The Transition to Flowering
Year: 1998
Type: article
Abstract: The general body plan of plants is established during embryogenesis, when the undifferentiated meristematic regions of root and shoot are set aside. However, much of plant development occurs postembryonically, through the reiterative production of organ primordia at the shoot apical meristem (SAM). In most species, the SAM initially gives rise to vegetative organs such as leaves, but at some point the SAM makes the transition to reproductive development and the production of flowers. This change in the developmental fate of primordia initiated at the SAM is controlled by environmental and endogenous signals (Bernier, 1988; McDaniel et al., 1992). However, unlike many developmental transitions in animals, the SAM of plants is not irreversibly “committed” to reproductive development once flowering commences. In some species and genotypes under certain environmental conditions, leafy shoots are formed after flowers in a phenomenon known as inflorescence reversion (see, e.g., Battey and Lyndon, 1990; Pouteau et al., 1997). This observation implies that the genes and processes involved in the transition to flowering are required to both initiate and maintain reproductive development. Because many species must reach a certain age or size before they can flower, the vegetative meristem is thought to first pass through a “juvenile” phase in which it is incompetent to respond to internal or external signals that would trigger flowering in an “adult” meristem. The acquisition of reproductive competence is often marked by changes in the morphology or physiology of vegetative structures—leaf shape offers one example—in a process known as vegetative phase change (Poethig, 1990; Lawson and Poethig, 1995). It is likely that some of the genes identified as important in controlling the transition from vegetative to reproductive development are also involved in vegetative phase change. In some species, the timing of flowering is primarily influenced by environmental factors, which serve to communicate the time of year and/or growth conditions favorable for sexual reproduction and seed maturation. These factors include photoperiod (i.e., day length), light quality (spectral composition), light quantity (photon flux density), vernalization (exposure to a long period of cold), and nutrient and water availability. Other species are less sensitive to environmental variables and appear to flower in response to internal cues such as plant size or number of vegetative nodes. Flowering can also be induced by stresses such as nutrient deficiency, drought, and overcrowding. This response enables the plant to produce seeds, which are much more likely to survive the stress than is the plant itself. Over the years, physiological studies have led to three models for the control of flowering time (reviewed in Bernier, 1988; Thomas and Vince-Prue, 1997). The florigen concept (reviewed in Lang, 1952; Evans, 1971) was based on the transmissibility of substances or signals across grafts between reproductive “donor” shoots and vegetative “recipients.” It was proposed that florigen, a flower-promoting hormone, was produced in leaves under favorable photoperiods and transported to the shoot apex in the phloem. The identification of a graft-transmissible floral inhibitor also led to the concept of a competing “antiflorigen.” Many research years were consumed hunting for florigen in the phloem sap, but its chemical nature has remained elusive. The inability to separate the hypothetical flowering hormones from assimilates led to a second model, the nutrient diversion hypothesis. This model proposed that inductive treatments result in an increase in the amount of assimilates moving to the apical meristem, which in turn induces flowering (reviewed in Sachs and Hackett, 1983; Bernier, 1988). The view that assimilates are the only important component in directing the transition to flowering was superseded by the multifactorial control model, which proposed that a number of promoters and inhibitors, including phytohormones and assimilates, are involved in controlling the developmental transition (Bernier, 1988). According to this model, flowering can only occur when the limiting factors are present at the apex in the appropriate concentrations and at the right times. This model attempted to account for the diversity of flowering responses by proposing that different factors could be limiting for flowering in different genetic backgrounds and/or under particular environmental conditions. Genetic analysis of flowering time in pea, cereals, and Arabidopsis supports the hypothesis that the transition to flowering is under multifactorial control (reviewed in Snape et al., 1996; Weller et al., 1997; Koornneef et al., 1998b). Indeed, multiple genes that control flowering time have been identified in all three of these species. Moreover, some of these genes act to promote flowering and others to repress it; some interact with environmental variables and others appear to act autonomously. The most striking recent advances in our understanding of the genetic control of the timing of flowering have come from work on Arabidopsis. This area of research has been extensively reviewed (see Martínez-Zapater et al., 1994; Haughn et al., 1995; Weigel, 1995; Amasino, 1996; Aukerman and Amasino, 1996; Dennis et al., 1996; Hicks et al., 1996; Madueño et al., 1996; Peeters and Koornneef, 1996; Wilson and Dean, 1996; Coupland, 1997; Koornneef et al., 1998b; Levy and Dean, 1998; Piñeiro and Coupland, 1998), and a number of key findings have emerged. Flowering involves the sequential action of two groups of genes: those that switch the fate of the meristem from vegetative to floral (floral meristem identity genes), and those that direct the formation of the various flower parts (organ identity genes). Therefore, genes that control flowering time can be expected to interact with floral meristem identity genes, which in Arabidopsis include LEAFY (LFY), APETALA1 (AP1), CAULIFLOWER (CAL), AP2, and UNUSUAL FLORAL ORGANS (UFO). The floral meristem identity genes are themselves capable of influencing flowering time. For example, overexpression of LFY and AP1 causes early formation of determinate floral meristems (Mandel and Yanofsky, 1995; Weigel and Nilsson, 1995), whereas mutations in TFL1 affect both flowering time and meristem identity (Shannon and Meeks-Wagner, 1991). The regulation of floral meristem identity genes is under intense investigation. However, because of space constraints, this topic is covered here only briefly (for recent reviews, see Ma, 1997; Piñeiro and Coupland, 1998). To complement earlier reviews, we describe here the current view of the control of flowering time and discuss the classic physiological studies in the context of recent molecular genetic advances. We begin by introducing the genes and mutations identified in Arabidopsis that are known to influence the timing of the of under different growth conditions and genetic these and genes are separate that promote or repress The of in flowering is covered in two to discuss its in of flowering and its in In the second we the of substances such as phytohormones that have been in the control of flowering time and to these substances in the and genetic In the we discuss recent on genetic that control the floral and we present an model that to some of the known Arabidopsis is a photoperiods are and photoperiods are The of Arabidopsis are that they flower they have a vernalization This to and to flowering favorable conditions in the that affect flowering time in Arabidopsis have been identified through of in different and through of induced The identified genes that are to a in control are in of the genes identified by are from three and The analysis of in the the of the floral number of and that are not in the have been identified by this reviewed in Koornneef et al., 1998b). are in Arabidopsis that are known to affect flowering time. The response of to environmental such as vernalization and photoperiod with genetic of have established the of at that control flowering time in Arabidopsis of these appear to the endogenous developmental of the The floral be a that flowering the plant has a certain age or whereas the is to this as the plant The two signals from the the is for floral in response to inductive and the vernalization flowering to occur after an period of Genetic the of the and Flowering in Arabidopsis. This which has been from that in Koornneef et the as with the by are in whereas identified in are in The were initially in the et and Koornneef et et and et The genes have been to a in of flowering because and flower with vegetative phase et al., et al., 1995). The genes the of flowering with certain floral meristem identity genes For example, AP1 and are early in and of LFY the of These that the genes and AP1 and in a et al., 1997). that promote flowering in by or For example, and to and in the et al., 1995). However, when the mutations are with and mutations that result in the plants flower after they have produced an number of leaves and 1998), which that the of these genes not act by floral was on the of its to its et al., and by et al., 1997). The flowers and the shoot apex with a TFL1 must to flower formation at the apex and to the transition from vegetative to reproductive development. with this overexpression of TFL1 the vegetative and inflorescence growth et al., 1998). It is likely that TFL1 this in flowering by the of genes such as and which in the This is because the by mutations in these genes is to et al., 1997; and Dean, and Flowering in For on the of genes involved in flowering to Flowering long response of the or to flower earlier under inductive photoperiods and after vernalization not and Flowering in For on the of genes involved in flowering to Flowering long response of the or to flower earlier under inductive photoperiods and after vernalization not Genetic Flowering in Arabidopsis and of the The the vegetative to floral with the and influence on this are under long and light and vernalization that influence both floral meristem identity and flowering time are in and are based on genetic and analysis of in and all have been and is known the floral interact with the various most of the have been the Therefore, this model, which is an of those by Koornneef et and et not the of the between genes and that control flowering time in Arabidopsis. to a in the regulation of flowering time by the with the which has but et flowering as a in the this was and to which was by Koornneef et as a analysis of the of the the in and in the to be et al., 1998b). Therefore, the of the a of flowering that is by However, because is for a of a (see, e.g., and it is to or not be or in the et that a general and increase in during development could serve to change meristem and as a plant It to such a of in Arabidopsis and of the of flowering at in on changes in at such as of the in flowering time has that the such as and can themselves be as in genes of the floral between a number of and Arabidopsis that flowering and a for vernalization as a et al., that to the et al., et al., and Dean, The recent of has that and are likely to and Dean, at a second are required for the of flowering by et al., Aukerman and Amasino, at but and the and Amasino, 1995). of is and Amasino, and the of this can be at the molecular studies also be to the Arabidopsis Flowering For on the of genes involved in flowering to Flowering and Weigel, Coupland, and Meeks-Wagner, and Dean, Arabidopsis Flowering For on the of genes involved in flowering to Flowering and Weigel, Coupland, and Meeks-Wagner, and Dean, that many genes are involved in the regulation of flowering time in it is that a of both the in flowering time and the for vernalization is at to one of the two that a vernalization in et al., 1997). an important to in the is to in a number of plant species. The identification of mutations that flowering of genes that act to promote Many of these have been by response to vernalization and photoperiod and in Koornneef et al., of and response to photoperiod or and the genes are thought to act in the second of and respond to vernalization but flower under Because the of the genes appear to promote flowering of these genes are to act in the Moreover, the that these respond to vernalization that the vernalization with the in these genes of the be to the of genes a and the is the it is most in the shoot and root et al., Aukerman and Amasino, a with and et al., 1997). The of are to those of the and which of important for and et al., 1997). The is and the of in earlier flowering and Dean, of the of with meristem identity genes that is required for both and competence to respond to LFY and AP1 and Dean, or appear to act in a because in plants in which a of the two of the SAM (i.e., and are and flowering are et al., signals that promote flowering are also the of recent work by et The flowering and floral development. a with that it as a led et to that be involved in the production or of a For example, plants not flower under conditions, and plants an of in a flower earlier et al., 1998). these that is required to produce and/or the of a that in leaves and reproductive development in the leaves are required to the developmental of the apex has also been established to a set of leaves before they produce of many leaves been produced before they were in and 1997). However, the to primordia on the the of the developmental that some from the leaves development of the light in at regions of the by at three of light and are by the and light are by the and is by an and Vince-Prue, 1997). In are at to and two and and Vince-Prue, 1997). These have been by the they have on under different light conditions. Arabidopsis that were based on are also in flowering time. These include and based on were to These include and The of photoperiod in flowering was by and in the in classic with the of and the of (reviewed in Thomas and Vince-Prue, 1997). genetic studies have to molecular of the and an of Arabidopsis and to inductive photoperiods is to The with as and which initiate signals that interact with a and the day is and when the of the period a genes that promote flowering as are This in to the of floral meristem identity genes In light quality flowering with light and light flowering et al., The of that a in flowering under to conditions but is not involved in and 1997). studies on multiple that in to also flowering in response to light quality and 1997). In mutations in which a of that promote These that is involved in both and of flowering by inductive photoperiods Koornneef and 1997). light flowering in and the of the has been to one of the two identified in Arabidopsis et al., 1998). plants earlier than the and of et al., 1998), that light flowering and (see the of was to be in under long but not under et al., 1998), a for the of the Because the of both and and in the light and Vince-Prue, they could the of transitions to the the in was identified as the which has a long under light is sensitive to photoperiod and is not in flowering in a under light and inductive However, in the of of and in is flowering and et al., 1996; Koornneef and 1997). Therefore, is involved in the of but its with floral is genes that affect and that of the have been and in a and overexpression of in long and flowering et al., 1998; and 1998). of or also or the of as as genes, which that and and 1998). likely component of the is which was identified as a that the period of the by to et al., 1998). The the of plants to photoperiod and causes early flowering under that changes in the of the not can flowering time. the of light signals by the with the The of the that the of this is involved in flowering under However, the of the that which has been not in the et al., 1996; Koornneef and 1997). 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However, the of in vernalization is because not vernalization from flowering in these it of the vernalization in the of plants et al., 1998). to understanding the molecular of vernalization has been to of Arabidopsis that are in response to et al., The point for this genetic was a can be by a period of plants were and a of plants were and for plants that that which a response to these those that than were for et al., be in the of or in the of the by the vernalization identified mutations in at three groups et al., and a second identified which have not been to groups Levy and Dean, and have been in some and are by and have a that they are of a to and vernalization or that occurs in these two responses et al., of the genes some of the molecular involved in of flowering by physiological analysis has led to certain and processes in controlling the floral These include the of and In this we discuss the of these substances in flowering and to the and that in during floral from studies of a plant in the of flowering in by a long day or a the of in the phloem the apex and et al., this of the increase in that is in the SAM floral The the apex to be from the of most likely in the leaves and because plants induced by a day the as plants under photoperiods et al., In plants in with in with flower with the number of leaves as plants under long et al., 1997). In has a on the flowering of and which flower early when under these conditions and with the number of leaves as et al., 1997). in the or in the is for most of this Therefore, to these the of flowering by the of at and also the flowering of and but not of and et al., 1997). This result implies that and in processes that are of or separate from control of to the vegetative whereas and in processes of this control genetic with control of flowering is but the nature of this is For example, are at Arabidopsis and which are in or and which flower under some conditions The flowering time of and is not influenced by and both are likely to act in the et al., 1995). and flower in than they in long and the Flowering of these is by that vernalization not on et al., The of in the transition to flowering has been to the one are many in which the or of endogenous changes under conditions that flowering and because certain can flowering in some species, has been an on the of in floral and in the for florigen (reviewed in Evans, 1983; Thomas and Vince-Prue, 1997). the are at flowering in Moreover, they flowering of they promote flowering of and the can have a different in different species. For example, has when to but has on flowering in et al., In by to a in under photoperiods of flowering of plants under and of the and under long and Dean, the not flower with et al., and the flowers a to flowers early and as plants a that to be involved in or to et al., 1997). The of in of the LFY has been et al., 1998). The of LFY is in and the by long is In LFY is in a in with an of was also to flowering in plants in promote flowering in Arabidopsis at in by LFY et also the direct of with and on LFY produced a and both a This for two signals for account for with and In this was to result from two signals at the of these signals has not been identified from this it is and the is and The of in vernalization has particular because in some species, of to plants can for (see Lang, Evans, 1983; Martínez-Zapater et al., However, in the of species including most and of is not to a for vernalization Lang, Evans, Because are involved in flowering processes such as floral and and which occur after the it is that of can vernalization with this is the that vernalization increase the of plants to but that have direct in the process of vernalization that not a in vernalization in Arabidopsis from with a in and with which to the a vernalization response and Dean, However, because plants and this result must be with In the of in the transition to flowering is changes in and to be as the of (for a of this see Evans, are not the only of phytohormones that has been in the floral For example, is from studies on that by a in the transition to flowering in response to inductive photoperiods (reviewed in et al., inductive photoperiods the and of from the leaves to both the shoot and root In the this to the of primarily to the shoot and leaves, the of the leaves, and some makes its to the shoot its increase of et al., The of the and to the floral transition in Arabidopsis to be of a to that of flowering and on growth et al., has been to be to the and 1995), but the of mutations that in flowering be to a of in the genes the be that such have not been as In to and such as and be involved in flowering under certain and in some species et al., The is in and flower early under photoperiods et al., a for and in floral and The genetic that control the floral transition in Arabidopsis have been in a model that is and as e.g., and Martínez-Zapater et al., 1994; Coupland, 1995; et al., 1995; Koornneef et al., This model with the multifactorial control model, which was on the of physiological of flowering time (Bernier, 1988). is that the time at which flowering occurs is by between the action of that developmental age and and the action of floral The are that flowering has been the and to the meristem identity genes is one of the most of research in this in LFY are with flowering only after a of LFY has been et al., 1998). of AP1 is more to floral et al., 1997). LFY and of AP1 is after the point of floral The between the genes and LFY has been et al., 1998; et al., 1998). Indeed, and all a in of LFY and are required to some for of LFY In and appear to be for plants to respond to LFY et al., 1998). has been by et al., and Weigel, it a with to meristem identity TFL1 et al., 1997). TFL1 and have with one and the Genetic by et have and from the genes, and it has been proposed that these two genes to AP1 in a that to the to LFY This of and was also by et in of the of flowering in Arabidopsis (see The of in and appear to act as between some of the floral promoters and floral meristem the many known floral meristem genes this to be but it is that different to a set of floral meristem identity genes, which are themselves at in this area has been extensively reviewed and is not covered in here (see Koornneef et al., 1998b; Piñeiro and Coupland, 1998). In is in the molecular control of the floral The phase of the work the of genetic for example, to and of genetic that of the to genes or that backgrounds to both genes that in the and genes with more genes are and of genes that have been appear to of identification of the and of these to to in the various the genes controlling flowering time in Arabidopsis an important be to they to genes that flowering time in species. on be required to the of different genes in different species. this in we have a of from pea, and based on the physiological of the or and genetic for or these different genes would and it would also on in Arabidopsis. The to with genetic analysis in has important on the of the For example, the is involved in the production of a graft-transmissible floral whereas the of flowering and are not and are thought to the of the meristem to the and/or to and/or would to our understanding of the of these Arabidopsis have during the identification of in different species would a model, which could be of Arabidopsis to plant species. et Snape et and and et In to and early flowering in both long and 1997). of Arabidopsis to plant species. et Snape et and and et In to and early flowering in both long and 1997). We and the We our to include to and we to those work could not be to space in the on control of flowering time in Arabidopsis is by from the and the and the
Source: The Plant Cell
DOI: 10.2307/3870778
Authors: Yaron Y. Levy, Caroline Dean
Institution: John Innes Centre
Language: English
Subfield: Plant Science
Domain: Life Sciences
Open Access status: green
OpenAlex ID: W2135561607