Control of Flowering Time

Flowering is controlled by environmental conditions and developmental regulation. The complexity of this regulation is created by an intricate network of signaling pathways. Arabidopsis is an excellent model system in which to approach this complexity, because it responds to many of the environmental conditions that control flowering in other species, and genetic tools are well developed. Studies in Arabidopsis have led to the identification of components within individual signaling pathways that affect flowering, and to their positioning within molecular hierarchies. Furthermore, distinct signaling pathways are known to converge on the activation of the same flowering-time genes. This convergence of pathways on a common set of genes may enable the integration of different responses, so that the plant can produce a coordinated flowering response under conditions in which multiple environmental parameters are changing simultaneously. Also, genetic analysis of Arabidopsis varieties showing natural variation in flowering time has demonstrated how the activity of these pathways can be altered in nature and how balancing the effects of different environmental stimuli on flowering time is important in plants adapting to growth in different geographical locations. At present, the full complexity of the flowering network can only be approached in Arabidopsis where the necessary tools are available, and extensive efforts are being made to describe related pathways. For example, photoreception, circadian clock regulation, growth regulator synthesis and response, chromatin structure, and response to low temperatures play important roles in flowering-time control and are studied extensively in Arabidopsis. Nevertheless, there is a need to understand how the full diversity in flowering responses is generated. For example, Arabidopsis responds to photoperiod, but all ecotypes are long-day plants that flower earlier under long than short days, whereas many other species show the reverse response. Also, all Arabidopsis thaliana ecotypes are annual plants, and understanding the perennial habit will require a different model species. To understand the diversity in flowering responses, there is a need to look to other species, and here we compare detailed information from Arabidopsis with the emerging picture of the genetic control of flowering in short-day plants. The control of flowering has been reviewed frequently over the last few years (Koornneef et al., 1998b; Simpson et al., 1999; Reeves and Coupland, 2000; Samach and Coupland, 2000; Araki, 2001). However, progress has been rapid, and in the following review we emphasize results that have emerged recently. In particular, we summarize the current understanding of the signaling pathways involved in flowering control in Arabidopsis, and stress how alterations in the balance of activity between pathways can give rise to dramatically different flowering behaviors, for example between ecotypes. We also address recent progress in describing how these pathways function in species that show different responses to environmental conditions than does Arabidopsis. Signaling Pathways Involved in the Regulation of Flowering by Photoperiod in Arabidopsis. A diagram showing the putative relationships among genes involved in the photoperiod pathway. On the basis of the phenotypes of known mutants, genes shown in red generally repress flowering, whereas those in green promote it. Small the of the genes by in plants. between genes a whereas a and from the clock that the of the is circadian clock to the clock that the that it between to the following which the in the et al., et al., and et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., 1999; et al., et al., et al., et al., et al., et al., and et al., (Koornneef et al., et al., et al., Signaling Pathways Involved in the Regulation of Flowering by Photoperiod in Arabidopsis. A diagram showing the putative relationships among genes involved in the photoperiod pathway. On the basis of the phenotypes of known mutants, genes shown in red generally repress flowering, whereas those in green promote it. Small the of the genes by in plants. between genes a whereas a and from the clock that the of the is circadian clock to the clock that the that it between to the following which the in the et al., et al., and et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., et al., 1999; et al., et al., et al., et al., et al., et al., and et al., (Koornneef et al., et al., et al., the flowering-time of Arabidopsis, there is a that is flowering in long but to the under short are to and to a genetic that flowering in response to long and are of this long (Koornneef et al., is the of the known genes that is to this all of the other genes also in other pathways have effects and of and in other pathways et al., 1999; et al., 1999; et al., whereas and of et al., et al., 2001). The to a with related to those of et al., and a because it is in and et al., 2000; et al., 2001). of Arabidopsis genes that for the and et al., demonstrated that the are to the a of in and to The is and necessary for of et al., 2000; et al., but may have roles in et al., from a flowering and of photoperiod et al., in the also and genes et al., In and are in plants plants in which activity is by et al., that these genes of In with can the of et al., 1999; et al., However, that the that pathways are by et al., The a in long days, with a between and and and This is in short days, earlier et al., 2001). in long show a circadian in to that this is controlled by the circadian clock et al., 2001). is an of et al., and a circadian that in long et al., 2001). This is in the In the circadian mutants, and show an altered in that with their flowering to between the circadian clock and the flowering-time et al., 2001). This model that the circadian clock within the long-day to the of genes and have been for how flowering may be by and Samach and Coupland, 2000; Samach and 2001). The model that an that with a of In long-day plants, Arabidopsis, the plant is to the of the flowering is the that in that are are the same and to promote flowering, whereas in these are of the activation of by et that the of may a that is to only under long-day conditions that promote flowering, and that activation of by may to the activation of and to This a of the for that be involved in the activation of under long are and A On the basis of the that are flowering in long et al., and plants flower earlier than the in short et al., is a that the is flowering in long and plants are flowering in short days, that is involved in photoperiod et al., Furthermore, a of by of a for flowering between Arabidopsis ecotypes et al., 2001). This flowering under short because of a that the of under short in the flowering by the that does flowering and are for that the photoperiod in the have a of of require from to but under have been different of from to The that these is in are pathways that the clock to of and a that the and pathways that and 2000; 2001). The control of flowering and et al., whereas many have been in et al., 2000; et al., 2001). by the has detailed analysis of clock regulation. The of from plants the under the control of the et al., The a to for and other et al., and and et al., The in short and et al., and this be by the plants in of than a of to the in et al., This the that circadian is the of the of The The of the is to the of response from However, of this the that is in response are in that does function a response also known and other are in an in et al., The the is the with the of in with a in the and a circadian in et al., In the the of the circadian of in is that of a The in the of the with the of the on multiple and the of in a it a of the components of the are the and which are also involved in the of genes and are by the circadian with a in their et al., and The of all circadian those in and in different those in et al., and that may in of the circadian which be an to the of et al., 2001). of circadian to be by and of genes the of circadian under conditions and 1999; et al., The that and a circadian of that their a and that all that be components of the is also a between the of and on clock regulation, and flowering of flowering under long-day whereas of and the show a of the in also in flowering in short et al., The that and may be of a by the that in an et al., 2001). and to the in and whereas in mutants, the of and is and their of is and may in a in which and rise in the and repress the of to this and to repress their and their the of in the of and so et al., 2001). This may flowering time by the time of that flowering-time genes in the long-day and are be with the of and and of The of circadian can be by environmental conditions and that that affect of circadian by have been and of affect whereas affect of these also have effects on flowering but for many of it is their on flowering time is to an of circadian clock to of The and of will also affect flowering of the effects of on circadian clock regulation, and the of the is reviewed in this For example, a of on flowering can be from the and mutants, which are in the synthesis of the of all flowering in short and in long et al., that generally are of However, only a of this is to be to the long circadian also by these et al., The and all clock under However, the circadian that can be that an is also of the clock et al., The of and on clock only low et al., that the with in these is by a on circadian also describing the long-day in a also have effects on clock function and flowering A in flowering in long and a in the of et al., et al., whereas the of by to The of the in a shown to be on but of et al., whereas under red et al., 2001). of also a in long et al., The a an and that are to a The are to be in et al., The with within the that a in the of et al., The and has been in a of and The of within that it for by the in a that is by have been between and and between and et al., 2001). the of is by the clock and is on et al., may affect circadian by the of a pathway. is a of a of genes that also and et al., The the of However, a circadian and an has on the of and only a in the of the et al., The of can be by and that may be with the flowering et al., The of with circadian clock function is with the of in circadian clock regulation. by is on their and and can be by a of the et al., plants show a of and under that is by and are flowering under long short The also in the in of other which different of the the of in the regulation of the circadian activity is in the plants, and this activity has been shown to and in in plants may be a to an of of the This may and the pathway. The an to photoperiod et al., and this is to be in to of et al., 2001). to mutants, and flowering, and in the red response et al., a to a et al., et al., The with and for the regulation of but for the control of flowering that is of the signaling control flowering time et al., is circadian clock and the of the et al., 2001). The is for and in but in also to red by of in which is of circadian clock of the a by the circadian plants show a to and an of circadian these that is a of signaling that to the clock the also responses the of et al., 2000; et al., 2001). the complexity of the function of genes that control circadian and regulation are by the The is flowering in long days, and show a of to red but to of a of the et al., However, how this for in to is because in to mutants, are of also alterations in of The putative et al., 1999; et al., a but and to the et al., The is circadian clock In the the is in long and short days, and the is in that et al., The flowering of is in to of but how this to the roles of in in circadian clock is to low temperatures for will to this can between varieties of a species. For example, many Arabidopsis varieties will flower are to a but flower to low temperatures for to and a for is with a annual growth In these varieties flower have been to in the the the following and in response to the This is in to which and flower in the same a for The genetic control of by annual varieties that require with annual varieties that varieties and and these in the annual are to a et al., and and a and et al., The and of are in annual varieties of Arabidopsis than in annual In of in annual varieties from the a a of flowering, and of with the of annual varieties and et al., The between and by that the of the plants are to and that this in a that is with the on flowering For example, of plants for a in and by flowering time et al., genes is by have been of Flowering The of and the on Flowering the of The genes and promote flowering by is by it is by the flowering of well by to a of the pathway. is by flowering in this the flowering time genes and The to this model are in in the The of and the on Flowering the of The genes and promote flowering by is by it is by the flowering of well by to a of the pathway. is by flowering in this the flowering time genes and The to this model are in in the The other which a is The of this and et al., this on is for to flowering is by the that the of on flowering The function of is but it that may be involved in et al., varieties of Arabidopsis of that the of that these varieties are from by of the et al., The analysis of that by in response to to The of shown to be and and is it low in plant that are to the and et al., the of is and of is also in the of plants. in common with the of show to control of and led to the that regulation of by may be the basis of et al., with this flowering of of Arabidopsis, in in plants, and in in plants an flowering of plants that to et al., also in a the et al., A genetic approach also to genes for the In this plants The to that flowering et al., The to of by to because plants and temperatures for to in the but to low in the et al., However, the of in et al., 2001). demonstrated that in an low in an but that plants growth the of in the but in This that the of is the of in response to low but the of the et al., 2001). of that is related in to a that by chromatin et al., et al., 2001). A for by the of altered chromatin in The regulation of be by alterations in chromatin how this to the of is The analysis of function demonstrated that this is for the of the but for the response to A that to the response to is et al., 2001). in this by that of the in response to The also flowering, and of et al., et al., 2001). are with the that a regulator of and that in the of activity of this to of genes and of which is by et al., 2001). The a genetic between and The a that may a these have been of a of other plant but a in has been demonstrated et al., 2001). genes involved in and for response to the will from genetic and the on the analysis of that there may be to the of stress is a The a of that are flowering under all and are to and et al., and The between these by the that all of than plants in the long-day pathways and et al., to flowering by of and in plants this can be to a for also demonstrated because the of and 2001). Nevertheless, the of with of The and flowering in a and the in this is to in these genes. However, the does flowering in but does in other ecotypes that the but the of responds to of (Koornneef et al., et al., in the regulation of to be all of the by genetic that may all in a For example, are flowering than be a of a of these and and to be a for these genes in plant than flowering time (Koornneef et al., of the genes within the have been The of an the to and a et al., shown to in also an that regulation may play a in the et al., 2001). The a and putative and may a et al., genes are in a with the of the plant and and in and of flowering under short days, whereas of effects on flowering but in this regulation of in the of the et al., et al., 2001). The in which these is However, plants of within the and of plants the same time the This that in within the in other of the to the of the et al., may of Flowering in Arabidopsis. of a by of are by the and genes. The also signaling and of and may to promote the activity of by in which signaling may by has been in Arabidopsis, but has been shown to be involved in signaling in in and to the that it is involved in the demonstrated of the in response to The is the by The flowering-time is also by whereas and to between and the regulation of flowering genes may of but of The this are in in the Flowering in Arabidopsis. of a by of are by the and genes. The also signaling and of and may to promote the activity of by in which signaling may by has been in Arabidopsis, but has been shown to be involved in signaling in in and to the that it is involved in the demonstrated of the in response to The is the by The flowering-time is also by whereas and to between and the regulation of flowering genes may of but of The this are in in the have been in Arabidopsis, and the genes for the and genes in flowering time have been an that the in and The is to flower in short days, and is flowering than is the under long et al., plants are also in the of and In to the and have rise to plants that produce with (Koornneef and The and are in and et al., is by environmental that it may be involved in a in et al., of this plants are from short to long days, and with conditions that flowering et al., Furthermore, plants of also and earlier than control plants under long-day and short-day conditions et al., et al., This that are on flowering and is with that of flowering of plants. A for in the control of flowering is also by genes involved in related genes with roles in and have and with other et al., et al., and to et al., and to the of et al., 1999; et al., and et al., and also a their that the the in an the to and This is in et al., et al., and are to responses in the of and this A of this model is that responses in the of and genes This by plants, which low of in which and also The of the growth of and the of so that the earlier than the under short and et al., 2001). with the that are earlier flowering than plants, that the shown by is to of flowering by and This is an important because the all of the For example, the the and of of the may be by and other related and and flower of plants in which by to the effects of of and and of is to the In to and However, may also be involved in and In plants a the and and the may play a in responses in the where and are The to play an important in the by which the function of and This by the analysis of a a within the because this growth and flowering in the of et al., of the may to to so that it to repress growth and flowering in the of et al., for this model from recent analysis of The in the in the of but in the of is et al., 2001). However, this is by of the et al., 2001). regulation of by may be by a that the of plants a the also of responses and to plants and However, this be a for the regulation of these The regulator of responses that flowering in of the effects of these are to in genes the of and The is flowering, to the effects of activity of the pathway. of et al., and in et al., that is to in and et al., The in which this to responses is but it of and may be for in and flowering time regulation are and in and has been the in Arabidopsis et al., 2001). However, is the in response to This to a of which on which other can and a related to that in components of the The of and to the system that it of and be involved in in the in response to there is of this is in the the to flowering, and flowering et al., et al., On the basis of genetic by that with that flowering, to promote flowering the pathway. a function is the a to a flowering, and is by of a et al., 2001). have genetic between the and other flowering-time pathways. For example, genetic analysis that the in to the long-day because there is between the pathways. The of that the is under short days, and with that the long-day that flower under long et al., Reeves and Coupland, 2001). This that in short days, where the long-day is is the flowering and of function of this can long days, the of of the is because of the activity of the long-day pathway. is also recent for a between a an that in the and et al., 2001). mutants, and activity of a plants of and which is with of the et al., and plants also show to for and et al., 2001). the flowering by to be to the et al., This model that to repress activity the and to repress flowering, and this by However, plants, which flower under long flower the to to under long does require and this that the is the basis of the recent that of the flowering-time is by and by the long-day that the does the same flowering-time genes the other flowering-time pathways et al., 2000; et al., 2000; Samach et al., also on in which promote flowering is by the activity of the of is in in and in with and et al., et al., of also flowering of in short et al., The of on to a that is to the for and A which a of that activation of by and is the to with this in et al., 2001). is by plants than plants, that an in the regulation of flowering time et al., Arabidopsis have been that flower but progress from to flowering et al., et al., et al., 2001). The of this of flower which a and that et al., A with a et al., The flower are and genes that are to promote growth to repress flowering and The and the which and in the are in of et al., However, the of in in with the that of of these genes is for the A of of the genes by their The a an and a et al., 2001). This to Arabidopsis and which by and to a The a involved in the of of et al., 2001). The is for of the and of et al., and in of the et al., The of and to that these plant may in a to of in to repress by chromatin The may of a that and the of genes that promote The of genes in also by the that Arabidopsis which is related to the in the et al., 2001). because to However, the of the in the because are for et al., from a that but in the it be demonstrated that is for the of flowering in the et al., 2001). for and from a and The effects of on and are to those of the and a a and a that et al., 1999; et al., 2000; et al., However, and in the may in the with other related to and to a that for a is a in the of and show an et al., The analysis of that flowering in the a for to so that can The activation of flowering by environmental conditions photoperiod and be to these and that flower is is also that chromatin can affect flowering by changing The a a that is related to genes of the in chromatin et al., of of which affect flowering time et al., of the by these is of in flowering to in the of the which and of et al., a et al., of with the other and flowering in the that the of a of genes involved in flowering-time regulation. genetic pathways flowering in response to different environmental but these pathways converge to the of the same genes. For example, all of the flowering-time pathways to the activation of the same set of genes that within the and Coupland, is the of the known genes to be and of the et al., of the to the to that responds to the long-day flowering and to Furthermore, of a putative within the activation by but by the long-day and for the and a in which this under long but the under short days, where the pathway. This activation of the demonstrated that activation of by of these flowering pathways is the and long-day pathways converge on the than pathways an earlier that in the of and of the among Arabidopsis Flowering The pathways in in to emphasize their In particular, the effects of the integration of the photoperiod, and pathways on the regulation of of and is The this model are in in the of the among Arabidopsis Flowering The pathways in in to emphasize their In particular, the effects of the integration of the photoperiod, and pathways on the regulation of of and is The this model are in in the The of and by in the of an important of the of flowering time to changing This responses to environmental and which need to be to produce a response. For example, the annual growth habit the of flowering by the plant has been to which the plant to the following The between and in the activation of genes and can an because the activation of these genes by may be by the but in to of the genes the long of the following The analysis of that this a of convergence of flowering-time pathways. within the in response to to the in which function is related to in of the genes is The between and has been studied the genetic and molecular The the of that does of et al., Furthermore, the flowering by to the flowering of effects on whereas et al., of these results that does of to but in a pathway. In particular, the of other genes et al., the activation of and may by and