FT, A Mobile Developmental Signal in Plants

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1 Current Biology 21, R374 R378, May 10, 2011 ª2011 Elsevier Ltd All rights reserved DOI /j.cub , A Mobile Developmental Signal in Plants Minireview Philip A. Wigge Plants synchronise their flowering with the seasons to maximise reproductive fitness. While plants sense environmental conditions largely through the leaves, the developmental decision to flower occurs in the shoot apex, requiring the transmission of flowering information, sometimes over quite long distances. Interestingly, despite the enormous diversity of reproductive strategies and lifestyles of higher plants, a key component of this mobile flowering signal, or florigen, is contributed by a highly conserved gene: FLOWERING LOCUS T (). The gene encodes a small globular protein that is able to translocate from the leaves to the shoot apex through the phloem. Plants have evolved a variety of regulatory networks that control expression in response to diverse environmental signals, enabling flowering and other developmental responses to be seasonally timed. As well as playing a key role in flowering, recent discoveries indicate is also involved in other developmental processes in the plant, including dormancy and bud burst. The force that through the green fuse drives the flower Drives my green age; that blasts the roots of trees Dylan Thomas Since plants are sessile, they must adjust their development to their environment. In contrast to animals, in which the developmental blueprint is usually hardwired in the embryo, plant development is plastic and continues throughout the life of the organism, allowing adaptation to the external environment and climate. Additionally, while plants lack a central nervous system, they must coordinate events throughout their body plan, which in the case of redwoods can span as much as 100 meters. A key developmental transition in plants is the floral transition. The timing of the floral transition must be coordinated with a host of environmental factors, including the seasons, climate, other plants and sometimes pollinators, to ensure reproductive success. Higher plants are among the most successful organisms on Earth, and have evolved a remarkable diversity of lifestyle strategies to colonise almost every space available. Detailed investigation of the molecular mechanisms underlying the floral transition are revealing conserved as well as divergent regulatory mechanisms. Interestingly, while many of the transcription factors regulating flowering have diverged, the mobile protein signal that triggers flowering appears to be conserved in most if not all higher plants. This Minireview summarises recent advances in understanding how functions in different plants, and the significance of these findings. John Innes Centre, Colney Lane, Norwich NR4 7UH, UK. philip.wigge@bbsrc.ac.uk What is Florigen? Early Studies Many plants show a strong acceleration in flowering when grown under a particular photoperiod (i.e., daylength). Classical experiments were performed in the 1920s by Garner and Allard on a late flowering tobacco strain, Maryland Mammoth. By reducing the photoperiod experienced by tobacco plants, it was possible to greatly accelerate flowering [1]. Early experiments using controlled shading of either leaves or the plant apex revealed that leaves are the site of signal perception. Paradoxically, however, the effects of floral induction occur at the growing tip of the plant, the shoot apex, meaning that a signal must somehow be transmitted from the leaves to the shoot apex for flowering to be controlled. This led to the florigen hypothesis, florigen being a chemical generated by the leaves under inductive conditions that is transported to the shoot apex to induce flowering. Extensive grafting experiments among many different species strongly supported this hypothesis, since often a single induced leaf, grafted onto a non-induced plant, would be sufficient to induce flowering [2]. Despite this promising start, and many heroic experiments, identification of the molecular nature of the mobile signal had to wait for the advent of molecular genetics., a Key Florigen in Tomato, Rice and Arabidopsis While the challenges of biochemically isolating florigen proved to be insurmountable, the power of molecular genetics in the model plant Arabidopsis thaliana led to the identification of a key regulator, FLOWERING LOCUS T (). Mutations in caused a considerable delay in flowering [3], while overexpression of caused precocious flowering, indicating that is necessary and sufficient for the acceleration of the floral transition [4,5]. Intriguingly, was found to encode a small globular protein for which no clear molecular function was apparent. Furthermore, while most of the floral meristem genes known were specifically expressed at the apex, was distinctive in being expressed in the leaves [6]. Indeed, a major activator, CONSTANS (CO), is specifically expressed in the phloem, and overexpressing CO in the phloem to drive high levels of expression in the vasculature was sufficient to trigger early flowering [7], suggesting that, or a downstream factor, is able to travel from the vasculature to the shoot apex. Elegant experiments with an homolog from tomato, SINGLE-FLOWER TRUSS (S), revealed that branches overexpressing S, when grafted onto tomato and tobacco, are able to induce flowering. Control experiments showed that it was impossible to detect movement of the RNA, indicating that S protein, or a downstream target, was acting as a mobile signal in the plant to trigger flowering [8]. Subsequent experiments using fused to a gene encoding green fluorescent protein (GFP) in Arabidopsis [9] and rice [10] also revealed the ability of :GFP protein to travel from the vasculature to the shoot apex. Although GFP itself is able to traffic from the vasculature to the apex, there is evidence that is also mobile and this activity is required for floral induction. While expression of specifically in the phloem causes precocious flowering [7], this can

2 Special Issue R375 Figure 1. The FLOWERING LOCUS T () signalling system in plants. is expressed in the leaves under conditions that are favourable for flowering, for example in response to the appropriate photoperiod as well as environmental cues such as temperature. protein enters the phloem and is translocated to the shoot apical meristem (SAM). At the SAM, interacts with the bzip transcription factor FD, enabling the activation of floral meristem identity genes such as APETALA1 (AP1) in the domain where FD is expressed. be prevented by expressing active but non-mobile forms of in the vasculature [11,12]. Finally, grafting experiments in cucurbits demonstrated the ability of protein to move in the phloem sap and trigger flowering [13]. Taken together, these experiments confirmed the role of protein as a mobile inducer of flowering. Since then, has been shown to be sufficient to trigger flowering in a wide range of plants, indicating remarkable conservation across the plant kingdom. AP1 FD FD FD Temperature Vernalization Day length Light quality AP1 Shoot apical meristem (SAM) environmental Environmental signals signals How Does Signal? Given that is able to travel from the vasculature to the apex and induce flowering, a key question is how it activates the floral programme, since it has no obvious signalling domain. Protein protein interaction studies revealed the ability of Arabidopsis to bind the basic leucine zipper (bzip) transcription factor FD [14,15]. Furthermore, it was shown that FD is tightly expressed in the shoot apex in the spatial domain where floral meristem identity genes are upregulated, and it was possible to show that FD directly activates some of these in the presence of [14,15]. Thus, protein is able to translocate from the leaves to the apex and activate the FD transcription factor to convert meristems from a leaf to a floral fate (Figure 1). Interestingly, is closely related to the floral repressor, TERMINAL FLOWER1 (TFL1). Indeed, by changing just one amino acid on it is possible to convert it into a TFL1-like molecule [16]. Subsequent structural biology studies revealed that key residues that confer or TFL1-like behaviour exist on an exposed loop of these proteins [17]. These studies suggest that and TFL1, given their similarities, act through a common mechanism. A complete understanding of the mechanism of signalling awaits the crystal structure of the FD complex, preferably bound to DNA. Floral Pathway Signal Integration A key feature of the floral transition in plants is that it is responsive to both environmental signals (e.g., temperature, light quality and photoperiod) as well as endogenous signals Leaf Phloem transport Phloem Current Biology (e.g., hormones and age). In addition to signals that trigger flowering, plants often have a requirement for a prolonged period of cold (vernalization) in order to be competent to respond to floral signals. A vernalization requirement provides a mechanism to prevent the plant from initiating flowering in the autumn or winter, when frost may kill the buds. Additionally, the ability of plants to flower is often dependent on age, and even in relatively emphemeral plants like Arabidopsis, a pathway that measures developmental age signalling via micrornas has been shown to act to increase floral competence in the plant with age [18]. The major pathways that affect flowering in Arabidopsis identified by genetics are the photoperiod, gibberellin, vernalization and autonomous pathways. This raises the question of how these overlapping or potentially conflicting signals are assessed and integrated to provide a single

3 Current Biology Vol 21 No 9 R376 developmental decision. While hundreds of genes may influence the floral transition, the decision of when to flower largely depends on the final level of expression., along with two other key genes, LEAFY (LFY) and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS (SOC1), have therefore been termed floral pathway integrator (FPI) genes to account for this essential role in integrating flowering information [19]. The Major Floral Pathways A detailed summary of the major flowering pathways is beyond the scope of this review, but the reader is pointed to excellent recent reviews on the photoperiod [20], gibberellin [21] and vernalization pathways [22]. The photoperiod pathway accelerates flowering under inductive conditions. In Arabidopsis, these are long days, that is, days of about 16 hours light. The mechanism by which plants are able to accelerate flowering in response to long days represents a variation on the external coincidence model, first proposed by Bunning more than 70 years ago [23]. The gene CO is an output of the circadian clock and has a diurnal expression pattern that peaks about 16 hours after dawn. While CO protein is stable in the light, it is rapidly degraded in the dark. Thus, plants growing under short days will not accumulate CO protein, while plants in long days will [24]. CO is a zinc finger protein that is able to bind directly to the promoter and activate its expression [25,26]. Since CO levels are also influenced by light quality, this provides a mechanism by which light quality could influence flowering time [27]. Gibberellin (GA) mutants are late flowering in long days, and do not flower at all in short days [28], indicating that GA plays a key role in controlling the floral transition. The importance of GA in both long and short days suggests several roles, both -dependent and -independent. The FPIs LFY and SOC1 have been shown to be induced by GA [29,30], suggesting key nodes at which GA may be acting in the floral transition. Vernalization is one of the most heavily studied and well understood floral regulation pathways. In Arabidopsis, the key regulator of the vernalisation response is the MADS box transcription factor FLOWERING LOCUS C (FLC). In vernalization-requiring plants, FLC levels are very high before vernalization, but stably repressed through epigenetic marks after several weeks in the cold [31,32]. FLC has been shown to directly repress many key components of the floral pathway, including, FD and SOC1 [33], accounting for how the overexpression of FLC causes such a late flowering phenotype. The regulation of FLC silencing is complex, and serves as a paradigm for the activity of non-coding RNAs and post-translational histone modifications in controlling gene expression. The vernalization pathway also interacts with the so-called autonomous pathway, mutations in which perturb FLC levels. It is likely, however, that many of these genes are actually involved in separate cellular processes, and may not function in a linear pathway. As well as these classical pathways controlling flowering, a number of other factors play a role in influencing flowering. Ambient temperature has a strong effect on flowering, and indeed, high temperatures are able to accelerate flowering in short photoperiods almost as much as long photoperiods [34]. This process is -dependent, and mutations in genes that perturb levels also often disrupt the thermal acceleration of flowering [35,36]. The mechanism by which warm temperature accelerates flowering, however, is not known but is likely to involve chromatin structure [37,38]. As well as accelerating flowering, a number of genes function as floral repressors. These allow a number of environmental and endogenous signals, such as age and low temperature, to influence the floral transition. Of particular interest, the microrna mir156 has been shown to be a potent inhibitor of flowering, acting by repressing a class of transcription factors, the SQUA- MOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes, which activate flowering targets. mir156 declines with the age of the plant, providing a competence to respond to floral signals [18]. Another microrna, mir172, also plays a key role in repressing floral repressors, in this case AP2 transcription factors of the TOE and SMZ/SNZ classes, which have been shown to directly repress expression [39]. In the leaf, TEMPRANILLO1 and TEMPRANILLO2 have also been shown to repress and are proposed to balance CO activity [40]. Variations on a Theme: Learning from Other Plant Systems While was discovered in Arabidopsis, homologs have been described in rice and shown to be essential inducers of flowering. Indeed, when two homologs are inactivated in rice, the plants never flower [41]. Paradoxically, however, rice exhibits the opposite lifestyle strategy to Arabidopsis, requiring short days for flowering to be accelerated, and this correlates with the expression of a rice, Hd3a, which is weakly expressed in long days but strongly expressed in short days. Since it has been shown that a similar module to the CO signalling module exists in rice, this raises the question as to how an opposite developmental outcome can be achieved from a seemingly conserved signalling pathway. Interestingly, the rice equivalent of CO, Hd1, plays a critical role in mediating the photoperiod signal. While Hd1 activates expression in rice in short days, in long days Hd1 is converted into a transcriptional repressor [42]. Strikingly, flowering in Poplar is also regulated by. Poplar trees have a prolonged immature period spanning many years, and levels rise very gradually, year by year. The mechanism by which gene expression can be increased gradually over such a long period is not clear, but it is likely to involve chromatin structure [43]. This is an elegant example of how the pathways by which is activated can be altered to provide an alternative outcome in response to photoperiod. As well as modulating expression in response to different environmental factors, many plants have multiple -related genes. In pea, it appears that there are at least two genes that are expressed in the leaf and which interact with each other to control the floral transition [44]. Such a pathway, whereby different -related genes can interact to control the floral transition, is strikingly illustrated by elegant work in beet. In this case, it has been shown that there are two key paralogs, Bv1 and Bv2. While Bv2 is essential for flowering, Bv1 is a potent repressor of flowering, counteracting the activity of Bv2 [45]. Bv1 expression is down-regulated upon vernalization, providing a novel mechanism by which plants can overwinter. These examples highlight the remarkable flexibility of networks using signalling. The signalling system therefore provides a seemingly endless arrangement of possibilities for modulating the timing of flowering through different pathways of regulation as well as paralog divergence.

4 Special Issue R377 Not Just Flowering While research has understandably been focussed on its role in influencing the floral transition, there are clear indications that signalling plays a wider role in plant growth and development. As well as triggering flowering in tomato, the homolog S also influences a number of developmental responses, such as leaf maturation, stem growth and the formation of abscission zones [46].In addition to flowering, there are a number of other major seasonally dependent developmental responses. Particularly important in trees is bud-set and bud-burst, allowing deciduous trees to overwinter and survive prolonged periods of cold. The timing of bud set and bud break is critical for maximising fitness. In poplar, the onset of bud dormancy is triggered by shorter days and lower temperatures, and this is dependent on a concomitant down-regulation in expression; indeed, -overexpressing poplars do not set buds, indicating that the CO regulatory module plays a key role in this process [43]. Following winter, the buds must open in the spring. Interestingly, may also be involved in this process. It has been shown that prolonged chilling of dormant poplar buds, a treatment that simulates winter, causes both massive upregulation of expression in the embryonic leaves within the bud as well as the induction of enzymes that open the channels, or plasmodesmata (PD), between plant cells [47]. Closing of the PD is important for bud formation, but upon bud-burst it is proposed that opening of the PD facilitates the transfer of growth signals, possibly including, to stimulate bud growth [47]. Major Questions The last 10 years have witnessed a dramatic advance in our understanding of key events in the plant life cycle, including flowering and bud formation. To a remarkable extent, several problems that had seemed to be of almost intractable complexity have been shown to have a common regulator,. Major questions for the future will be to understand just how levels are able to be controlled by so many different environmental and endogenous signals. Particularly interesting is how the level of expression can be so precisely modulated, and how expression can be controlled to such a high degree over prolonged periods, many years, for example, in the case of trees. It is likely that such cellular memory mechanisms involve modulating chromatin structure. While temperature has been shown to have a very strong effect on flowering time, the mechanism by which warm temperature accelerates flowering is still not described. The tremendous advances in deep sequencing now make it feasible to obtain detailed transcription factor networks for regulatory factors and to map these changes in transcription factors and chromatin state over time in a tissue-specific manner genome-wide [48]. This provides us with an unprecedented opportunity to understand the molecular mechanisms underlying plant lifecycle decisions [49]. The complexity of the regulatory networks involved suggests that a whole area of mathematical modelling approaches may need to be developed if we are to be able to understand and test the systems under investigation. A predictive knowledge of how influences so many aspects of plant growth and development holds great promise for breeding better crop varieties [50]. Acknowledgements I apologise to colleagues whose work I have been unable to cite owing to space constraints. I thank members of the lab for insightful discussions. 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