Year: 2000
Type: review
Abstract: One of the most important environmental factors affecting flowering time is the daily duration of light, the photoperiod, which was first discovered by Garner and Allard in the 1920s (Thomas and Vince-Prue, 1997, and refs. therein). Plants in which flowering occurs or is accelerated in short days (SD) or long days (LD) are known as SD plants or LD plants, respectively. LD plants often flower in later spring or early summer (when the daylength becomes longer) to set seeds in a favorable season. SD plants generally flower in fall (when photoperiods are getting shorter) to finish reproduction before the cold winter arrives. Synchronization of flowering time with a reliable environmental cue such as the photoperiod also increases the chance of out-breeding and genetic recombination. The photoperiodic control of flowering is brought about by the interactions of genes involved in the developmental control of floral initiation, the regulation of the circadian clock, and the signal transduction of photoreceptors (Thomas and Vince-Prue, 1997). Recent molecular genetic studies in a facultative LD plant, Arabidopsis, have made notable progress in identifying genetic pathways and molecular components associated with the control of flowering time and the function of the circadian clock, which have been discussed in two recent Updates (Pineiro and Coupland, 1998; Somers, 1999). This Update focuses on the recent advances in our understanding of plant photoreceptors phytochromes and cryptochromes, and their roles in the regulation of flowering time. Flower formation is initiated by the transition of the apical meristem from a vegetative fate to a floral fate. Mechanisms that control the timing of floral initiation have been extensively studied in Arabidopsis by the identification of mutations that flower earlier or later than the wild type but otherwise remain healthy (Koornneef et al., 1998). These mutations are known as flowering-time mutations and the corresponding genes are known as flowering-time genes. In addition, many genes that were initially studied for their roles in other aspects of plant development, such as light perception, hormone metabolism, signal transduction, and floral meristem specification, also play roles in the regulation of flowering time and are sometimes also referred to as flowering-time genes. Based on phenotypic and genetic epistasis analysis of these mutations, flowering-time genes have been grouped into several signal transduction pathways that either suppress or promote floral initiation. These signaling pathways transmit either the developmental or environmental signals to regulate the expression of the floral-meristem-identity genes that control the formation of the floral meristem. Readers are referred to two recent reviews for detailed discussions of genes associated with these pathways in Arabidopsis (Koornneef et al., 1998;Levy and Dean, 1998). One of the major signal transduction pathways regulating flowering time is known as either the LD promotion pathway (Koornneef et al., 1998) or the photoperiodic pathway (Levy and Dean, 1998), which relays light and photoperiodic timing signals to the floral initiation process. Mutations of genes in this pathway reduce a plant's responsiveness to photoperiods. As a facultative LD plant, Arabidopsis grown in LD conditions flowers earlier than when grown withinSD. Misexpression of genes associated with the LD pathway may also delay the flowering of Arabidopsis plants grown in LD, but does not alter the flowering time of plants grown inSD, resulting in reduced sensitivity (hyposensitive) to photoperiod. Mutations in genes such as CO(CONSTANS; Putterill et al., 1995),PHYA (phytochrome A; Johnson et al., 1994; Reed et al., 1994), CRY2 (cryptochrome 2; Guo et al., 1998), andGI (GIGANTEA; Fowler et al., 1999; Park et al., 1999), are of this type. The elevated expression of the CCA1(circadian clock associated; Wang and Tobin, 1998) and LHY(late elongated hypocotyl; Schaffer et al., 1998) genes also results in photoperiod-hyposensitive late-flowering. On the other hand, a mutant that flowers earlier than the wild type in both LD and SD may also have reduced sensitivity to photoperiod. Early-flowering mutations in genes such as PHYB(phytochrome B; Goto et al., 1991), PHYD (phytochrome D;Aukerman et al., 1997; Devlin et al., 1999b), PHYE(phytochrome E; Devlin et al., 1999a), ELF3 (early flowering; Hicks et al., 1996; Zagotta et al., 1996), andPEF (phytochrome early flowering; Ahmad and Cashmore, 1996) belong to this group. We often assume that a late-flowering mutation corresponds to a gene product that normally promotes floral initiation, whereas an early-flowering mutant implies that the corresponding gene product is a suppressor of floral initiation. Not surprisingly, many genes isolated to date that are associated with the photoperiodic pathway encode either photoreceptors or proteins associated with the circadian clock. The primary photosensory receptors of higher plants are the red/far-red light receptors called phytochromes and the blue/UV-A light receptors called cryptochromes (Kendrick and Kronenberg, 1994). Blue light (approximately 400–500 nm) and red light (approximately 600–700 nm) are the two spectra of solar radiation that are most effectively absorbed and utilized by the photosynthetic system of plants. Therefore, the regulation of plant development by phytochromes and cryptochromes allows plants to optimize their developmental processes in coordination with the availability of energy and metabolite resources. Phytochromes are photochromic proteins that exist as two photo-interconvertible isomeric forms: the red-light-absorbing form (Pr) and the far-red-light-absorbing form (Pfr; Kendrick and Kronenberg, 1994; Hughes, 1999). Arabidopsis has five phytochrome genes, PHYA to PHYE, which encode the apoproteins of PHYA to PHYE, respectively (Quail et al., 1995). Mutations in four of the Arabidopsis phytochrome genes have been isolated and studied (see below). Different phytochromes regulate either distinct light responses or similar responses under different light conditions (light quantity, quality, and timing). Taking the well-characterized light-inhibition of hypocotyl elongation as an example (Quail et al., 1995), the phyA mutant is impaired in hypocotyl inhibition in far-red light, but not in red light. Conversely, the phyBmutant loses the ability to inhibit hypocotyl elongation in red light, but not in far-red light, suggesting that although phyA and phyB both mediate light inhibition of hypocotyl elongation, phyA functions primarily in far-red light, whereas phyB acts mainly in red light. Cryptochromes are flavoproteins that share amino acid sequence similarity with DNA photolyases that catalyze blue/UV-A light-dependent DNA repairing (Sancar, 1994; Cashmore et al., 1999). Cryptochromes have no DNA photolyase activity; they usually have a C-terminal domain with little sequence homology to photolyase and they show characteristics of blue/UV-A light receptors in plants. Arabidopsis has at least two cryptochrome genes, CRY1 and CRY2. Similar to phytochromes, genetic studies of Arabidopsis cryptochrome mutations affecting light-dependent hypocotyl inhibition have played a critical role in our understanding of cryptochromes. The isolation of an Arabidopsis mutant, hy4, which has an elongated hypocotyl in blue light, allowed the of the first cryptochrome gene (Koornneef et al., Ahmad and Cashmore, The later referred to as a associated with a that blue/UV-A light, as was for a plant blue/UV-A light et al., plant's sensitivity to blue/UV-A light by the expression of et al., The Arabidopsis cryptochrome was CRY1 as the et al., 1998). The amino acid sequence of CRY2 and CRY1 are about but most of the sequence similarity is in the whereas the C-terminal are et al., 1998). is in to blue light et al., 1998; Guo et al., 1999), which is of the of phyA et al., and refs. therein). is not role the of phyA and may but no in the expression has been for Based on the that plants were to blue light, a genetic was to for Arabidopsis a long hypocotyl in blue light et al., 1998; et al., 1998). the resulting from this a in flowering time than in hypocotyl inhibition and to to a photoperiod-hyposensitive late-flowering mutation by Guo et al., 1998). the isolation of the Arabidopsis cryptochrome genes have been isolated from not other plant and but also and et al., and refs. therein). of and cryptochromes have that these proteins play important roles in the function and regulation of circadian et al., 1998; et al., 1999). photoreceptors light signals to are the early of signal may light signals to other by a light-dependent or may by and with signaling that at least for phytochromes, the early of the signal transduction both of phytochromes are and with signal proteins in a light-dependent phytochromes were first to than a et al., but this has a In light of the phytochrome has and 1997; Cashmore, 1998; and 1998; and 1999; Hughes, 1999). that has from this is the identification of the of the phytochrome transduction in flowering plants. recent have this et al., 1998; et al., 1999). One for the of phytochrome to the discovered was that cryptochromes with phyA in and in the the CRY1 in by phyA the in of by phyA was in red light or blue light than in the et al., 1998). The of was also to in in a and which the of a the of of for phytochrome is (phytochrome et al., 1999). The gene was isolated from a the C-terminal domain of Arabidopsis PHYA as the in by the to both the and of is a than in the of In with a of phytochromes, was in in a The that was in plants phyB an of phyB in the of in played a role in phyB plants the similar to that of a phyB plants elongated in red light but not in blue or far-red light et al., 1999). may also regulate the of other a to such an et al., 1999). In an in the form of phyA to about to four than the The of not to the of this in an in in both the and may play a role in phytochrome signal Arabidopsis mutant with gene by a sensitivity to both red light and far-red light in and et al., 1999). photoreceptors in the Phytochromes and cryptochromes are both and that both of photoreceptors the either or in a light-dependent The of phytochromes and cryptochromes has been studied In these a a of a and a such as or is in plants, and the of the is by the of the These studies that phyA and phyB in the in the but are to the in the light and 1996; et al., 1999; et al., 1999). Arabidopsis and are also although no light regulation of the of cryptochromes has been et al., 1999; Guo et al., 1999; et al., 1999). is for in 1999). In the of a a to a and in the with the may the of the to the similar may also played by plant has been that may as a for phytochromes in conditions such as the et al., 1999; 1999). the of the in the a may with other proteins to gene expression 1999). two and have been The gene was by of the of mutation that was isolated as an suppressor of mutation et al., 1999). is a that has a and a domain et al., 1999). mutant plants an hypocotyl inhibition in to light, suggesting that is a of The expression of was in light the of phytochromes, a regulation on the phytochrome signal The gene (phytochrome was isolated on the of with the C-terminal domain of in a et al., 1998). a domain and a domain that may have a role in the with of genes. The in and phytochromes was on red with the but with the form of Arabidopsis phyB et al., 1999). In to the expression of was in light et al., 1999). is a of phytochrome plants a reduced hypocotyl inhibition in to light. with the that and of phytochrome to a such as may of the signal transduction to the regulation of gene plants reduced light responsiveness for expression of genes et al., 1998). is that although Arabidopsis studied to date has been to play a role in both hypocotyl inhibition and floral initiation, most mutations or plants the genes have no in flowering time. of these factors to may that are two phytochrome signal transduction pathways to the two different developmental of the flowering-time genes associated with the photoperiodic pathway and have functions in both hypocotyl inhibition and flowering time (Levy and Dean, and refs. therein). These may not by signal transduction pathways of the in this In for photoreceptors regulating photoperiodic spectra have been extensively in different plants to light flowering time. These early with of the of light on and elongation, to the of phytochrome (Thomas and Vince-Prue, 1997, and refs. therein). The recent studies of mutations have allowed to functions of photoreceptors in the regulation of flowering time. of the most to the spectra of light regulation of flowering time are the and the (Thomas and Vince-Prue, 1997). In a the SD photoperiod is by a light at the of the photoperiod. a the light is often in the of a long conditions the LD photoperiod that promotes flowering in LD plants, and are referred to as in the In Arabidopsis, far-red light, blue light, and red light were at flowering in although red light was the least et al., 1998). with far-red light or light in far-red spectra are also in flowering et al., et al., 1995). of red and blue light on Arabidopsis flowering time. The Arabidopsis plants were at for in the and grown under or light The plant grown in blue light for that in light for and the plant grown in red light was not flowering was about before phyA promotes The Arabidopsis phyA mutant flowers later than plants in LD et al., 1994; and 1998) or conditions with either et al., or et al., 1994; and 1998). with the that phyA a role in Arabidopsis plants phyA earlier than the wild type in both SD and conditions et al., 1995). phyA mutant plants and plants sensitivity to photoperiod, they at about the time in SD as in the mutant of LD plant, also a similar to that of the Arabidopsis phyA The phyA mutant normally photoperiods but to to with the mutant at about the time and conditions et al., 1997). the phyA mutant a that delay the flowering of the plants, suggesting that phyA signaling may suppress the of a floral suppressor et al., 1997). or functions of photoreceptors in regulating floral initiation of The signal transduction pathways of the and with a Arabidopsis mutation was as a of the which no et al., 1997). mutant was into genetic and to The mutant plants no phenotypic whereas plants impaired in both the and genes earlier than the mutation in both LD and SD conditions et al., 1997; Devlin et al., This The the ability to to the far-red light by elongated and accelerated responses known as the and 1997; Devlin et al., 1999). flowering under in which is far-red light, may plants to their before the of other plants becomes has been that Arabidopsis has at least other phytochrome associated with responses et al., Based on the that Arabidopsis has phytochrome associated with responses et al., 1999b), a genetic was to for mutations that elongated resulting in the isolation of mutation et al., The no phenotypic was in mutant This the function of is also similar to that of other mutant earlier than mutant in SD conditions et al., In SD plants mutations in both the and early that the no of flowering et al., that phyB and normally inhibit flowering in a but their by an Plants mutations in and genes have reduced of floral initiation, that they flower early with or the The two Arabidopsis impaired in phytochrome and earlier than the wild type in both LD and SD conditions et al., the of is to phytochromes, may that the of the of phytochromes with to the floral initiation of The that the of Arabidopsis phytochromes play roles in flowering to with this The function of in flowering although may have a The mutant the was to flower under SD conditions and 1995). was also that mutant in the in both SD and conditions with either or and that with blue light a than with light or red light et al., in to other is a of in the flowering time of mutant et al., and et al., 1996; Zagotta et al., 1996; et al., 1999). of these may by to other mutant the and the earlier than the wild type in SD which was as the of the phyB and the mutant CRY1 et al., 1998). the in flowering time also in the mutant et al., 1996; Zagotta et al., 1996; et al., 1999). The of of in floral initiation promotes are to the photoperiod-hyposensitive late-flowering mutant, although the the than the the Guo et al., 1998; et al., 1998). mutant plants in LD but not in SD plants early in SD but not in LD Therefore, either a mutation or an of the CRY2 gene in the reduced sensitivity to photoperiods. blue light is known to promote flowering of Arabidopsis, may that the mutant, which is impaired in a blue light show a flowering in blue light. this was not the The mutant at the time as the wild type in blue light or red light, but the late-flowering of in light in light et al., et al., 1999). Therefore, the flowering promotion function of is on both blue and red light. is the late-flowering of the in the of both blue light and red In other does the function of a blue light red was that a cryptochrome may to by a phytochrome in red light to et al., 1998). this may not flowering genetic studies have that phytochromes and often on floral initiation. the function of in flowering to the of red and blue light, that either the is or that red light is not for the of et al., 1999). The as in the in that promotes flowering of the inhibition of floral initiation et al., 1998; et al., 1999). phyB mutant plants a early-flowering in red light than in light or light. similar to function in hypocotyl elongation, the of phyB in floral initiation is also on red light et al., 1998). with the that phyB flowering whereas phyB mutant as early as mutant in light. The not suppress the mutant in light et al., 1999), which may by the function of and or inhibition of floral initiation is on red light to may also exist and known to promote mutant plants earlier than mutant, and in the mutant as early as the phyB mutant et al., 1994; Devlin et al., 1996; and 1998). These that phyA may also inhibit the function of and and as the phyA mutant in to a with light in far-red spectra et al., 1994), is to to the and phyB and to the phyA function in hypocotyl phyA may mediate a inhibition of the phyB function One of this to the flowering time of the Arabidopsis wild type with phyA grown in light or in far-red light under conditions plants to flower in the of and In to photoreceptors in to regulate floral initiation. As and inhibit flowering in a Similar has also been for and mutant in blue light, although the mutant flowering in such conditions et al., 1999). This was to that in to to also a promotion of floral initiation, but the of is by et al., 1999; does the of a floral that both phytochrome and cryptochrome the is the that photoreceptors regulate expression of flowering-time genes for signal has been that flowering-time genes are in different photoperiods. the of the was in LD than in SD conditions et al., 1997). This is floral initiation is to a by the of expression and 1995). with the important role of floral initiation and the of phyB and on flowering the mutation of the CRY2 or has been to or respectively et al., 1998; and 1999). of flowering-time is also on photoperiod, and is at higher in LD than in SD conditions et al., 1995). was that was at mutant plants than the wild type in LD whereas expression was elevated in plants CRY2 in both LD and SD conditions et al., 1998). On the other hand, the expression of not to in the phyB mutant and 1999). the function of to the expression of may in or mutant plants. of the expression of flowering-time genes in mutations and under different photoperiodic conditions may a of the role of different photoreceptors in the regulation of expression of the flowering-time genes. photoreceptors may regulate flowering time in to different photoperiods. The daylength signal may by the circadian clock, to floral initiation the circadian clock may regulate the signal transduction of photoreceptors affecting floral initiation, as by the signal transduction at the but at the of the circadian of an pathway of the circadian clock The of the circadian clock at the of a a plant's responsiveness to the light on floral initiation, which often the photoperiodic the conditions as plants grown in a photoperiod to and with light at different the of light on floral initiation may or at of by the of the circadian clock 1998). regulation of the signal transduction of photoreceptors by the circadian clock has been referred to as and The circadian clock is an or may as the signaling system that is made of that the circadian an pathway that the to the environmental such as light, and an pathway that of the to circadian 1999; Somers, 1999). the molecular of the circadian clock in plant studies in other have a as the of the 1999). Arabidopsis flowering-time genes have been isolated and to associated with the function of the circadian clock. Mutations or of these genes in a photoperiodic of which the for the role of the circadian clock in the regulation of photoperiodic The genes known to flowering time and was isolated as a photoperiod-hyposensitive early-flowering mutation that early in both LD and also an elongated hypocotyl in red and blue light et al., mutant circadian for and when under light, but the mutant in suggesting a function of ELF3 in the pathway et al., The Arabidopsis was isolated as a circadian clock mutation that has a short in et al., The of daylength on flowering time was in the mutant in the and was when the mutation was into the is that the of the earlier or later than the wild type in SD or LD respectively et al., whereas other flowering-time mutations flowering time in early or of the gene may into photoperiodic and both encode which when photoperiod-hyposensitive elongated in light, and circadian in Arabidopsis et al., 1998; Wang and Tobin, 1998). The expression of both circadian that by the of the The mutant a of circadian expression of several genes and Tobin, 1999). and may in a in the regulation of the circadian clock. and are by the has been to and both and et al., 1999). of the which a of in of many genes, and photoperiod-hyposensitive early flowering et al., 1999). photoperiod-hyposensitive late-flowering mutation in Arabidopsis is (Koornneef et al., 1998). gene was and to encode a et al., 1999; Park et al., 1999). is a may the time of floral initiation, which been to by the regulation of the expression of flowering-time genes. The of and ELF3 were to on other et al., 1999; Park et al., 1999). The expression of a circadian with different in LD and SD conditions et al., 1999). is that the circadian expression of other flowering-time genes, and may also have distinct in different photoperiods. The function of these genes may the floral initiation process. these genes may as the factors to regulate the signal transduction of a as by the of these proteins flowering time our understanding of the photoperiodic The circadian clock is by the of photoreceptors to with a of about In light, the of photoreceptors generally the of the clock, resulting in to that in et al., 1995). has been that mutations of and CRY1 the circadian of to at a a than that of the wild type under light conditions et al., This that in the regulation of the Arabidopsis circadian clock, phyA acts in of red light and blue light, phyB functions in red light, and acts in both and of blue light. The function of phyA in the of the circadian clock in to blue light was by that the phyA mutant was in to a in but not in blue light with the wild type. reduced sensitivity to photoperiod, not the circadian clock, at least when was for the et al., This is with a that may not have a major role in light regulation of the circadian clock. and are involved in the regulation of the circadian clock, is to the in flowering time in the and is the of the of regulation of the circadian clock, a of the of the on the floral initiation or is that mutations in and CRY1 genes the circadian clock in the similar for the circadian expression of the their on flowering time were and sometimes the phyA mutant but the phyB mutant This to that the in flowering time of and are to the of a of the circadian clock. these photoreceptors may the floral initiation but the signal transduction of photoreceptors may than by the circadian clock, as by the The function of the circadian clock in regulating flowering time by the photoperiodic or the circadian of floral in to light at different of the (Thomas and Vince-Prue, 1997). Arabidopsis plants grown conditions to flower by a at a and the promotion of flowering by such circadian 1998). This by an that the of a on floral initiation is by the circadian clock to phyA this also to the photoperiodic for other spectra of light in The floral initiation may example for signal phyB mutations of the SD plant and the LD plant Arabidopsis both an early-flowering This was that the flowering of SD and LD plants to One of this is that phyB may suppress floral initiation of but the signal transduction or responsiveness to phyB signaling is by the of the circadian clock, resulting in different daylength responses in the flowering time of different plants. the of on floral initiation may by the As the function of is involved in photoperiodic both mutation and of the CRY2 gene in reduced responsiveness of floral initiation to photoperiods. and is not involved in light of the circadian clock. Therefore, the of on photoperiodic flowering is to from signal transduction the plant's to by an of the circadian clock in different daylength Recent molecular genetic studies of plant photoreceptors have that the of phytochromes and cryptochromes either suppress or promote floral initiation, and that a may function the to of the flowering-time genes. photoreceptors control photoperiodic may regulate flowering time in to different photoperiods regulation of the circadian clock. the of a on floral initiation may by the circadian clock, resulting in different responses in different photoperiods. is that the expression or of a signaling may with distinct in different and as such may as the that the signal transduction of a the flowering in different photoperiods. The identification of such factors and of the expression or of these factors the function of photoreceptors may light on the of photoreceptors in the control of flowering time. The and other for critical of the and for and for to the of an Arabidopsis flower from
Source: PLANT PHYSIOLOGY
DOI: 10.1104/pp.123.1.39
Author: Chentao Lin
Institution: University of California, Los Angeles
Language: English
Topic: Light effects on plants
Subfield: Plant Science
Domain: Life Sciences
Open Access status: green
Award: G5388775558
OpenAlex ID: W2002627943