The seasonal cue day length regulates the timing of the floral transition in plants through periodic histone modifications of the FT gene, which encodes a flowering signal in plants. These modifications dampen FT expression at dusk to prevent precocious flowering.
The developmental transition from a vegetative to a reproductive phase (i.e., flowering) is timed by the seasonal cue day length or photoperiod in many plant species. Through the photoperiod pathway, inductive day lengths trigger the production of a systemic flowering signal, florigen, to provoke the floral transition. FLOWERING LOCUS T (FT), widely conserved in angiosperms, is a major component of the mobile florigen. In the long-day plant Arabidopsis, FT expression is rhythmically activated by the output of the photoperiod pathway CONSTANS (CO), specifically at the end of long days. How FT expression is modulated at an adequate level in response to the long-day cue to set a proper flowering time remains unknown. Here, we report a periodic histone deacetylation mechanism for the photoperiodic modulation of FT expression. We have identified a plant-unique core structural component of an Arabidopsis histone deacetylase (HDAC) complex. In long days, this component accumulates at dusk, and is recruited by a MADS-domain transcription factor to the FT locus specifically at the end of the day, leading to periodic histone deacetylation of FT chromatin at dusk. Furthermore, we found that at the end of long days CO activity not only activates FT expression but also enables HDAC-activity recruitment to FT chromatin to dampen the level of FT expression, and so prevent precocious flowering in response to the inductive long-day cue. These results collectively reveal a periodic histone deacetylation mechanism for the day-length control of flowering time in higher plants.
The timing of the developmental transition from a vegetative to a reproductive phase is critically important for reproductive success in flowering plants. Plants synchronize the timing of their floral transition with the changing seasons to flower at a suitable time. The change in day length, or photoperiod, is a key seasonal cue, especially at high latitudes. It is through the photoperiod pathway that day lengths trigger the production of a systemic flowering signal, florigen, to induce the transition from vegetative to reproductive growth and flowering. The FT protein is a major component of the mobile florigen signal. In the model flowering plant Arabidopsis, FT mRNA expression is rhythmically activated by the gene CONSTANS, which is the output of the photoperiod pathway, specifically at the end of long days. In this study, we aimed to address how the level of FT expression is modulated in response to the long-day cue to set the appropriate flowering time. We show that on long days a transcription factor recruits histone deacetylase activity to remove acetyl marks from histones at the FT gene specifically at dusk, thereby dampening FT mRNA expression upon its transcriptional activation by CONSTANS. This sets the correct level of FT expression at the end of long days, and thus prevents precocious flowering in response to the long-day cue.
Plants synchronize their cellular and physiological functions according to the photoperiod (the length of the light period) in the cycle of 24 h. Photoperiod adjusts several traits in the plant life cycle, including flowering and senescence in annuals and seasonal growth cessation in perennials. Photoperiodic development is controlled by the coordinated action of photoreceptors and the circadian clock. During the past 10 years, remarkable progress has been made in understanding the molecular mechanism of the circadian clock, especially with regard to the transition of Arabidopsis from the vegetative growth to the reproductive phase. Besides flowering photoperiod also modifies plant photosynthetic structures and traits. Light signals controlling biogenesis of chloroplasts and development of leaf photosynthetic structures are perceived both by photoreceptors and in chloroplasts. In this review, we provide evidence suggesting that the photoperiodic development of Arabidopsis leaves mimics the acclimation of plant to various light intensities. Furthermore, the chloroplast-to-nucleus retrograde signals that adjust acclimation to light intensity are proposed to contribute also to the signaling pathways that control photoperiodic acclimation of leaves.
acclimation; chloroplast biology; circadian clock; leaf/vegetative development; light signaling; photomorphogenesis; plastid signaling
The circadian system drives pervasive biological rhythms in plants. Circadian clocks integrate endogenous timing information with environmental signals, in order to match rhythmic outputs to the local day/night cycle. Multiple signaling pathways affect the circadian system, in ways that are likely to be adaptively significant. Our previous studies of natural genetic variation in Arabidopsis thaliana accessions implicated FLOWERING LOCUS C (FLC) as a circadian-clock regulator. The MADS-box transcription factor FLC is best known as a regulator of flowering time. Its activity is regulated by many regulatory genes in the "autonomous" and vernalization-dependent flowering pathways. We tested whether these same pathways affect the circadian system.
Genes in the autonomous flowering pathway, including FLC, were found to regulate circadian period in Arabidopsis. The mechanisms involved are similar, but not identical, to the control of flowering time. By mutant analyses, we demonstrate a graded effect of FLC expression upon circadian period. Related MADS-box genes had less effect on clock function. We also reveal an unexpected vernalization-dependent alteration of periodicity.
This study has aided in the understanding of FLC's role in the clock, as it reveals that the network affecting circadian timing is partially overlapping with the floral-regulatory network. We also show a link between vernalization and circadian period. This finding may be of ecological relevance for developmental programing in other plant species.
FT-INTERACTING PROTEIN 1 is a novel protein that is involved in transporting florigen, a long-known mobile signal that induces flowering in plants in response to day length, from companion cells to sieve elements in the phloem of Arabidopsis.
The capacity to respond to day length, photoperiodism, is crucial for flowering plants to adapt to seasonal change. The photoperiodic control of flowering in plants is mediated by a long-distance mobile floral stimulus called florigen that moves from leaves to the shoot apex. Although the proteins encoded by FLOWERING LOCUS T (FT) in Arabidopsis and its orthologs in other plants are identified as the long-sought florigen, whether their transport is a simple diffusion process or under regulation remains elusive. Here we show that an endoplasmic reticulum (ER) membrane protein, FT-INTERACTING PROTEIN 1 (FTIP1), is an essential regulator required for FT protein transport in Arabidopsis. Loss of function of FTIP1 exhibits late flowering under long days, which is partly due to the compromised FT movement to the shoot apex. FTIP1 and FT share similar mRNA expression patterns and subcellular localization, and they interact specifically in phloem companion cells. FTIP1 is required for FT export from companion cells to sieve elements, thus affecting FT transport through the phloem to the SAM. Our results provide a mechanistic understanding of florigen transport, demonstrating that FT moves in a regulated manner and that FTIP1 mediates FT transport to induce flowering.
The transition to flowering is the most dramatic phase change in flowering plants and is crucial for reproductive success. Such a transition from vegetative to reproductive growth is controlled by seasonal changes in day length. Studies originally performed in the 1930s were the first to suggest that day length is perceived by a plant's leaves; by contrast, flower formation takes place in the shoot apical meristem (the tip of the shoot that gives rise to plant organs, such as leaves and flowers). The term “florigen” was later proposed to describe a mobile floral stimulus that moves from leaves to the shoot apical meristem to induce flowering. It is only recently that FLOWERING LOCUS T (FT) in Arabidopsis, and its orthologs in various other plant species, was identified as being florigen, but how florigen is transported in plants remains completely unknown. Here, we report that a novel ER membrane protein, FT-INTERACTING PROTEIN 1 (FTIP1), interacts with FT in companion cells of the phloem (a specialized type of parenchyma cell in the phloem of the plant's vascular system) and mediates FT protein movement from companion cells to sieve elements (the conducting cells of the phloem), thus affecting FT transport to the shoot apical meristem in Arabidopsis. To our knowledge, this study reveals the first regulator that is required for florigen transport and offers new insights into possible florigen transport mechanisms in other flowering plants.
In order to maximize reproductive success, plants have evolved different strategies to control the critical developmental shift marked by the transition to flowering. As plants have adapted to diverse environments across the globe, these strategies have evolved to recognize and respond to local seasonal cues through the induction of specific downstream genetic pathways, thereby ensuring that the floral transition occurs in favorable conditions. Determining the genetic factors involved in controlling the floral transition in many species is key to understanding how this trait has evolved. Striking genetic discoveries in Arabidopsis thaliana (Arabidopsis) and Oryza sativa (rice) revealed that similar genes in both species control flowering in response to photoperiod, suggesting that this genetic module could be conserved between distantly related angiosperms. However, as we have gained a better understanding of the complex evolution of these genes and their functions in other species, another possibility must be considered: that the genetic module controlling flowering in response to photoperiod is the result of convergence rather than conservation. In this review, we show that while data clearly support a central role of FLOWERING LOCUS T (FT) homologs in floral promotion across a diverse group of angiosperms, there is little evidence for a conserved role of CONSTANS (CO) homologs in the regulation of these loci. In addition, although there is an element of conserved function for FT homologs, even this component has surprising complexity in its regulation and evolution.
flowering time; CONSTANS; FLOWERING LOCUS T; photoperiod
Day-length and the circadian clock control critical aspects of plant development such as the onset of reproduction by the photoperiodic pathway.1 CONSTANS (CO) regulates the expression of a florigenic mobile signal from leaves to the apical meristem and thus is central to the regulation of photoperiodic flowering.2 This regulatory control is present in all higher plants,3 but the time in evolution when it arose was unknown. We have shown that the genomes of green microalgae encode members of the CONSTANS-like (COL) protein family. One of these genes, the Chlamydomonas reinhardtii CO homolog (CrCO), can complement the co mutation in Arabidopsis.4 CrCO expression is controlled by the clock and photoperiod in Chlamydomonas and at the same time is involved in the correct timing of several circadian output processes such as the accumulation of starch or the coordination of cell growth and division. We have proposed that, since very early in the evolutionary lineage that gave rise to higher plants, CO homologs have been involved in the photoperiod control of important developmental processes, and that the recruitment of COL proteins in other roles may have been crucial for their evolutionary success.
photoperiod; flowering; constans; signaling; Arabidopsis; Chlamydomomas
In arabidopsis (Arabidopsis thaliana), FLOWERING LOCUS T (FT) and FLOWERING LOCUS C (FLC) play key roles in regulating seasonal flowering-responses to synchronize flowering with optimal conditions. FT is a promoter of flowering activated by long days and by warm conditions. FLC represses FT to delay flowering until plants experience winter.
The identification of genes controlling flowering in cereals allows comparison of the molecular pathways controlling seasonal flowering-responses in cereals with those of arabidopsis. The role of FT has been conserved between arabidopsis and cereals; FT-like genes trigger flowering in response to short days in rice or long days in temperate cereals, such as wheat (Triticum aestivum) and barley (Hordeum vulgare). Many varieties of wheat and barley require vernalization to flower but FLC-like genes have not been identified in cereals. Instead, VERNALIZATION2 (VRN2) inhibits long-day induction of FT-like1 (FT1) prior to winter. VERNALIZATION1 (VRN1) is activated by low-temperatures during winter to repress VRN2 and to allow the long-day response to occur in spring. In rice (Oryza sativa) a VRN2-like gene Ghd7, which influences grain number, plant height and heading date, represses the FT-like gene Heading date 3a (Hd3a) in long days, suggesting a broader role for VRN2-like genes in regulating day-length responses in cereals. Other genes, including Early heading date (Ehd1), Oryza sativa MADS51 (OsMADS51) and INDETERMINATE1 (OsID1) up-regulate Hd3a in short days. These genes might account for the different day-length response of rice compared with the temperate cereals. No genes homologous to VRN2, Ehd1, Ehd2 or OsMADS51 occur in arabidopsis.
It seems that different genes regulate FT orthologues to elicit seasonal flowering-responses in arabidopsis and the cereals. This highlights the need for more detailed study into the molecular basis of seasonal flowering-responses in cereal crops or in closely related model plants such as Brachypodium distachyon.
Flowering; vernalization; photoperiod; day length; VRN1; VRN2; FLC; FT; cereals; arabidopsis; MADS
Summary of recent advances
Plants possess a circadian clock that enables them to coordinate internal biological events with external daily changes. Recent studies in Arabidopsis revealed that tissue specific clock components exist and that the clock network architecture also varies within different organs. These findings indicate that the makeup of circadian clock(s) within a plant is quite variable. Plants utilize the circadian clock to measure day-length changes for regulating seasonal responses, such as flowering. To ensure that flowering occurs under optimum conditions, the clock regulates diurnal CONSTANS (CO) expression. Subsequently, CO protein induces FLOWERING LOCUS T (FT) expression which leads to flowering. It is emerging that both CO and FT expression are intricately controlled by groups of transcription factors with overlapping functions.
Determining the proper time to flower is important to ensure the reproductive success of plants. The model plant Arabidopsis is able to measure day-length and promotes flowering in long day (LD) conditions. One of the most prominent mechanisms in photoperiodic flowering is the clock-regulated gene expression of CONSTANS (CO) and the stabilization and activation of CO protein by light (regarded as external coincidence). We recently demonstrated that timing of the blue-light dependent formation of FLAVIN-BINDING, KELCH REPEAT, F-BOX 1 (FKF1) and GIGANTEA (GI) protein complex is crucial for regulating the timing of CO gene expression. The expression of FKF1 and GI is clock regulated, and their expression patterns have the same phase in LD (regarded as internal coincidence) but not in short day (SD) conditions, where floral induction is greatly delayed. Hence, timing of the FKF1-GI complex formation is regulated by the coincidence of both external and internal cues. Here, we propose a molecular mechanism for CO regulation by FKF1-GI complex formation.
Arabidopsis; circadian clock; photoperiodic flowering; CONSTANS; GIGANTEA; FKF1; CDF1
Transition to flowering in plants is tightly controlled by environmental cues, which regulate the photoperiod and vernalization pathways, and endogenous signals, which mediate the autonomous and gibberellin pathways. In this work, we investigated the role of two Zn2+-finger transcription factors, the paralogues AtVOZ1 and AtVOZ2, in Arabidopsis thaliana flowering. Single atvoz1-1 and atvoz2-1 mutants showed no significant phenotypes as compared to wild type. However, atvoz1-1 atvoz2-1 double mutant plants exhibited several phenotypes characteristic of flowering-time mutants. The double mutant displayed a severe delay in flowering, together with additional pleiotropic phenotypes. Late flowering correlated with elevated expression of FLOWERING LOCUS C (FLC), which encodes a potent floral repressor, and decreased expression of its target, the floral promoter FD. Vernalization rescued delayed flowering of atvoz1-1 atvoz2-1 and reversed elevated FLC levels. Accumulation of FLC transcripts in atvoz1-1 atvoz2-1 correlated with increased expression of several FLC activators, including components of the PAF1 and SWR1 chromatin-modifying complexes. Additionally, AtVOZs were shown to bind the promoter of MOS3/SAR3 and directly regulate expression of this nuclear pore protein, which is known to participate in the regulation of flowering time, suggesting that AtVOZs exert at least some of their flowering regulation by influencing the nuclear pore function. Complementation of atvoz1-1 atvoz2-1 with AtVOZ2 reversed all double mutant phenotypes, confirming that the observed morphological and molecular changes arise from the absence of functional AtVOZ proteins, and validating the functional redundancy between AtVOZ1 and AtVOZ2.
VOZ; Flowering; Arabidopsis; FLC; MOS
Brachypodium distachyon (Brachypodium) is a model for the temperate grasses which include important cereals such as barley, wheat and oats. Comparison of the Brachypodium genome (accession Bd21) with those of the model dicot Arabidopsis thaliana and the tropical cereal rice (Oryza sativa) provides an opportunity to compare and contrast genetic pathways controlling important traits. We analysed the homologies of genes controlling the induction of flowering using pathways curated in Arabidopsis Reactome as a starting point. Pathways include those detecting and responding to the environmental cues of day length (photoperiod) and extended periods of low temperature (vernalization). Variation in these responses has been selected during cereal domestication, providing an interesting comparison with the wild genome of Brachypodium. Brachypodium Bd21 has well conserved homologues of circadian clock, photoperiod pathway and autonomous pathway genes defined in Arabidopsis and homologues of vernalization pathway genes defined in cereals with the exception of VRN2 which was absent. Bd21 also lacked a member of the CO family (CO3). In both cases flanking genes were conserved showing that these genes are deleted in at least this accession. Segmental duplication explains the presence of two CO-like genes in temperate cereals, of which one (Hd1) is retained in rice, and explains many differences in gene family structure between grasses and Arabidopsis. The conserved fine structure of duplications shows that they largely evolved to their present structure before the divergence of the rice and Brachypodium. Of four flowering-time genes found in rice but absent in Arabidopsis, two were found in Bd21 (Id1, OsMADS51) and two were absent (Ghd7, Ehd1). Overall, results suggest that an ancient core photoperiod pathway promoting flowering via the induction of FT has been modified by the recruitment of additional lineage specific pathways that promote or repress FT expression.
Plants monitor environmental factors, such as temperature and day length, and also endogenous factors, such as their age and phytohormones, to decide when to flower. These cues are utilized to control expression levels of genes required for flowering. Thus, flowering time control is a unique model for understanding how gene activity is precisely regulated at the transcriptional level. In Arabidopsis, a remarkable number of non-coding RNA molecules have been identified by advanced sequencing technology. Recent progress in the flowering field has revealed several non-coding RNAs that play a major role in determining flowering time. Here, we introduce how two types of non-coding RNA species, microRNA (miRNA) and long noncoding RNA (lncRNA), contribute to flowering via regulation of target gene activity involved in this vital developmental transition.
Arabidopsis thaliana; Flowering; Long noncoding RNA (lncRNA); MicroRNA (miRNA); Reproductive competency; Vernalization
Plants must precisely time flowering to capitalize on favorable conditions. Although we know a great deal about the genetic basis of flowering phenology in model species under controlled conditions, the genetic architecture of this ecologically-important trait is poorly understood in non-model organisms. Here, we evaluated the transition from vegetative growth to flowering in Boechera stricta, a perennial relative of Arabidopsis thaliana. We examined flowering time QTLs using 7,920 recombinant inbred individuals, across seven lab and field environments differing in vernalization, temperature, and photoperiod. Genetic and environmental factors strongly influenced the transition to reproduction. We found directional selection for earlier flowering in the field. In the growth chamber experiment, longer winters accelerated flowering, whereas elevated ambient temperatures delayed flowering. Our analyses identified one large effect QTL (nFT), which influenced flowering time in both experiments and the probability of flowering in the field. In Montana, homozygotes for the native allele at nFT showed a selective advantage of 6.6%. Nevertheless, we found relatively low correlations between flowering times in the field and the growth chambers. Additionally, we detected flowering-related QTLs in the field which were absent across the full range of laboratory conditions, thus emphasizing the need to conduct experiments in natural environments.
developmental stage at flowering; field-lab comparison; photoperiod; quantitative trait loci; transition to flowering; vernalization
Background and Aims
Reproductive phase change in Arabidopsis thaliana is characterized by two transitions in phytomer identity, the differentiation of the first elongate internode (bolting transition) and of the first flower (floral transition). An evaluation of the dynamics of these transitions was sought by examining the precision of the corresponding phytomer identity changes.
The length of the first elongate internode and the frequency of chimeric inflorescence structures, e.g. paraclades not subtended by a leaf (no-leaf/paraclades) and flowers subtended by a bract (bract/flowers), were measured in the Wassilewskija (Ws) accession and 47 early flowering mutants under a wide range of photoperiods. The impact of photoperiodic perturbations applied to Ws plants at different times of development was also evaluated.
In Ws, both types of characters were remarkably constant across photoperiods in spite of a high degree of interindividual variability. Bract/flowers were not normally produced in Ws, but they were observed in conditions that suggest enhanced light signalling, e.g. in response to continuous light perturbations and in mutants with reduced hypocotyl elongation. In contrast, no-leaf/paraclades were normally present in approx. 20 % of Ws plants, and their frequency was increased in conditions that suggest reduced light signalling, e.g. in mutants with altered specification of long-day responses. The length of the first elongate internode was unrelated to the rate of stem elongation and to the regulation of reproductive phase change.
Bract/flowers and no-leaf/paraclades corresponded to opposite effects on the floral transition that reflected different dynamics of progression to flowering. In contrast, the length of the first elongate internode was only indirectly related to the regulation of reproductive phase change and was mainly dependent on global morphogenetic constraints. This paper proposes that morphogenetic variability could be used to identify critical phases of development and characterize the canalization of developmental patterns.
Arabidopsis; bolting; early flowering mutants; flowering time; internode patterning; phase change; photoperiod; phytomer identity
In plants, flowering is a critical developmental transition orchestrated by four regulatory pathways. Distinct alleles encoding mutant forms of the Arabidopsis potential calcium sensor CML24 cause alterations in flowering time. CML24 can act as a switch in the response to day length perception; loss-of-function cml24 mutants are late flowering under long days, whereas apparent gain of CML24 function results in early flowering. CML24 function is required for proper CONSTANS (CO) expression; components upstream of CO in the photoperiod pathway are largely unaffected in the cml24 mutants. In conjunction with CML23, a related calmodulin-like protein, CML24 also inhibits FLOWERING LOCUS C (FLC) expression and therefore impacts the autonomous regulatory pathway of the transition to flowering. Nitric oxide (NO) levels are elevated in cml23/cml24 double mutants and are largely responsible for FLC transcript accumulation. Therefore, CML23 and CML24 are potential calcium sensors that have partially overlapping function that may act to transduce calcium signals to regulate NO accumulation. In turn, NO levels influence the transition to flowering through both the photoperiod and autonomous regulatory pathways.
calcium; nitric oxide; calmodulin; cell signaling; flowering
Summary of recent advances
Plants utilize circadian clocks to synchronize their physiological and developmental events with daily and yearly changes in the environment. Recent advances in Arabidopsis research have provided a better understanding of the molecular mechanisms of the circadian clock and photoperiodism. One of the most important questions is whether the mechanisms studied in Arabidopsis are conserved in other plants. Homologs of many Arabidopsis clock genes have been identified in various plants and some gene functions have been characterized. It seems that the circadian clocks in plants are similar. Recent success in molecular genetics has also revealed the mechanisms of photoperiodic flowering in cereals. The day-length sensing mechanisms appear to have diverged more between long-day plants and short-day plants than the circadian clock.
Age-related resistance (ARR) is a plant defense response characterized by enhanced resistance to certain pathogens in mature plants relative to young plants. In Arabidopsis thaliana the transition to flowering is associated with ARR competence, suggesting that this developmental event is the switch that initiates ARR competence in mature plants (Rusterucci et al. in Physiol Mol Plant Pathol 66:222–231, 2005). The association of ARR and the floral transition was examined using flowering-time mutants and photoperiod-induced flowering to separate flowering from other developmental events that occur as plants age. Under short-day conditions, late-flowering plant lines ld-1 (luminidependens-1), soc1-2 (suppressor of overexpression of co 1-2), and FRI+ (FRIGIDA) displayed ARR before the transition to flowering occurred. Early-flowering svp-31, svp-32 (short vegetative phase), and Ws-2 were ARR-defective, whereas early-flowering tfl1-14 (terminal flower 1-14) displayed ARR at the same time as Col-0. While svp-31, svp-32 and Ws-2 produced few rosette leaves, tfl1-14 produced a rosette leaf number similar to Col-0, suggesting that the development of a minimum number of rosette leaves is necessary to initiate ARR competence under short-day conditions. Photoperiod-induced transient expression of FT (FLOWERING LOCUS T) caused precocious flowering in short-day-grown Col-0 but this was not associated with ARR competence. Under long-day conditions co-9 (constans-9) mutants did not flower but displayed an ARR response at the same time as Col-0. This study suggests that SVP is required for the ARR response and that the floral transition is not the developmental event that regulates ARR competence.
Electronic supplementary material
The online version of this article (doi:10.1007/s11103-013-0083-7) contains supplementary material, which is available to authorized users.
Arabidopsis; Pseudomonas syringae; Age-related resistance; Developmental resistance; Flowering; Photoperiod
Higher plants use multiple perceptive measures to coordinate flowering time with environmental and endogenous cues. Physiological studies show that florigen is a mobile factor that transmits floral inductive signals from the leaf to the shoot apex. Arabidopsis FT protein is widely regarded as the archetype florigen found in diverse plant species, particularly in plants that use inductive photoperiods to flower. Recently, a large family of FT homologues in maize, the Zea CENTRORADIALIS (ZCN) genes, was described, suggesting that maize also contains FT-related proteins that act as a florigen. The product of one member of this large family, ZCN8, has several attributes that make it a good candidate as a maize florigen. Mechanisms underlying the floral transition in maize are less well understood than those of other species, partly because flowering in temperate maize is dependent largely on endogenous signals. The maize indeterminate1 (id1) gene is an important regulator of maize autonomous flowering that acts in leaves to mediate the transmission or production of florigenic signals. This study finds that id1 acts upstream of ZCN8 to control its expression, suggesting a possible new link to flowering in day-neutral maize. Moreover, in teosinte, a tropical progenitor of maize that requires short-day photoperiods to induce flowering, ZCN8 is highly up-regulated in leaves under inductive photoperiods. Finally, vascular-specific expression of ZCN8 in Arabidopsis complements the ft-1 mutation, demonstrating that leaf-specific expression of ZCN8 can induce flowering. These results suggest that ZCN8 may encode a florigen that integrates both endogenous and environmental signals in maize.
florigen; FT orthologue; long-distance signalling; maize; photoperiod induction; teosinte; transcription factor
CONSTANS (CO) is an important flowering-time gene in the photoperiodic flowering pathway of annual Arabidopsis thaliana in which overexpression of CO induces early flowering, whereas mutations in CO cause delayed flowering. The closest homologs of CO in woody perennial poplar (Populus spp.) are CO1 and CO2. A previous report  showed that the CO2/FLOWERING LOCUS T1 (FT1) regulon controls the onset of reproduction in poplar, similar to what is seen with the CO/FLOWERING LOCUS T (FT) regulon in Arabidopsis. The CO2/FT1 regulon was also reported to control fall bud set. Our long-term field observations show that overexpression of CO1 and CO2 individually or together did not alter normal reproductive onset, spring bud break, or fall dormancy in poplar, but did result in smaller trees when compared with controls. Transcripts of CO1 and CO2 were normally most abundant in the growing season and rhythmic within a day, peaking at dawn. Our manipulative experiments did not provide evidence for transcriptional regulation being affected by photoperiod, light intensity, temperature, or water stress when transcripts of CO1 and CO2 were consistently measured in the morning. A genetic network analysis using overexpressing trees, microarrays, and computation demonstrated that a majority of functionally known genes downstream of CO1 and CO2 are associated with metabolic processes, which could explain their effect on tree size. In conclusion, the function of CO1 and CO2 in poplar does not appear to overlap with that of CO from Arabidopsis, nor do our data support the involvement of CO1 and CO2 in spring bud break or fall bud set.
The onset of flowering is an important adaptive trait in plants. The small ephemeral species Arabidopsis thaliana grows under a wide range of temperature and day-length conditions across much of the Northern hemisphere, and a number of flowering-time loci that vary between different accessions have been identified before. However, only few studies have addressed the species-wide genetic architecture of flowering-time control. We have taken advantage of a set of 18 distinct accessions that present much of the common genetic diversity of A. thaliana and mapped quantitative trait loci (QTL) for flowering time in 17 F2 populations derived from these parents. We found that the majority of flowering-time QTL cluster in as few as five genomic regions, which include the locations of the entire FLC/MAF clade of transcription factor genes. By comparing effects across shared parents, we conclude that in several cases there might be an allelic series caused by rare alleles. While this finding parallels results obtained for maize, in contrast to maize much of the variation in flowering time in A. thaliana appears to be due to large-effect alleles.
Plants use day-length information to coordinate flowering time with the appropriate season to maximize reproduction. In Arabidopsis, the long-day specific expression of CONSTANS (CO) protein is crucial for flowering induction. Although light signaling regulates CO protein stability, the mechanism by which CO is stabilized in the long-day afternoon has remained elusive. Here we demonstrate that FLAVIN-BINDING, KELCH REPEAT, F-BOX 1 (FKF1) protein stabilizes CO protein in the afternoon in long days. FKF1 interacts with CO through its LOV domain, and blue light enhances this interaction. In addition, FKF1 simultaneously removes CYCLING DOF FACTOR 1 (CDF1) that represses CO and FLOWERING LOCUS T (FT) transcription. Together with CO transcriptional regulation, FKF1 protein controls robust FT mRNA induction through multiple feedforward mechanisms that accurately control flowering timing.
The endogenous circadian clock regulates many physiological processes related to plant survival and adaptability. GIGANTEA (GI), a clock-associated protein, contributes to the maintenance of circadian period length and amplitude, and also regulates flowering time and hypocotyl growth in response to day length. Similarly, EARLY FLOWERING 4 (ELF4), another clock regulator, also contributes to these processes. However, little is known about either the genetic or molecular interactions between GI and ELF4 in Arabidopsis. In this study, we investigated the genetic interactions between GI and ELF4 in the regulation of circadian clock-controlled outputs. Our mutant analysis shows that GI is epistatic to ELF4 in flowering time determination, while ELF4 is epistatic to GI in hypocotyl growth regulation. Moreover, GI and ELF4 have a synergistic or additive effect on endogenous clock regulation. Gene expression profiling of gi, elf4, and gi elf4 mutants further established that GI and ELF4 have differentially dominant influences on circadian physiological outputs at dusk and dawn, respectively. This phasing of GI and ELF4 influences provides a potential means to achieve diversity in the regulation of circadian physiological outputs, including flowering time and hypocotyl growth.
microarray; LHY; endogenous clock; GI; ELF4
Plants monitor changes in day length to coordinate flowering with favorable seasons to increase their fitness. The day-length specific induction of FLOWERING LOCUS T (FT) regulated by CONSTANS (CO) is the crucial aspect of photoperiodic flowering in Arabidopsis thaliana. Recent studies elucidated some mechanisms of CO-dependent FT induction. Here, we demonstrate another mechanism of CO-dependent FT regulation. Our results indicate that CO protein regulates FT transcription partially by forming a complex with ASYMMETRIC LEAVES 1 (AS1) protein, which regulates leaf development partly by controlling gibberellin (GA) levels. We identified AS1 as a CO-interacting protein in yeast and verified their interaction in vitro and in planta. We also showed that the AS1 temporal and spatial expression pattern overlapped with that of CO. In addition, as1 mutants showed GA-independent delayed flowering under different light/dark conditions. FT expression levels in the as1 mutants and the SUC2:CO-HA/as1 line under long-day and 12-h light/12-h dark conditions were reduced compared to wild-type plants and the SUC2:HA-CO line, respectively. Moreover, AS1 directly bound to the specific regions of the FT promoter in vivo. These results indicate that CO forms a functional complex with AS1 to regulate FT expression and that AS1 plays different roles in two regulatory pathways, both of which concomitantly regulate a precise timing of flowering.
Arabidopsis; ASYMMETRIC LEAVES1 (AS1); CONSTANS (CO); FLOWERING LOCUS T (FT); Flowering time; Photoperiodic pathway
Background and Aims
Plant aerial development is well known to be affected by day length in terms of the timing and developmental stage of floral transition. Arabidopsis thaliana is a ‘long day’ plant in which the time to flower is delayed by short days and leaf number is increased. The aim of the work presented here was to determine the effects of different day lengths on individual leaf area expansion. The effect of flower emergence per se on the regulation of leaf expansion was also tested in this study.
Care was taken to ensure that day length was the only source of micro-meteorological variation. The dynamics of individual leaf expansion were analysed in Ler and Col-0 plants grown under five day lengths in five independent experiments. Responses at cellular level were analysed in Ler plants grown under various day lengths and treatments to alter the onset of flowering.
When the same leaf position was compared, the final leaf area and both the relative and absolute rates of leaf expansion were decreased by short days, whereas the duration of leaf expansion was increased. Epidermal cell number and cell area were also altered by day-length treatments and some of these responses could be mimicked by manipulating the date of flowering.
Both the dynamics and cellular bases of leaf development are altered by differences in day length even when visible phenotypes are absent. To some extent, cell area and its response to day length are controlled by whole plant control mechanisms associated with the onset of flowering.
Arabidopsis thaliana; day length; leaf expansion rate; duration of expansion; cell division; flowering
Flowering is a critical transition in plant development, the timing of which can have considerable fitness consequences. Until recently, research into the genetic control of flowering time and its associated developmental changes was focused on core eudicots (for example, Arabidopsis) or monocots (for example, Oryza). Here we examine the flowering response of Aquilegia formosa, a member of the eudicot order Ranunculales that is emerging as an important model for the investigation of plant ecology and evolution.
We have determined that A. formosa has a strong vernalization requirement but little or no photoperiod response, making it a day neutral (DN) plant. Consistent with this, the Aquilegia homolog of FLOWERING LOCUS T (AqFT) is expressed in both long and short days but surprisingly, the locus is expressed before the transition to flowering. In situ hybridizations with homologs of several Arabidopsis Floral Pathway Integrators (FPIs) do not suggest conserved functions relative to Arabidopsis, the potential exceptions being AqLFY and AqAGL24.2.
In Aquilegia, vernalization is critical to flowering but this signal is not strictly required for the transcriptional activation of AqFT. The expression patterns of AqLFY and AqAGL24.2 suggest a hypothesis for the development of Aquilegia's determinate inflorescence whereby their differential expression controls the progression of each meristem from inflorescence to floral identity. Interestingly, none of the Aquilegia expression patterns are consistent with a function in floral repression which, combined with the lack of a FLC homolog, means that new candidate genes must be identified for the control of vernalization response in Aquilegia.