LFY:VP16 is not a neomorphic allele
A concern with any gain-of-function allele is that it has activity unrelated to the normal function of the gene, or neomorphic activity (Muller, 1932). This would be the case, for example, if LFY:VP16 interacted with promoters or proteins that are not targets of unmodified LFY. A hallmark of neomorphic mutations is that they are not affected by the dosage of the wild-type gene. We have previously shown that the homeotic organ conversions in LFY:VP16 flowers are strongly dependent on the copy number of endogenous wild-type LFY, indicating that this phenotype is not due to neomorphic activity of LFY:VP16 (Parcy et al., 1998
). To confirm that LFY:VP16 similarly does not act as a neomorph with respect to floral reversion, but rather as an antimorph, we studied a weak LFY:VP16 line, which does not show any homeotic organ conversions in a wild-type background, but produces an intermediate phenotype when in a lfy heterozygous background, and a strong phenotype when in a lfy homozygous mutant background (Fig. 3B) (Parcy et al., 1998
). When introduced into an ag mutant background, this LFY:VP16 line showed no evidence of reversion. However, when we reduced the copy number of wild-type LFY from two to one in the ag line carrying the weak LFY:VP16 insertion, frequent reversion was observed (Fig. 3C,D). An even more dramatic reversion was seen in a lfy homozygous mutant background; the floral meristem stopped producing floral organs and gave rise only to new floral buds (Fig. 3E,F). This observation demonstrates that LFY:VP16 and endogenous LFY compete for the same targets in the reversion process, as they do in specifying floral organ identity. We also note that, in a lfy mutant background, LFY:VP16 produces a phenotype that is very different from weak loss-of-function alleles, for which an extensive allelic series has been described (Huala and Sussex, 1992
; Levin and Meyerowitz, 1995
; Schultz and Haughn, 1991
; Schultz and Haughn, 1993
; Weigel et al., 1992
).
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As a further test to determine whether the LFY:VP16 effect was indeed due to the altered transcriptional activation potential conferred by the VP16 fusion, we transformed ag heterozygotes with the LFY:mVP16 construct, which carries a truncated and inactive variant of the VP16 activation domain (Parcy et al., 1998). None of 12 LFY:mVP16 ag primary transformants showed any sign of reversion. In contrast, 3 out of 4 LFY:VP16 ag primary transformants showed complete or partial reversion. Fishers exact test shows the two genotypes to be significantly different regarding reversion with P=0.007, from which we conclude that the VP16 transcriptional activation potential is necessary to induce floral reversion. Taken together with the observation that reversion in an ag background is observed both in plants that are compromised in wild-type LFY function (in lfy heterozygotes) and in LFY:VP16 plants, we conclude that LFY:VP16 is a dominant-negative allele of LFY with respect to floral reversion.
Expression of floral markers in LFY:VP16 ag
We extended our morphological analysis of reverting flowers in LFY:VP16 ag by analyzing the expression of two floral marker genes, AP1 and AG. AP1 is initially activated throughout floral meristems, but becomes confined to the two outer whorls of organs, sepals and petals, from stage 3 on (Fig. 4A) (Mandel et al., 1992). Repression of AP1 at this time is due to activation of AG in the center of the flowers (Fig. 5A) (Drews et al., 1991
; Gustafson-Brown et al., 1994
).
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AG, which is expressed in the center of wild-type flowers, is activated precociously and throughout young flowers in LFY:VP16 (Fig. 5C) (Parcy et al., 1998). In the proliferating meristems of ag flowers, mutant AG RNA continues to be expressed (Fig. 5E,F) (Gustafson-Brown et al., 1994
). Initially, a similar pattern was seen in LFY:VP16 ag flowers, but in older flowers, mutant AG RNA disappeared from the central meristem (Fig. 5H inset), indicating that it had lost floral identity. The disappearance of AG RNA from the center of flowers, however, appeared to be delayed relatively to that of AP1.
Role of TFL1 in LFY:VP16-induced floral reversion
One of the few cloned genes known to promote shoot meristem identity (or repress floral meristem identity) is TFL1 (Bradley et al., 1997; Ratcliffe et al., 1998
; Ratcliffe et al., 1999
). Having shown that LFY:VP16 has a dominant-negative effect on the maintenance of floral meristem identity, we wondered whether TFL1 might mediate this effect. In wild type, TFL1 is expressed in inflorescence meristems, but not developing flowers (Fig. 6A-C) (Bradley et al., 1997
). Surprisingly, we found that TFL1 was activated in LFY:VP16 floral primordia, even though there was little morphological evidence for reversion in these flowers (Fig. 6D,E). In older flowers, weak ectopic TFL1 expression was observed near the tip of the gynoecium, and, less often, in a group of cells at the base of the abnormal gynoecium (Fig. 6F).
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DISCUSSION |
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Floral reversion in Arabidopsis
Two types of situations in which floral meristems behave as inflorescence meristems have been described in Arabidopsis. One example is provided by ap1 cal double mutants, or even more strikingly, ap1 cal ful triple mutants, in which the inflorescence shoot meristem produces primordia that often behave very similarly to secondary inflorescence meristems (Bowman et al., 1993; Ferrándiz et al., 2000
). This phenotype is reminiscent of floral reversion in many other species, typically induced by the removal of floral inductive cues (Battey and Lyndon, 1990
). The ap1 cal and ap1 cal ful phenotypes are characterized by a failure to establish robust LFY expression, with concomitant ectopic TFL1 expression in lateral meristems. That changes in LFY and TFL1 expression are responsible for the ap1 cal and ap1 cal ful defects has been confirmed by demonstrating that overexpression of LFY or inactivation of TFL1 strongly suppresses meristem proliferation in ap1 cal and ap1 cal ful mutants (Bowman et al., 1993
; Ferrándiz et al., 2000
). On the other hand, overexpression of AG, which acts downstream of LFY, is insufficient to suppress any aspect of the ap1 cal ful phenotype (Ferrándiz et al., 2000
).
In contrast to ap1 cal or ap1 cal ful mutants, other mutants produce floral primordia that revert to an inflorescence shoot meristem only after several whorls of floral organs have been produced. This group of mutants includes ag mutants and lfy heterozygotes grown under short days, and ap1 clv1 mutants (Clark et al., 1993; Okamuro et al., 1996
). Similarly, LFY:VP16 ag floral meristems produce at least two whorls of organs before reverting to an inflorescence meristem. Also in contrast to ap1 cal or ap1 cal ful, inactivation of TFL1 has only modest effects on floral reversion of LFY:VP16. Together, these observations indicate that the LFY:VP16 allele uncouples the role of LFY in establishing and maintaining floral meristem identity.
Role of LFY in maintaining floral meristem identity
How does LFY contribute to the maintenance of floral meristem identity? LFY is a DNA-binding protein that directly regulates transcription of downstream genes (Busch et al., 1999; Parcy et al., 1998
; Wagner et al., 1999
). One of these targets is AG, which represses floral reversion (Mizukami and Ma, 1997
; Okamuro et al., 1996
). The additive effects of reducing LFY copy number and inactivating AG on floral reversion indicate that LFY does not maintain floral meristem identity solely by ensuring a sufficient level of AG expression. This result is consistent with the finding that AG RNA expression is not obviously altered in young flowers of lfy/LFY plants grown in short days (Okamuro et al., 1996
).
There are two alternative explanations for the increased floral reversion in ag/ag lfy/LFY or ag/ag LFY:VP16 plants. One possibility is that LFY and AG act entirely independently on floral reversion. Another possibility is that LFY acts as an AG substitute to maintain floral meristem identity in ag mutants. Indeed, LFY continues to be expressed in the center of (long-day grown) ag floral meristems (D. W., unpublished results). If maintenance of high levels of LFY expression in these meristems is compromised in short days, this could cause floral reversion in ag mutants, further exacerbated when LFY copy number is reduced.
LFY:VP16 is an activated version of LFY that can activate targets such as AG and AP1 more strongly than wild-type LFY and that can therefore be classified as a hypermorphic allele with respect to activation of these targets (Parcy et al., 1998). In contrast, LFY:VP16 appears to be an antimorphic allele with respect to maintenance of floral meristem identity, because it acts in a manner opposite to that of wild-type LFY.
Considering the evidence for LFY:VP16 being a transcriptional activator and the fact that at least one shoot identity gene, TFL1, is derepressed in LFY:VP16 floral meristems, we postulate that transcriptional repression by LFY is involved in preventing reversion of a floral to an inflorescence meristem. If we assume further that floral reversion involves the activation of a hypothetical set of shoot identity genes, we can envision two scenarios through which LFY affects these genes (Fig. 8). In the first scenario, LFY negatively regulates shoot identity genes indirectly by activating a transcriptional repressor that downregulates or represses shoot identity genes. In the second scenario, LFYs primary effect is transcriptional repression, either through direct repression of shoot identity genes, or though repression of a positive regulator of shoot identity genes. In both cases, reducing LFY activity in lfy heterozygotes would lead to floral reversion because of increased activity of shoot identity genes. However, if LFYs primary effect was transcriptional activation of a hypothetical reversion repressor, LFY:VP16 should be even more effective than wild-type LFY in activating this repressor, and we would not expect reversion. In contrast, if LFYs primary effect were repression of a hypothetical reversion activator, LFY:VP16 would have an opposite effect from wild-type LFY. Because LFY:VP16 acts in a dominant-negative fashion floral reversion is observed both when wild-type LFY is reduced (in lfy heterozygous plants) and in LFY:VP16 plants we believe it most plausible that LFYs primary effect in maintaining floral meristem identity is transcriptional repression.
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Which are the genes repressed by LFY to prevent floral reversion? TFL1 is derepressed both in lfy mutants (Ratcliffe et al., 1999) and in LFY:VP16 plants (this work). However, although the TFL1 promoter contains putative LFY binding sites, these are not bound by LFY in vitro (M. A. Busch and D. W., unpublished data), suggesting either that TFL1 is not a direct target of LFY, or that other proteins are required for interaction of LFY with TFL1 regulatory sequences. To further understand the interaction of LFY and TFL1, it will be necessary to define the regulatory sequences sufficient for normal TFL1 expression.
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ACKNOWLEDGMENTS |
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