Year: 2004
Type: review
Abstract: At a certain point in their life cycle, annual plants undergo a major developmental transition and switch from vegetative to reproductive development. This process is rarely reversible, and ensuring that the timing of this transition is optimal for pollination and seed development is a major factor in reproductive success. Physiological and genetic analysis of flowering has shown that multiple environmental and endogenous inputs influence the timing of the switch. The molecular identity of these different inputs is being dissected using molecular genetic approaches in Arabidopsis. The multiple pathways quantitatively regulate an overlapping set of common targets, the floral pathway integrators, whose activities convert the shoot apical meristem to a reproductive fate. An emerging idea is that changing the predominance of these input pathways could account for much of the plasticity and diversity of flowering time control within and between plant species (Simpson and Dean, 2002). During the last few years, the data relevant to a molecular understanding of flowering time control have increased rapidly, making it unwieldy to comprehensively review the field. In addition, there have been numerous and excellent recent reviews on various aspects of flowering time control (Mouradov et al., 2002; Ratcliffe and Riechmann, 2002; Simpson and Dean, 2002; Henderson et al., 2003; Yanovsky and Kay, 2003). To complement these, we have chosen, in this review, to group genes involved in flowering time into pathways that enable the floral transition and those that promote it. We also discuss the role of genes defined through early-flowering mutants. Are they specific floral repressors or more global regulators needed to reset patterns of gene expression? Pathways That Enable or Promote the Floral Transition Determine Flowering Time. The different pathways are grouped into those that promote and those that enable the floral transition. The enabling pathways regulate the ability of the meristem to respond to floral promotive signals from different environmental and endogenous cues. Pathways That Enable the Floral Transition. A central regulator of the enabling pathways is the floral repressor FLC. High levels of FLC repress the activity of the floral pathway integrators, and this antagonizes their activation by floral promotion pathways. Many genes are involved in regulating FLC expression. FCA, FY, FVE, FPA, and vernalization repress FLC (FLD and LD are not included here because they are not required in all genotypes). FRI, VIP3/4, ESD4, and EFS upregulate FLC. TFL1 and SVP also may antagonize the activation of the floral pathway integrators but are not included here because their regulation and interaction with FLC are unclear. This concept of pathways that enable the floral transition emerged from the analysis of double and triple combinations of mutants from the classically defined photoperiod, gibberellin (GA), and autonomous pathways (Reeves and Coupland, 2001). Single autonomous pathway mutants (fca-1), which had high levels of FLC, flowered much later than single photoperiod pathway (constans-2 [co-2]) or GA pathway (ga1-3) mutants under long-day conditions. Under the same conditions, co-2 ga1-3 double mutants (in which FCA is active) flowered extremely late, if they flowered at all, and were later flowering than co-2 fca-1 and ga1-3 fca-1. Therefore, FCA activity by itself has little promotive effect on flowering time. However, if FCA activity is absent and FLC levels are high, the plant does not respond as well to promotive flowering signals. The pathways that enable the floral transition could be likened to the control of a sluice gate in a lock on a canal. The plant is like a boat waiting to move from one lock to the next (vegetative to reproductive development). The floral repressors act as the gate itself, inhibiting the passage of water (floral promotion) into the lock. However, there are multiple controls that can open or close the sluice gate, and their combined action determines how high the gate rises and thus how much water is permitted to flow through. It is the water itself that allows the boat to move on to the next lock, but how long the water takes reach the right level is determined by the control of the sluice gate. FLC is a MADS box transcriptional regulator, expressed predominantly in shoot and root apices (Michaels and Amasino, 2000), that acts to quantitatively repress flowering (Michaels and Amasino, 1999a; Sheldon et al., 1999) through repression of the floral pathway integrators FT, SOC1, and LFY (Nilsson et al., 1998; Kardailsky et al., 1999; Kobayashi et al., 1999; Blaézquez and Weigel, 2000; Lee et al., 2000; Samach et al., 2000). FLC plays a central role in vernalization requirement and response. mutants and that a vernalization requirement have increased FLC and plants have FLC levels et al., and Amasino, et al., 2002). of FLC in flowering in which is vernalization but in plants and (Michaels and Amasino, 1999a; Sheldon et al., of in different has shown that at FLC to flowering time (Michaels and Amasino, 2000; et al., 2003). In the of this to be the of regulation of the gene than of different FLC The FLC in is much than that of and this is with the of a in the of FLC in a to be required for FLC regulation et al., 2002; et al., 2003; et al., are close of FLC in the MADS to et al., is also et al., to to act as floral repressors whose is if at all, by is by but the role it plays in flowering time is et al., 2003). TFL1 a that is to and is with et al., et al., Kardailsky et al., 1999; Kobayashi et al., In to the floral activity of FT, TFL1 the vegetative and the of the and et al., et al., activities are to from TFL1 the of LFY and and also a to these genes in the meristem et al., Ratcliffe et al., LFY and TFL1 in the floral on the of the meristem et al., 1999; Ratcliffe et al., The activity of TFL1 and flowering time and the of the et al., that TFL1 are but flowering can be in plants by vernalization or of FCA Dean, and This effect is not FLC because FLC levels are in between autonomous pathway mutants and mutants plants that later than the autonomous pathway mutants et al., et al., This interaction between FLC and TFL1 the of FLC in the meristem as it does to LFY and SVP also acts as a floral repressor and a MADS et al., 2000). SVP acts in a to flowering and does not the of photoperiod or vernalization on flowering time. the flowering by of and double mutants like single mutants. and SVP to in the same floral which with the photoperiod pathway et al., 2003). it shown that and can act as floral repressors and 2003). and a is flowering than is the The does not in an early-flowering but it does the early-flowering the and are of which the of a of the of flowering and 2003; and does by as a repressor of genes and In with developmental which it to the interaction with a to control flowering time on an of and 2003). of FLC which in that a annual they the vernalization requirement is they in at is a major for flowering time in et al., 2000). FLC levels to an that it the influence of the promotive of long a that interaction with or et al., 2000). levels are at all of plant and is not by vernalization and Dean, or of not flowering FLC, levels not have a effect on flowering time and Dean, of FLC in plants flowering in the of vernalization (Michaels and Amasino, 2000). Many early-flowering different of early-flowering by the and different that the early-flowering has at in the of et al., 2000). to be common et al., 2002; et al., and a high of in has been This may for flowering time in et al., 2002). genes that in the of FLC have been through the analysis of early-flowering mutants that have been to FLC or shown to have FLC expression. of these mutants emerged from for mutants that flowered in flowering in et al., in (Reeves et al., and photoperiod and Amasino, 2003). a whose are et al., 2003). the of and autonomous pathway mutants and is to of the and and Amasino, 2003). FLC regulators have been as of activity and vernalization mutants and 2002; et al., 2003). mutants than mutants and also floral that genes regulate multiple genes that influence flowering time and developmental with and from and In with the of the and is a of the transcriptional which is required for the of a of genes and 2002). a of and is to as a in et al., 2003). the process that in plants as they for in FLC levels and flowering (Michaels and Amasino, 1999a; Sheldon et al., is with flowering more than the flowering time effect an is also a The is the meristem and from plants vernalization et al., This that vernalization had an a in gene is by the that the plant is to The be reset the of seed development to that vernalization is required for flowering in the next The molecular of vernalization has been through the of mutants a vernalization et al., and Amasino, of FLC levels in vernalization mutants gene FLC in the but of development in FLC levels increased in and mutants et al., et al., 2002). Therefore, the of and is to FLC that they are of the that a of FLC levels not in the in that is involved in the of the repression of FLC and Amasino, a with a plant and a involved in is in the later of and the Therefore, to be to the of the of and in the of the and Amasino, a to of a group required in to repression of certain genes et al., 2001). group of and act to patterns of gene set by transcriptional as of the which through the of specific on et al., 2002; et al., 2002; et al., 2002). with the idea that FLC in a the at FLC in mutants shown to be a with transcriptional activity et al., 2001). has been shown to in at the FLC that are of an in and and a in et al., and Amasino, in FLC are on in the vernalization pathway et al., and Amasino, the in through the FLC of which were in to required for FLC regulation as defined in analysis of FLC et al., 2002). This analysis defined one and one that FLC in the of also were for repression and of repression by vernalization within the et al., 2002). The between the and the has to be a for predominantly through the regulation of the floral pathway et al., 2002). plants flowered as a of increased in mutants. FLC in these the plants had been that to FLC. of the on by the may be the process required et al., a that that in in a et al., 2002). specific FLC in is To little is the of FLC expression. The vernalization to be in the or to high FLC levels in the ensuring a vernalization requirement in FLC is not the flowering time of because an in that flowering time can be vernalization (Michaels and Amasino, 2001). A is a gene with to et al., 2002; et al., SOC1, is by but SOC1, this is of FLC mutants are but this is not by vernalization et al., 2002; et al., to act of but of but of that the between these genes may not be (Michaels et al., The of to be by a role for this process on the of on flowering time and vernalization has not been et al., 2003). and mutants are as in an autonomous pathway because they in all et al., Lee et al., and of the autonomous pathway to FLC (Michaels and Amasino, Sheldon et al., The of the mutants can be by vernalization or in these environmental are to in to the autonomous pathway et al., However, does not repress FLC levels in these that vernalization and floral promotion have different et al., and Dean, The genes of the autonomous pathway not in a but as a of a common FLC FCA and one with and mutants on flowering time combined with and mutants et al., FCA a with and a interaction at the et al., The FCA is with one of which a in flowering time control et al., FCA by and within et al., 2003). This the of one of the of FCA at the of the FCA thus the of The is under developmental the FCA interaction and is on FY, which with FCA through the et al., 2002; et al., 2003; Simpson et al., 2003). a with and a and to a group of The is an of involved in et al., 2000). The is that FCA through and the to this interaction between the FCA and the of for this interaction is FCA but FLC is by is not The analysis also grouped the activities of and in the repression of FLC et al., also an et al., a et al., but how they has not been A double has not been and may be et al., which that and are for an role in plant development. This is not the for the double which can be et al., and are regulators of FLC that on flowering time et al., and Amasino, LD a that is to the et al., in and LD also may with as for FCA and (Simpson et al., a that is with a of a which to into a the of from et al., 2003; et al., 2003). In a acts to FLC the of FLC and flowering et al., 2003). regulation is emerging as a major to FLC A pathways control the of a common is how the predominance of those activities is to FLC, the and the repression by genes of the autonomous This predominance may be to of the of FCA is at levels development as a of FCA the of an within FCA et al., 2003). However, as by levels of an which an is FCA levels in the shoot and root by to et al., 2002). This may a specific developmental to FCA levels and thus FLC levels in the meristem at later of development. of from FCA the and in increased levels of FCA much in development. This the repression of flowering by et al., 2003). the timing or levels of FCA and can the of their Therefore, the of FCA may have to FCA activity in development and flowering Pathways That Promote the Floral Transition. and promote the floral transition by the floral pathway The photoperiod pathway flowering under long The with as and the and with the in are by this and into flowering time of Under with the under long the activation of by and to an in and the promotion of also acts of the The and repress At is the this at this role is by The and act to promote flowering or by The GA flowering under by regulating the of the floral integrators, and this effect at on To and respond to in photoperiod, plants be to and this to an or and In the and the are the involved in by these acts to reset the that it in with is a of one of which a is by and to in the of and to be of the central et al., 2000). genes that influence and flowering time the et al., 2000; et al., 2000; et al., 2001). mutants are flowering in long and an in This is on that may act as a et al., 2000). of flowering in long and a of et al., 2001). The flowering but has influence on the et al., 2000). genes that a an in involved in and a of the It has been that the of these with in between and that the to and in a et al., et al., 2003). However, recent of the of have shown that and a of that these in a pathway et al., 2003). also is a of the pathway between the and the It as an early-flowering that the and but under et al., The for this has been by a of recent has been to a whose is in a with a at the of the et al., et al., 2001). The of the has been shown to antagonize input to the and the Therefore, it has been that in by at et al., 2000). In the the of under the to the the to Therefore, on the regulation of flowering time from role in the how in is but it does a of and has been shown to with et al., 2001). also are in the to mutants are with and and are flowering et al., 2003). The is also in the and an of from a for of in a et al., 2000). In to these and mutants the the and the of a of et al., 2000; et al., 2003). these data that and of and act to the of the that it the and Therefore, these genes the and regulation of the timing of the floral transition. and have been as for in et al., et al., 1998; and and all and with a single The of and and is by the with a in the in gene the of one in of the and et al., 1998; and 1998; and 1999; et al., 2002). a regulator whose also is by the with a of in the in the of and et al., 1998; et al., 2000). the of and a has been these to an transcriptional and et al., 2001). During the and in a of at the of the in and the act to repress and levels by the of the as a of the of their in and the repression of and the an However, it be that aspects of this have to be which has to the development of an in which the of the the et al., 2002; et al., This the of a of genes in of the photoperiod et al., 2000). The of these genes the cycle, of the of time. data have that also may be involved in the mutants like the of the that it may with to and et al., 2002). The gene plays a role in and for how is a factor with and mutants under long but flowering time is in of flowering under photoperiod et al., et al., 2001). levels of are in a of mutants. In and levels are in the early-flowering levels are The of these on the to be into a flowering effect an idea that is with the regulation of expression. also is by photoperiod, and under in the Under long there is a in at the of the an that is by Therefore, a has been a for the of under long high levels with to an in et al., 2001). This of molecular for the of by This that the a that is to at certain of the with these a In the is for by the of and input to is by and and Kay, 2002). In long-day conditions, with the in the activation of and the promotion of these in understanding the photoperiod regulation of the that the of unclear. However, recent that may be involved et al., 2003). It is that and are that a in under but not long This may act as of the et al., 2003). The of in flowering time has been shown through In the a single an increased of and this an early-flowering in et al., 2001). The photoperiod and pathways on a few that and The molecular of the action between the pathways has been by the levels of these genes in a of the activation of by of by of FLC et al., the photoperiod in and mutants combined with increased levels of FLC by et al., In a the of can be by the of high levels of FLC, which the levels of and photoperiod et al., 2003). To how the between these pathways are the involved in repression by FLC and activation by were in a of in A defined that activation by and repression by FLC. A MADS box is within the and this shown to FLC in et al., 2002). and FLC are FLC to the in at the the of in the activation of et al., 2002). In addition, high levels of FLC the of which the promotion of et al., 2003). FLC acts at levels to the of the photoperiod promotive also flowering time of photoperiod a pathway (Simpson and Dean, 2002). is by which in a in the of to flowering the of et al., and this is by a gene that a that and 2003). and also repress but their are the effect of is absent et al., et al., et al., In to and promote is flowering in in which the at the of the is or the is by a et al., and is flowering under long 2000). It has been that and promote flowering one on floral pathway integrators and one by repression of et al., 2003). Therefore, the and pathways act in an to the a that to regulate flowering under a to the plant of how the is with the by the of different than the at at the has effect et al., 2003). At to act as the regulating mutants than triple an effect that is by levels et al., 2003). The effect of the on flowering also is At but this effect is at The increased in flowering to be by the of activity at At with to promote mutants are However, at is as flowering as the double at a of activity at the et al., 2003). The role of on flowering time control also has been in the and flowering time mutants et al., 2003). The flowering of plants is at and mutants little in flowering time at or FCA and are to a repression of that does not FLC, the of these genes within the pathways that enable the floral transition et al., 2003). This has been as that FCA and in a pathway that in to their role in the autonomous However, it is that this is a effect of those mutants high levels of FLC, which regulation by the The of on flowering may all be through the pathway activation of and may not FCA or have the that flowering a gene in the GA are flowering in long and et al., 1998; et al., The is to GA and is flowering and plants a gene involved in GA or to also et al., a in GA levels or to GA this effect is in et al., a in the in GA an long-day plant because it under mutants are to and also are flowering in et al., have that the GA pathway is from the photoperiod pathway and the enabling pathway and have that the GA pathway has influence on flowering time in long than in et al., et al., 2000; and Coupland, 2001). However, in the of the long-day promotion the GA pathway is an of flowering (Reeves and Coupland, 2001). have that vernalization the GA and in plant GA can for a vernalization Sheldon et al., However, in vernalization and GA action are because the fca-1 ga1-3 and FLC ga1-3 in which GA is respond to vernalization (Michaels and Amasino, et al., 2000). in GA or in flowering time is an of of the GA is because LFY activity is in a ga1-3 and increased by GA in the and ga1-3 et al., The of which is for to an that is a for and Weigel, 2000). A has an overlapping with LFY in the floral meristem and can the LFY in et al., 2001). is GA that it may a role in the GA of the LFY may flowering time by LFY expression. The of the has not been of LFY flowering but complement the flowering time effect of ga1-3 et al., This may be to floral SOC1, also being by et al., The of a in that also may influence et al., et al., 2003). a with a and a plant and is to be of a et al., 2003). mutants are flowering in and flowering in long but the early-flowering is in ga1-3 and double mutants et al., et al., 2003). This that can patterns but that this effect is by Therefore, the of LFY to complement the of ga1-3 may be to the of in is the in FT, SOC1, and LFY that the of the photoperiod, and activation pathways. The through which the LFY are from those required for that at of the of these different promotion pathways at the level of the LFY and Weigel, 2000). are in the control of flowering time in Arabidopsis. that are flowering under conditions, that flowering et al., In of and have been shown to the flowering time of fca-1 mutants et al., 2000). the of in flowering time control et al., genetic for a role for in the promotion of flowering is mutants and et al., the et al., and plants in et al., are these plant regulators in floral promotion pathways. In to the pathways which on the regulation of the floral pathway integrators, there is an of genes that have been as floral repressors on their being have been to group into genetic but they have been as genes expressed in the floral and in the vegetative by et al., 2003). This of floral repressors has to the idea that in the of flowering is the developmental pathway and vegetative development is for a through the repression of genes expressed in the floral A of vegetative is to be that plants can they on the process of flowering and seed An of these be to reset gene for the next or to these global A with development is that in plants are in development to a the that are from within the whose recent expressed genes as those that floral be global of gene to the the of the the is and the is these genes expressed in the and the floral be expressed of early-flowering mutants that this are and mutants are as vegetative and et al., mutants increased of genes involved in floral identity et al., et al., genes involved in seed are in but not in et al., that gene is in a to be a factor et al., and is a of and to a role in the of et al., 2001). gene to be involved in the of is as being required for the repression of development et al., is to the gene from which a group that acts as a molecular in involved in the of et al., is expressed the but because are it not to later in development et al., a that to in seed were et al., 2001). plants and expressed LFY and the floral genes and The that and are of that predominantly at the which are for have been as mutants that shown to be to and in plants et al., 2000). However, recent has shown that in and is to a role in gene in the et al., 2003). early-flowering mutants may genes with more in the of of gene expression. The has an early-flowering and a because of the of a et al., et al., 2003). is a of a with shown to have increased levels of FT, which for the early-flowering et al., 2003; and 2003). and were expressed at levels in the floral development not et al., 2003). A central role of may be in the of repression in the The of with mutants and may be to the requirement for as well as the of repression to levels of that are to a group and is required for the repression of et al., The has an early-flowering that is by the of as by flowering time analysis of a double The of may be from the of of from the In addition, specific floral repressors may that act to the vegetative gene analysis using a group of floral repressors the of plants from to long-day conditions. included the genes that can repress and et al., which like may be by et al., 2003). and in the The plant life can be in floral of global gene and specific repression and promotion of floral pathway We and for this review and Henderson for on the We the and and the for
Source: The Plant Cell
DOI: 10.1105/tpc.015958
Institution: John Innes Centre
Language: English
Subfield: Plant Science
Domain: Life Sciences
Open Access status: bronze
Funder: European Commission
OpenAlex ID: W2072605733