JXB Advance Access originally published online on September 27, 2006
Journal of Experimental Botany 2006 57(13):3415-3418; doi:10.1093/jxb/erl159
Floral Signalling |
The control of flowering in time and space
Department of Cell and Developmental Biology, John Innes Centre, Colney Lane, Norwich NR4 7UH, UK
* To whom correspondence should be addressed. E-mail: philip.wigge{at}bbsrc.ac.uk
Received 4 May 2006; Accepted 18 August 2006
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Abstract |
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 Top Abstract IntroductionPhotoperiodic induction of...FT signallingReferences |
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The transition to flowering is one of the most important developmental decisions made by plants. Classical studies have highlighted the importance of photoperiod in controlling flowering time. More recently, the identification of mutants specifically affected in the photoperiod pathway in the model system Arabidopsis thaliana has enabled the flowering time pathways to be placed in a molecular context. This review highlights recent advances in understanding how photoperiod signals (perceived in the leaves) act at the apex of the plant where the floral stimulus is perceived. The photoperiod pathway acts predominantly through the gene CONSTANS to activate the small signalling molecule FT. While FT transcription is induced in the leaves, it is essential that FT protein is present at the apex of the plant. FT at the apex interacts with the transcription factor FD to induce flowering.
Key words: Arabidopsis, FD, florigen, flowering, FT
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Introduction |
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TopAbstractIntroductionPhotoperiodic induction of...FT signallingReferences |
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Flowering is one of the most important decisions during plant development. The control of flowering time and its intimate connection to environmental factors has intrigued and puzzled scientists for many years (Quetelet, 1842). Classical early studies that focused on the contribution of daylength to control flowering time demonstrated that plants have different requirements for floral induction, and can be classified as either short day, long day or daylength neutral with respect to flowering (Thomas and Vince-Prue, 1997). Experiments from the 1920s onwards demonstrated the existence of a graft-transmissible substance produced in the leaves in response to daylength; this mysterious substance was called florigen and postulated to be able to promote the switch to reproductive development. Despite decades of careful work, it proved impossible to purify the elusive active ingredient biochemically (Zeevaart, 1976). Significant progress was again made when the problem of flowering time was pursued in the tractable genetic model system Arabidopsis thaliana (thale cress). Forward genetic screens to isolate late-flowering mutants provided a cornucopia of genes for analysis. Perhaps surprisingly, rather than a single ‘florigen’ dozens of loci, all playing a role in the control of the floral transition, were identified (Koornneef, 1991). Subsequent genetic analyses enabled these to be classified into the photoperiod, vernalization, autonomous, or gibberellic acid (GA) pathways. These studies allowed an elaborate and detailed visualization of interconnected genetic networks to be described (Blazquez, 2000). Such pathways provided a very useful consolidation of the different components, but in themselves raised two conceptual challenges: how is information from various cues integrated during the decision to flower and how can the complex changes occurring in space and time at the plant apex be understood as it develops?
Firstly, given that multiple pathways affect the floral transition, it becomes essential to understand how the different pathways communicate with each other and integrate their output signal. An important conceptual advance was the proposal of floral pathway integrators (FPIs) that act to integrate flowering signals and serve as gates to activate the flowering pathway (Blazquez and Weigel, 2000; Simpson and Dean, 2002). The floral transition has also to be intimately connected with additional events affecting the whole organism, such as internode elongation, carbon resource mobilization, and leaf development and specification. These changes are subject to hormonal control, and there is evidence for hormones, in particular GA, playing a role in the floral transition (Achard et al., 2004; Blazquez and Weigel, 2000).
Secondly, the evocation of flowering occurs in a very dynamic and complex spatial pattern at the apex. Cells moving down the flanks of the shoot meristem are activated to form primordia. These are initially specified as leaves during vegetative development, but develop as flowers following the reproductive transition. The developmental fate of primordia is, however, flexible, as emerging organs that would otherwise form leaves give rise to flowers under a strong photoperiod induction (Hempel et al., 1998). Furthermore, the competence of the apex to respond to floral inducing signals increases with the age of the shoot apical meristem (SAM) (Blazquez et al., 1997). How these developmental changes are closely co-ordinated in time and space is still poorly understood (Parcy, 2005).
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Photoperiodic induction of flowering |
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TopAbstractIntroductionPhotoperiodic induction of...FT signallingReferences |
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Arabidopsis flowers rapidly in response to photoinductive cues. For plants grown under non-inductive short days, a single long day photoperiod is sufficient to trigger flowering (Corbesier et al., 1996). The use of photoinduction to trigger the floral transition in a synchronized fashion is a valuable tool for studying floral induction. In a series of key experiments, Hempel et al. (1998) demonstrated the remarkable developmental plasticity of the apex to inductive signals. Primordia emerging at the flanks of the shoot apex, initially programmed to become leaf/paraclade tissue can instead be converted into floral meristems by shifting a plant from short days to long days. The ability of floral inductive signals to alter the developmental fate of emerging primordia was shown to be dependent on the competence of the apex to respond, which is itself the output of the level of the transcription factor LEAFY. By altering the copy number of LEAFY under its own promoter or with heterozygous lfy lines, changes of LFY level led to a proportionate change in the competence of the apex to undergo the floral transition (Blazquez et al., 1997). Using global expression profiling, it was possible to characterize the transcriptional changes in genes throughout the apex in the transition from vegetative to reproductive development. It was shown that co and ft mutants display nearly identical reductions in the expression of key floral homeotic genes on floral induction, while in the lfy background the effects are more subtle (Schmid et al., 2003).
While LEAFY is expressed at the apex and provides competence to respond to floral inductive signals, the photoperiod pathway is primarily active in the leaves. The isolation of constitutively late-flowering mutants, regardless of photoperiod, enabled the genetic characterization of the long-day pathway in Arabidopsis. Subsequent cloning of the genes involved and elegant biochemical studies have led to close support for the coincidence model. In this model, CO mRNA oscillates diurnally, reaching a peak about 12 h after the initiation of daylight (Suarez-Lopez et al., 2001). Under short-day conditions the CO mRNA peak occurs in the dark, and CO protein, which is only stable in the light is unable to accumulate (Valverde et al., 2004). Under long-day conditions however, CO mRNA peaks in the light and the translated protein reaches a significant level since it is stabilized in the light (Valverde et al., 2004). CO protein is then able to activate its target genes. Thus the control of CO occurs at both the transcriptional and protein level. It is now clear, that control of CO transcription as an output of the circadian clock is essential for the diurnal cycling of a plant. A number of clock genes, including GI, LHY, and CCA1 are responsible for controlling CO transcript levels. Interestingly, CO is transcribed at the plant apex as well as in the vasculature of the leaves. In leaves, a very important CO output has been shown to be the gene FT. ft loss of function alleles are late flowering, while the overexpression of FT causes very early flowering (Kardailsky et al., 1999; Kobayashi et al., 1999). Consistent with FT being activated by CO, the FT expression is largely confined to the leaf vasculature (Takada and Goto, 2003). The polycomb protein TFL2 plays an important role in preventing activation of FT at the shoot apex, where CO is also present (Takada and Goto, 2003). Ectopic CO overexpression in the complete loss of function background ft-10, can almost completely suppress the early flowering phenotype, suggesting that FT is the major output of CO (Yoo et al., 2005). Consistently, profiling experiments with plants moved from short days to long days have shown that FT is the only gene specifically up-regulated rapidly in leaves in a CO-dependent manner (Wigge et al., 2005). The specific expression of CO in vasculature is sufficient to stimulate rapid flowering in a graft transmissible fashion. These observations suggested that a signal downstream of CO is sufficient to stimulate flowering.
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FT signalling |
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TopAbstractIntroductionPhotoperiodic induction of...FT signallingReferences |
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Unlike many of the flowering time genes, which are transcription factors, FT has no obvious biochemical function from its primary amino acid sequence. Although FT belongs to a highly conserved family of small (20 kDa) globular proteins, the RKIPs found in all the major kingdoms (Yeung et al., 1999), there are no obvious functional domains present. It could be shown by two-hybrid analysis that FT interacts with the transcription factor FD. fd mutants are late flowering and significantly suppress the early phentoype of 35S FT. FD is expressed on the flanks of the shot apical meristem, in a region where flower primordia are initiated. Although FD is expressed in vegetatively growing tissue, it is up-regulated on floral induction. In the presence of FT, FD is able to induce a number of important target genes including APETALA1 (AP1) and FRUITFULL (FUL). The expression domain of FD suggests why ectopic FT is able to induce precocious, but not ectopic AP1 induction: FT action requires the presence of FD transcription factor. In this model, the FD expression domain provides the spatial constraints on FT signalling. The expression of FT is limiting for FD activity, however, and since FT is transcribed in the leaves, this raises the important issue of how FT protein moves to the FD domain in the apex. In an elegant experiment, FT was expressed from an heat-inducible promoter and it could be demonstrated that a single heat shock is sufficient to detect FT mRNA in tissue dissected from the apex as measured by qRT PCR (Huang et al., 2005).
The demonstration that FT mRNA is transcribed in the leaves yet acts at the apex suggests that, in this case, FT has at least some of the properties of the elusive ‘florigen’. Although the large number of genes that affect flowering time may appear overwhelming, it is becoming apparent that having a molecular understanding of their function is essential for understanding how they operate in the plant. Despite these exciting breakthroughs, many interesting questions remain to be answered. Given that FT signalling is important for controlling the floral transition in distantly related plants such as rice (Hayama et al., 2003; Ishikawa et al., 2005), it will be especially interesting to see if such movement can be observed in other systems and whether other plants rely more on additional signals. Although the binding of FT to FD appears critical for FD activation, the mechanistic basis of why this should be the case is not known. For example it is possible that FD binding to DNA requires FT, alternatively, FT may act as a transcriptional activator for FD. FD protein as seen by FD GFP fusions, appears to be constitutively nuclear (Abe et al., 2005), so it is unlikely that it is the nuclear to cytoplasmatic partitioning that is affected by FT. FT is closely related to the gene TFL1. Intriguingly, TFL1 has symmetrically opposite roles in the plant, acting as a potent inhibitor of flowering when overexpressed and causing premature terminal flowers to form when mutated (Bradley et al., 1997; Shannon and Meeks-Wagner, 1991). Remarkably, converting a single amino acid on TFL1 to the corresponding residue on FT is sufficient to convert TFL1 from a repressor to an activator of flowering (Hanzawa et al., 2005). Structural studies have confirmed that the specificity of FT and TFL1 signalling resides in a divergent loop on the outside of the proteins (Ahn et al., 2006). The working model therefore is that the binding of FT to the transcription factor FD converts it into an activator of flowering, while binding of TFL1 converts it into a floral repressor.
In terms of the signal that moves itself, there are some interesting questions. While FT mRNA induced in the leaves appears detectable near the apex, it has not been demonstrated whether FT protein moves to the apex as well. In systems were mRNA is actively transported there is often active repression of translation of the transcript before it reaches its destination, and precise control of mRNA location is a mechanism to fine-tune protein activity during development (Bullock et al., 2004). This model would suggest that while FT mRNA transcript is present in the leaves, FT protein might only be translated at the apex. While movement for FT mRNA has been demonstrated, studies of FT protein have not yet been described. Movement of FT protein could also be a significant contributing factor in modulating its activity. Given that FT mRNA is observed at the apex, another key question is whether the mRNA movement is facilitated by a larger complex or if it occurs independently. Finally, the observation that the KNOX homeodomain is sufficient for trafficking of not just KN1 itself but its associated mRNA, as well, is a timely reminder that nature is often more complex than we might initially think (Kim et al., 2005).
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