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1.  Photoperiodic Regulation of Flowering Time through Periodic Histone Deacetylation of the Florigen Gene FT 
PLoS Biology  2013;11(9):e1001649.
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.
Author Summary
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.
doi:10.1371/journal.pbio.1001649
PMCID: PMC3760768  PMID: 24019760
2.  Quantitative analysis of regulatory flexibility under changing environmental conditions 
Day length changes with the seasons in temperate latitudes, affecting the many biological rhythms that entrain to the day/night cycle: we measure these effects on the expression of Arabidopsis clock genes, using RNA and reporter gene readouts, with a new method of phase analysis.Dusk sensitivity is proposed as a simple, natural and general mathematical measure to analyse and manipulate the changing phase of a clock output relative to the change in the day/night cycle.Dusk sensitivity shows how increasing the numbers of feedback loops in the Arabidopsis clock models allows more flexible regulation, consistent with a previously-proposed, general operating principle of biological networks.The Arabidopsis clock genes show flexibility of regulation that is characteristic of a three-loop clock model, validating aspects of the model and the operating principle, but some clock output genes show greater flexibility arising from direct light regulation.
The analysis of dynamic, non-linear regulation with the aid of mechanistic models is central to Systems Biology. This study compares the predictions of mechanistic, mathematical models of the circadian clock with molecular time-series data on rhythmic gene expression in the higher plant Arabidopsis thaliana. Analysis of the models helps us to understand (explain and predict) how the clock gene circuit balances regulation by external and endogenous factors to achieve particular behaviours. Such multi-factorial regulation is ubiquitous in, and characteristic of, living systems.
The Earth's rotation causes predictable changes in the environment, notably in the availability of sunlight for photosynthesis. Many biological processes are driven by the environmental input via sensory pathways, for example, from photoreceptors. Circadian clocks provide an alternative strategy. These endogenous, 24-h rhythms can drive biological processes that anticipate the regular environmental changes, rather than merely responding. Many rhythmic processes have both light and clock control. Indeed, the clock components themselves must balance internal timing with external inputs, because circadian clocks are reset daily through light regulation of one or more clock components. This process of entrainment is complicated by the change in day length. When the times of dawn and dusk move apart in summer, and closer together in winter, does the clock track dawn, track dusk or interpolate between them?
In plants, the clock controls leaf and petal movements, the opening and closing of stomatal pores, the discharge of floral fragrances, and many metabolic activities, especially those associated with photosynthesis. Centuries of physiological studies have shown that these rhythms can behave differently. Flowering in Ipomoea nil (Pharbitis nil, Japanese morning glory) is controlled by a rhythm that tracks the time of dusk, to give a classic example. We showed that two other rhythms associated with vegetative growth track dawn in this species (Figure 5A), so the clock system allows flexible regulation.
The relatively small number of components involved in the circadian clockwork makes it an ideal candidate for mathematical modelling. Molecular genetic studies in a variety of model eukaryotes have shown that the circadian rhythm is generated by a network of 6–20 genes. These genes form feedback loops generating a rhythm in mRNA production. A single negative feedback loop in which a gene encodes a protein that, after several hours, turns off transcription is capable of generating a circadian rhythm, in principle. A single light input can entrain the clock to ‘local time', synchronised with a light–dark cycle. However, real circadian clocks have proven to be more complicated than this, with multiple light inputs and interlocked feedback loops.
We have previously argued from mathematical analysis that multi-loop networks increase the flexibility of regulation (Rand et al, 2004) and have shown that appropriately deployed flexibility can confer functional robustness (Akman et al, 2010). Here we test whether that flexibility can be demonstrated in vivo, in the model plant, A. thaliana. The Arabidopsis clock mechanism comprises a feedback loop in which two partially redundant, myb transcription factors, LATE ELONGATED HYPOCOTYL (LHY) and CIRCADIAN CLOCK ASSOCIATED 1 (CCA1), repress the expression of their activator, TIMING OF CAB EXPRESSION 1 (TOC1). We previously modelled this single-loop circuit and showed that it was not capable of recreating important data (Locke et al, 2005a). An extended, two-loop model was developed to match observed behaviours, incorporating a hypothetical gene Y, for which the best identified candidate was the GIGANTEA gene (GI) (Locke et al, 2005b). Two further models incorporated the TOC1 homologues PSEUDO-RESPONSE REGULATOR (PRR) 9 and PRR7 (Locke et al, 2006; Zeilinger et al, 2006). In these circuits, a morning oscillator (LHY/CCA1–PRR9/7) is coupled to an evening oscillator (Y/GI–TOC1) via the original LHY/CCA1–TOC1 loop.
These clock models, like those for all other organisms, were developed using data from simple conditions of constant light, darkness or 12-h light–12-h dark cycles. We therefore tested how the clock genes in Arabidopsis responded to light–dark cycles with different photoperiods, from 3 h light to 18 h light per 24-h cycle (Edinburgh, 56° North latitude, has 17.5 h light in midsummer). The time-series assays of mRNA and in vivo reporter gene images showed a range of peak times for different genes, depending on the photoperiod (Figure 5C). A new data analysis method, mFourfit, was introduced to measure the peak times, in the Biological Rhythms Analysis Software Suite (BRASS v3.0). None of the genes showed the dusk-tracking behaviour characteristic of the Ipomoea flowering rhythm. The one-, two- and three-loop models were analysed to understand the observed patterns. A new mathematical measure, dusk sensitivity, was introduced to measure the change in timing of a model component versus a change in the time of dusk. The one- and two-loop models tracked dawn and dusk, respectively, under all conditions. Only the three-loop model (Figure 5B) had the flexibility required to match the photoperiod-dependent changes that we found in vivo, and in particular the unexpected, V-shaped pattern in the peak time of TOC1 expression. This pattern of regulation depends on the structure and light inputs to the model's evening oscillator, so the in vivo data supported this aspect of the model. LHY and CCA1 gene expression under short photoperiods showed greater dusk sensitivity, in the interval 2–6 h before dawn, than the three-loop model predicted, so these data will help to constrain future models.
The approach described here could act as a template for experimental biologists seeking to understand biological regulation using dynamic, experimental perturbations and time-series data. Simulation of mathematical models (despite known imperfections) can provide contrasting hypotheses that guide understanding. The system's detailed behaviour is complex, so a natural and general measure such as dusk sensitivity is helpful to focus on one property of the system. We used the measure to compare models, and to predict how this property could be manipulated. To enable additional analysis of this system, we provide the time-series data and experimental metadata online.
The circadian clock controls 24-h rhythms in many biological processes, allowing appropriate timing of biological rhythms relative to dawn and dusk. Known clock circuits include multiple, interlocked feedback loops. Theory suggested that multiple loops contribute the flexibility for molecular rhythms to track multiple phases of the external cycle. Clear dawn- and dusk-tracking rhythms illustrate the flexibility of timing in Ipomoea nil. Molecular clock components in Arabidopsis thaliana showed complex, photoperiod-dependent regulation, which was analysed by comparison with three contrasting models. A simple, quantitative measure, Dusk Sensitivity, was introduced to compare the behaviour of clock models with varying loop complexity. Evening-expressed clock genes showed photoperiod-dependent dusk sensitivity, as predicted by the three-loop model, whereas the one- and two-loop models tracked dawn and dusk, respectively. Output genes for starch degradation achieved dusk-tracking expression through light regulation, rather than a dusk-tracking rhythm. Model analysis predicted which biochemical processes could be manipulated to extend dusk tracking. Our results reveal how an operating principle of biological regulators applies specifically to the plant circadian clock.
doi:10.1038/msb.2010.81
PMCID: PMC3010117  PMID: 21045818
Arabidopsis thaliana; biological clocks; dynamical systems; gene regulatory networks; mathematical models; photoperiodism
3.  FTIP1 Is an Essential Regulator Required for Florigen Transport 
PLoS Biology  2012;10(4):e1001313.
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.
Author Summary
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.
doi:10.1371/journal.pbio.1001313
PMCID: PMC3328448  PMID: 22529749
4.  Photoperiodic flowering regulation in Arabidopsis thaliana 
Photoperiod, or the duration of light in a given day, is a critical cue that flowering plants utilize to effectively assess seasonal information and coordinate their reproductive development in synchrony with the external environment. The use of the model plant, Arabidopsis thaliana, has greatly improved our understanding of the molecular mechanisms that determine how plants process and utilize photoperiodic information to coordinate a flowering response. This mechanism is typified by the transcriptional activation of FLOWERING LOCUS T (FT) gene by the transcription factor CONSTANS (CO) under inductive long-day conditions in Arabidopsis. FT protein then moves from the leaves to the shoot apex, where floral meristem development can be initiated. As a point of integration from a variety of environmental factors in the context of a larger system of regulatory pathways that affect flowering, the importance of photoreceptors and the circadian clock in CO regulation throughout the day has been a key feature of the photoperiodic flowering pathway. In addition to these established mechanisms, the recent discovery of a photosynthate derivative trehalose-6-phosphate as an activator of FT in leaves has interesting implications for the involvement of photosynthesis in the photoperiodic flowering response that were suggested from previous physiological experiments in flowering induction.
doi:10.1016/B978-0-12-417162-6.00001-8
PMCID: PMC4326075
Photoperiodism; Flowering; Phenology; Circadian Clock; Florigen
5.  Regulation of Arabidopsis Flowering by the Histone Mark Readers MRG1/2 via Interaction with CONSTANS to Modulate FT Expression 
PLoS Genetics  2014;10(9):e1004617.
Day-length is important for regulating the transition to reproductive development (flowering) in plants. In the model plant Arabidopsis thaliana, the transcription factor CONSTANS (CO) promotes expression of the florigen FLOWERING LOCUS T (FT), constituting a key flowering pathway under long-day photoperiods. Recent studies have revealed that FT expression is regulated by changes of histone modification marks of the FT chromatin, but the epigenetic regulators that directly interact with the CO protein have not been identified. Here, we show that the Arabidopsis Morf Related Gene (MRG) group proteins MRG1 and MRG2 act as H3K4me3/H3K36me3 readers and physically interact with CO to activate FT expression. In vitro binding analyses indicated that the chromodomains of MRG1 and MRG2 preferentially bind H3K4me3/H3K36me3 peptides. The mrg1 mrg2 double mutant exhibits reduced mRNA levels of FT, but not of CO, and shows a late-flowering phenotype under the long-day but not short-day photoperiod growth conditions. MRG2 associates with the chromatin of FT promoter in a way dependent of both CO and H3K4me3/H3K36me3. Vice versa, loss of MRG1 and MRG2 also impairs CO binding at the FT promoter. Crystal structure analyses of MRG2 bound with H3K4me3/H3K36me3 peptides together with mutagenesis analysis in planta further demonstrated that MRG2 function relies on its H3K4me3/H3K36me3-binding activity. Collectively, our results unravel a novel chromatin regulatory mechanism, linking functions of MRG1 and MRG2 proteins, H3K4/H3K36 methylations, and CO in FT activation in the photoperiodic regulation of flowering time in plants.
Author Summary
The photoperiodic flowering in Arabidopsis requires the key regulator CO and its target gene FT. However, how CO regulates FT expression in the context of chromatin remains largely obscure. In this work, we present Arabidopsis MRG1/2 as novel chromatin effectors directly involved in the CO-FT photoperiodic flowering. Firstly, MRG1/2 proteins are identified as recognition factors of H3K4 and H3K36 methylation via their chromodomains. The mrg1 mrg2 double mutant shows a late-flowering phenotype only under long-day conditions through down-regulation of FT but not of CO. MRG2 can directly target in vivo the FT promoter chromatin in a H3K4me3/H3K36me3-level dependent manner. More importantly, MRG2 and CO physically interact and enhance each other's binding to the FT promoter in planta. Determination of co-crystal structures of MRG2 with H3K4me3/H3K36me3 peptides and mutagenesis of a key amino acid residue involved in structural interaction demonstrate that MRG2 reader activity is essential for in planta function. Taken together, our findings uncover a novel mechanism of FT activation in flowering promotion and provide a striking example of mutual interplay between a transcription factor and a histone methylation reader in transcription regulation.
doi:10.1371/journal.pgen.1004617
PMCID: PMC4161306  PMID: 25211338
6.  Diversity of Flowering Responses in Wild Arabidopsis thaliana Strains 
PLoS Genetics  2005;1(1):e6.
Although multiple environmental cues regulate the transition to flowering in Arabidopsis thaliana, previous studies have suggested that wild A. thaliana accessions fall primarily into two classes, distinguished by their requirement for vernalization (extended winter-like temperatures), which enables rapid flowering under long days. Much of the difference in vernalization response is apparently due to variation at two epistatically acting loci, FRI and FLC. We present the response of over 150 wild accessions to three different environmental variables. In long days, FLC is among those genes whose expression is most highly correlated with flowering. In short days, FRI and FLC are less important, although their contribution is still significant. In addition, there is considerable variation not only in vernalization response, but also in the response to differences in day length or ambient growth temperature. The identification of accessions that flower relatively early or late in specific environments suggests that many of the flowering-time pathways identified by mutagenesis, such as those that respond to day length, contribute to flowering-time variation in the wild. In contrast to differences in vernalization requirement, which are mainly mediated by FRI and FLC, it seems that variation in these other pathways is due to allelic effects at several different loci.
Synopsis
Flowering is a quintessential adaptive trait in plants: Its correct timing ensures, for example, that plants do not produce seeds when they will not find favorable conditions for dispersal or germination. Befitting its importance, flowering is affected by several different environmental variables. The authors have compared the flowering times of over 150 Arabidopsis thaliana wild strains in response to three environmental factors: ambient growth temperature, day length, and vernalization (extended winter-like temperatures). Genetic and molecular analyses confirmed the important role of the previously identified FRI and FLC genes in flowering time. Genome-wide expression studies showed that FLC is among the genes whose expression is most highly correlated with flowering. Their studies, however, also revealed that the impact of FRI and FLC depends not only on vernalization treatment, which leads to repression of FRI and FLC activity, but also on day length. Within the groups of relatively early- and late-flowering strains, they find several unique responses, suggesting that many of the signaling pathways identified in mutant studies of laboratory strains are also being used to generate flowering diversity in the wild.
doi:10.1371/journal.pgen.0010006
PMCID: PMC1183525  PMID: 16103920
7.  PEP1 of Arabis alpina Is Encoded by Two Overlapping Genes That Contribute to Natural Genetic Variation in Perennial Flowering 
PLoS Genetics  2012;8(12):e1003130.
Higher plants exhibit a variety of different life histories. Annual plants live for less than a year and after flowering produce seeds and senesce. By contrast perennials live for many years, dividing their life cycle into episodes of vegetative growth and flowering. Environmental cues control key check points in both life histories. Genes controlling responses to these cues exhibit natural genetic variation that has been studied most in short-lived annuals. We characterize natural genetic variation conferring differences in the perennial life cycle of Arabis alpina. Previously the accession Pajares was shown to flower after prolonged exposure to cold (vernalization) and only for a limited period before returning to vegetative growth. We describe five accessions of A. alpina that do not require vernalization to flower and flower continuously. Genetic complementation showed that these accessions carry mutant alleles at PERPETUAL FLOWERING 1 (PEP1), which encodes a MADS box transcription factor orthologous to FLOWERING LOCUS C in the annual Arabidopsis thaliana. Each accession carries a different mutation at PEP1, suggesting that such variation has arisen independently many times. Characterization of these alleles demonstrated that in most accessions, including Pajares, the PEP1 locus contains a tandem arrangement of a full length and a partial PEP1 copy, which give rise to two full-length transcripts that are differentially expressed. This complexity contrasts with the single gene present in A. thaliana and might contribute to the more complex expression pattern of PEP1 that is associated with the perennial life-cycle. Our work demonstrates that natural accessions of A. alpina exhibit distinct life histories conferred by differences in PEP1 activity, and that continuous flowering forms have arisen multiple times by inactivation of the floral repressor PEP1. Similar phenotypic variation is found in other herbaceous perennial species, and our results provide a paradigm for how characteristic perennial phenotypes might arise.
Author Summary
Perennial plants live for many years and cycle between flowering and vegetative growth. These stages of the life cycle are often initiated by environmental conditions and occur seasonally. However, many herbaceous perennial species such as strawberry, rose, or Arabis alpina contain varieties that flower continuously irrespective of the seasons. Here we characterize this genetic variation in A. alpina and show that five continuously flowering accessions carry independent mutations in the PERPETUAL FLOWERING 1 (PEP1) gene. These mutations impair the activity of the PEP1 floral repressor causing the plants to flower without requirement for winter cold and to flower continuously. This result has interesting parallels with strawberry and rose, where inactivation of a different floral repressor controlling response to day length gives rise to naturally occurring perpetual flowering forms. We also show that PEP1 in A. alpina has a complex duplicated structure that gives rise to two overlapping transcripts. This arrangement differs from the simple structure of PEP1 orthologues in related annual species, such as FLC of Arabidopsis thaliana, suggesting that duplication of PEP1 might contribute to the complex transcriptional patterns associated with PEP1 function in perennials. Our work provides insight into genetic variation contributing to the perennial life history of plants.
doi:10.1371/journal.pgen.1003130
PMCID: PMC3527215  PMID: 23284298
8.  Arabidopsis FLC clade members form flowering-repressor complexes coordinating responses to endogenous and environmental cues 
Nature Communications  2013;4:1947.
The developmental transition to flowering is timed by endogenous and environmental signals through multiple genetic pathways. In Arabidopsis, the MADS-domain protein FLOWERING LOCUS C is a potent flowering repressor. Here, we report that the FLOWERING LOCUS C clade member MADS AFFECTING FLOWERING3 acts redundantly with another clade member to directly repress expression of the florigen FLOWERING LOCUS T and inhibit flowering. FLOWERING LOCUS C clade members act in partial redundancy in floral repression and mediate flowering responses to temperature, in addition to their participation in the flowering-time regulation by vernalization and photoperiod. We show that FLOWERING LOCUS C, MADS AFFECTING FLOWERING3 and three other clade members can directly interact with each other and form nuclear complexes, and that FLOWERING LOCUS C-dependent floral repression requires other clade members. Our results collectively suggest that the FLOWERING LOCUS C clade members act as part of several MADS-domain complexes with partial redundancy, which integrate responses to endogenous and environmental cues to control flowering.
Flowering time is a critical developmental transition for a plant’s reproductive success and it depends on endogenous and environmental signals. Here Gu et al. show that MADS-domain floral repressors form protein complexes that coordinate Arabidopsis responses to these cues and regulate its flowering time.
doi:10.1038/ncomms2947
PMCID: PMC3709509  PMID: 23770815
9.  SRR1 is essential to repress flowering in non-inductive conditions in Arabidopsis thaliana  
Journal of Experimental Botany  2014;65(20):5811-5822.
Summary
SRR1 regulates flowering time in Arabidopsis by integrating photoperiodic and photoperiod-independent signals. By promoting expression of several repressors of FT, SRR1 represses flowering in non-inductive conditions.
Timing of flowering is determined by environmental and developmental signals, leading to promotion or repression of key floral integrators. SENSITIVITY TO RED LIGHT REDUCED (SRR1) is a pioneer protein previously shown to be involved in regulation of the circadian clock and phytochrome B signalling in Arabidopsis thaliana. This report has examined the role of SRR1 in flowering time control. Loss-of-function srr1-1 plants flowered very early compared with the wild type under short-day conditions and had a weak flowering response to increasing daylength. Furthermore, FLOWERING LOCUS T (FT) transcript levels were elevated already in short days in srr1-1 compared with the wild type. This correlated with elevated end of day levels of CONSTANS (CO), whereas levels of CYCLING DOF FACTOR 1 (CDF1), a repressor of CO transcription, were reduced. srr1-1 gi-2 and srr1-1 co-9 double mutants showed that SRR1 can also repress flowering independently of the photoperiodic pathway. srr1-1 flowered consistently early between 16 °C and 27 °C, showing that SRR1 prevents premature flowering over a wide temperature range. SRR1 also promotes expression of the repressors TEMPRANILLO 1 (TEM1) and TEM2. Consequently their targets in the gibberellin biosynthesis pathway were elevated in srr1-1. SRR1 is thus an important focal point of both photoperiodic and photoperiod-independent regulation of flowering. By stimulating expression of the FT-binding repressors CDF1, TEM1 and TEM2, and FLC, flowering is inhibited in non-inductive conditions.
doi:10.1093/jxb/eru317
PMCID: PMC4203120  PMID: 25129129
Arabidopsis; circadian clock; flowering time control; photoperiod; repressors; SRR1.
10.  Potent Induction of Arabidopsis thaliana Flowering by Elevated Growth Temperature 
PLoS Genetics  2006;2(7):e106.
The transition to flowering is an important event in the plant life cycle and is modulated by several environmental factors including photoperiod, light quality, vernalization, and growth temperature, as well as biotic and abiotic stresses. In contrast to light and vernalization, little is known about the pathways that mediate the responses to other environmental variables. A mild increase in growth temperature, from 23 °C to 27 °C, is equally efficient in inducing flowering of Arabidopsis plants grown in 8-h short days as is transfer to 16-h long days. There is extensive natural variation in this response, and we identify strains with contrasting thermal reaction norms. Exploiting this natural variation, we show that FLOWERING LOCUS C potently suppresses thermal induction, and that the closely related floral repressor FLOWERING LOCUS M is a major-effect quantitative trait locus modulating thermosensitivity. Thermal induction does not require the photoperiod effector CONSTANS, acts upstream of the floral integrator FLOWERING LOCUS T, and depends on the hormone gibberellin. Analysis of mutants defective in salicylic acid biosynthesis suggests that thermal induction is independent of previously identified stress-signaling pathways. Microarray analyses confirm that the genomic responses to floral induction by photoperiod and temperature differ. Furthermore, we report that gene products that participate in RNA splicing are specifically affected by thermal induction. Above a critical threshold, even small changes in temperature can act as cues for the induction of flowering. This response has a genetic basis that is distinct from the known genetic pathways of floral transition, and appears to correlate with changes in RNA processing.
Synopsis
When to flower is an important decision in the life cycle of a plant, as it determines the plant's reproductive success. Not surprisingly, plants closely monitor the state of their life cycle along with the external environment in order to determine the onset of flowering. Several factors including light, temperature, and abiotic stress are known to affect the timing of flowering. The authors show that growth temperatures above a finely tuned threshold can rapidly trigger flowering, bypassing the need for other inductive stimuli such as day length. Exploiting a combination of Mendelian genetics, natural variation, and genomics, they show thermal induction of flowering to have a unique genetic basis. Genomic responses to temperature and light during floral induction differ, and temperature-specific changes include alterations in RNA processing.
doi:10.1371/journal.pgen.0020106
PMCID: PMC1487179  PMID: 16839183
11.  ZCN8 encodes a potential orthologue of Arabidopsis FT florigen that integrates both endogenous and photoperiod flowering signals in maize 
Journal of Experimental Botany  2011;62(14):4833-4842.
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.
doi:10.1093/jxb/err129
PMCID: PMC3192997  PMID: 21730358
florigen; FT orthologue; long-distance signalling; maize; photoperiod induction; teosinte; transcription factor
12.  The time of day effects of warm temperature on flowering time involve PIF4 and PIF5 
Journal of Experimental Botany  2014;65(4):1141-1151.
Warm temperature promotes flowering in Arabidopsis thaliana and this response involves multiple signalling pathways. To understand the temporal dynamics of temperature perception, tests were carried out to determine if there was a daily window of enhanced sensitivity to warm temperature (28 °C). Warm temperature applied during daytime, night-time, or continuously elicited earlier flowering, but the effects of each treatment were unequal. Plants exposed to warm night (WN) conditions flowered nearly as early as those in constant warm (CW) conditions, while treatment with warm days (WD) caused later flowering than either WN or CW. Flowering in each condition relied to varying degrees on the activity of CO , FT , PIF4 , and PIF5 , as well as the action of unknown genes. The combination of signalling pathways involved in flowering depended on the time of the temperature cue. WN treatments caused a significant advance in the rhythmic expression waveform of CO, which correlated with pronounced up-regulation of FT expression, while WD caused limited changes in CO expression and no stimulation of FT expression. WN- and WD-induced flowering was partially CO independent and, unexpectedly, dependent on PIF4 and PIF5 . pif4-2, pif5-3, and pif4-2 pif5-3 mutants had delayed flowering under all three warm conditions. The double mutant was also late flowering in control conditions. In addition, WN conditions alone imposed selective changes to PIF4 and PIF5 expression. Thus, the PIF4 and PIF5 transcription factors promote flowering by at least two means: inducing FT expression in WN and acting outside of FT by an unknown mechanism in WD.
Summary
The timing of warm temperature cues dictates the magnitude of the early flowering response in Arabidopsis thaliana and the contribution of CO, FT, PIF4, and PIF5 to promotion of flowering.
doi:10.1093/jxb/ert487
PMCID: PMC3935576  PMID: 24574484
Circadian clock; CONSTANS; flowering; FLOWERING LOCUS T; PHYTOCHROME INTERACTING FACTOR; PIF4; PIF5; temperature response.
13.  A Regulatory Network for Coordinated Flower Maturation 
PLoS Genetics  2012;8(2):e1002506.
For self-pollinating plants to reproduce, male and female organ development must be coordinated as flowers mature. The Arabidopsis transcription factors AUXIN RESPONSE FACTOR 6 (ARF6) and ARF8 regulate this complex process by promoting petal expansion, stamen filament elongation, anther dehiscence, and gynoecium maturation, thereby ensuring that pollen released from the anthers is deposited on the stigma of a receptive gynoecium. ARF6 and ARF8 induce jasmonate production, which in turn triggers expression of MYB21 and MYB24, encoding R2R3 MYB transcription factors that promote petal and stamen growth. To understand the dynamics of this flower maturation regulatory network, we have characterized morphological, chemical, and global gene expression phenotypes of arf, myb, and jasmonate pathway mutant flowers. We found that MYB21 and MYB24 promoted not only petal and stamen development but also gynoecium growth. As well as regulating reproductive competence, both the ARF and MYB factors promoted nectary development or function and volatile sesquiterpene production, which may attract insect pollinators and/or repel pathogens. Mutants lacking jasmonate synthesis or response had decreased MYB21 expression and stamen and petal growth at the stage when flowers normally open, but had increased MYB21 expression in petals of older flowers, resulting in renewed and persistent petal expansion at later stages. Both auxin response and jasmonate synthesis promoted positive feedbacks that may ensure rapid petal and stamen growth as flowers open. MYB21 also fed back negatively on expression of jasmonate biosynthesis pathway genes to decrease flower jasmonate level, which correlated with termination of growth after flowers have opened. These dynamic feedbacks may promote timely, coordinated, and transient growth of flower organs.
Author Summary
Perfect flowers have both male organs that produce and release pollen and female organs that make and harbor seeds. Flowers also often attract pollinators using visual or chemical signals. So that male, female, and pollinator attraction functions occur at the right time, flower organs must grow and mature in a coordinated fashion. In the model self-pollinating plant Arabidopsis, a transcriptional network regulates genes that ensure coordinated growth of different flower organs, as well as pollen release and gynoecium (female) competence to support pollination. This network also regulates nectary development and production of volatile chemicals that may attract or repel insects. We have studied growth, chemical signal levels, and gene expression in mutants affected in components of this network, in order to determine how flower growth is controlled. Several plant hormones act in a cascade that promotes flower maturation. Moreover, regulatory feedback loops affect the timing and extent of developmental steps. Positive feedbacks may ensure that the development of different flower organs is coordinated and rapid, whereas negative feedbacks may allow growth to cease once flowers have opened. Our results provide a framework to understand how flower opening and reproduction are coordinated in Arabidopsis and other flowering plants.
doi:10.1371/journal.pgen.1002506
PMCID: PMC3276552  PMID: 22346763
14.  Repression of Flowering by the miR172 Target SMZ 
PLoS Biology  2009;7(7):e1000148.
The flowering repressors SMZ and FLM, members of the AP-2 and MADS domain transcription factor families, unexpectedly work together to regulate flowering time via their effects on expression of the FT gene.
A small mobile protein, encoded by the FLOWERING LOCUS T (FT) locus, plays a central role in the control of flowering. FT is regulated positively by CONSTANS (CO), the output of the photoperiod pathway, and negatively by FLC, which integrates the effects of prolonged cold exposure. Here, we reveal the mechanisms of regulation by the microRNA miR172 target SCHLAFMÜTZE (SMZ), a potent repressor of flowering. Whole-genome mapping of SMZ binding sites demonstrates not only direct regulation of FT, but also of many other flowering time regulators acting both upstream and downstream of FT, indicating an important role of miR172 and its targets in fine tuning the flowering response. A role for the miR172/SMZ module as a rheostat in flowering time is further supported by SMZ binding to several other genes encoding miR172 targets. Finally, we show that the action of SMZ is completely dependent on another floral repressor, FLM, providing the first direct connection between two important classes of flowering time regulators, AP2- and MADS-domain proteins.
Author Summary
Flowering is a pivotal event in the life cycle of many plants and is therefore under tight control. The ability to detect the daily photoperiod is of particular importance in many plant species, as it enables them to enter the reproductive phase in response to seasonal changes in day length. When the photoperiod is permissive to flowering, a signal is produced in leaves that is transported to the shoot meristem, where it initiates the formation of flowers. It is now widely accepted that an important component of this long-distance signal is the flowering protein FT. Here, we show that the AP2-like transcription factor SMZ, which represses flowering and is a target of the regulatory miRNA172 microRNA, functions together with related proteins to directly regulate FT expression. Using chromatin immunoprecipitation coupled to genome tiling arrays, we find that SMZ binds directly to the FT genomic locus and to several other key flowering-related loci. Unexpectedly, the ability of SMZ to repress flowering strictly depends on the presence of the MADS-domain transcription factor FLM. In addition, SMZ binds to its own regulatory sequences and those of three closely related genes, providing evidence of strong negative feedback between SMZ and the other AP2-like miRNA172 targets.
doi:10.1371/journal.pbio.1000148
PMCID: PMC2701598  PMID: 19582143
15.  CONSTANS is a photoperiod regulated activator of flowering in sorghum 
BMC Plant Biology  2014;14:148.
Background
Sorghum genotypes used for grain production in temperate regions are photoperiod insensitive and flower early avoiding adverse environments during the reproductive phase. In contrast, energy sorghum hybrids are highly photoperiod sensitive with extended vegetative phases in long days, resulting in enhanced biomass accumulation. SbPRR37 and SbGHD7 contribute to photoperiod sensitivity in sorghum by repressing expression of SbEHD1 and FT-like genes, thereby delaying flowering in long days with minimal influence in short days (PNAS_108:16469-16474, 2011; Plant Genome_in press, 2014). The GIGANTEA (GI)-CONSTANS (CO)-FLOWERING LOCUS T (FT) pathway regulates flowering time in Arabidopsis and the grasses (J Exp Bot_62:2453-2463, 2011). In long day flowering plants, such as Arabidopsis and barley, CONSTANS activates FT expression and flowering in long days. In rice, a short day flowering plant, Hd1, the ortholog of CONSTANS, activates flowering in short days and represses flowering in long days.
Results
Quantitative trait loci (QTL) that modify flowering time in sorghum were identified by screening Recombinant Inbred Lines (RILs) derived from BTx642 and Tx7000 in long days, short days, and under field conditions. Analysis of the flowering time QTL on SBI-10 revealed that BTx642 encodes a recessive CONSTANS allele containing a His106Tyr substitution in B-box 2 known to inactivate CONSTANS in Arabidopsis thaliana. Genetic analysis characterized sorghum CONSTANS as a floral activator that promotes flowering by inducing the expression of EARLY HEADING DATE 1 (SbEHD1) and sorghum orthologs of the maize FT genes ZCN8 (SbCN8) and ZCN12 (SbCN12). The floral repressor PSEUDORESPONSE REGULATOR PROTEIN 37 (PRR37) inhibits sorghum CONSTANS activity and flowering in long days.
Conclusion
Sorghum CONSTANS is an activator of flowering that is repressed post-transcriptionally in long days by the floral inhibitor PRR37, contributing to photoperiod sensitive flowering in Sorghum bicolor, a short day plant.
doi:10.1186/1471-2229-14-148
PMCID: PMC4046011  PMID: 24884377
Photoperiod; Sorghum; Flowering time; QTL; CONSTANS; PRR37
16.  Coordination of Plastid and Light Signaling Pathways upon Development of Arabidopsis Leaves under Various Photoperiods 
Molecular Plant  2011;5(4):799-816.
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.
doi:10.1093/mp/ssr106
PMCID: PMC3399700  PMID: 22199239
acclimation; chloroplast biology; circadian clock; leaf/vegetative development; light signaling; photomorphogenesis; plastid signaling
17.  The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals 
Annals of Botany  2009;103(8):1165-1172.
Background
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.
Scope
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.
Conclusions
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.
doi:10.1093/aob/mcp063
PMCID: PMC2685306  PMID: 19304997
Flowering; vernalization; photoperiod; day length; VRN1; VRN2; FLC; FT; cereals; arabidopsis; MADS
18.  Comparative Genomics of Flowering Time Pathways Using Brachypodium distachyon as a Model for the Temperate Grasses 
PLoS ONE  2010;5(4):e10065.
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.
doi:10.1371/journal.pone.0010065
PMCID: PMC2856676  PMID: 20419097
19.  Natural variation reveals that intracellular distribution of ELF3 protein is associated with function in the circadian clock 
eLife  2014;3:e02206.
Natural selection of variants within the Arabidopsis thaliana circadian clock can be attributed to adaptation to varying environments. To define a basis for such variation, we examined clock speed in a reporter-modified Bay-0 x Shakdara recombinant inbred line and localized heritable variation. Extensive variation led us to identify EARLY FLOWERING3 (ELF3) as a major quantitative trait locus (QTL). The causal nucleotide polymorphism caused a short-period phenotype under light and severely dampened rhythm generation in darkness, and entrainment alterations resulted. We found that ELF3-Sha protein failed to properly localize to the nucleus, and its ability to accumulate in darkness was compromised. Evidence was provided that the ELF3-Sha allele originated in Central Asia. Collectively, we showed that ELF3 protein plays a vital role in defining its light-repressor action in the circadian clock and that its functional abilities are largely dependent on its cellular localization.
DOI: http://dx.doi.org/10.7554/eLife.02206.001
eLife digest
Life on Earth tends to follow a daily rhythm: some animals are awake during the day and asleep at night, whilst others are more active at night, or during the twilight around dawn and dusk. For many living things, these cycles of activity are driven by an internal body clock that helps the organism to adapt to the daily cycle of light and dark—and similar internal clocks also exist in plants.
These internal clocks define daily—or circadian—cycles whereby multiple genes are switched ‘on’ or ‘off’ at different time points in every 24-hr period. And, because light and ambient temperatures also vary with time of the day, many organisms use these external signals as cues to reset their own internal clocks. Moreover, the hours of daylight and temperature vary around the world, and also with the seasons, so plants and animals must be able to change how these external signals influence their internal clocks so that they stay in tune with the day/night cycle. However, it is not clear how they do this.
To explore this question, Anwer et al. grew plants that were from a cross between two types of the model plant Arabidopsis thaliana from different environments: one from Germany, and the other from Tajikistan in Central Asia. These offspring were also genetically engineered so that an enzyme that could give off light was produced under the control of the internal clock. Anwer et al. found that the plants continued to glow and fade with an almost daily rhythm even after external cues, such as changes in temperature or light, had been removed.
Different offspring plants consistently glowed and faded with different rhythms such that some had, for example, a 21-hr day and others a 28-hr day. These differences were caused by many genes that differed from the original German and Tajikistan parent plants, and Anwer et al. ‘mapped’ one of these genetic differences to a single gene. Offspring that inherited a version of a gene called ELF3 from the Tajikistan parent had internal clocks that ran faster when the plant was under the light. These plants also gradually stopped glowing as brightly as the German parent when they were kept in the dark, suggesting that their internal clocks were ‘ticking more softly’. It was already known that the ELF3 gene affected the circadian clock in plants, and Anwer et al. thus concluded that the plants with Tajikistan version of this gene, called ELF3-Sha, were also less able to reset their internal clocks to synchronize in response to external cues.
Anwer et al. also showed that the normal ELF3 protein is more likely to be found in the nucleus of a plant cell than the ELF3-Sha version, which might suggest that this protein is involved in switching genes off. Further research is now needed to uncover exactly how the ELF3 protein does this to keep the plant's internal clock ‘ticking’ correctly.
DOI: http://dx.doi.org/10.7554/eLife.02206.002
doi:10.7554/eLife.02206
PMCID: PMC4071560  PMID: 24867215
circadian clock; QTL mapping/cloning; cell biology; eQTL; population analysis; Arabidopsis
20.  A Companion Cell–Dominant and Developmentally Regulated H3K4 Demethylase Controls Flowering Time in Arabidopsis via the Repression of FLC Expression 
PLoS Genetics  2012;8(4):e1002664.
Flowering time relies on the integration of intrinsic developmental cues and environmental signals. FLC and its downstream target FT are key players in the floral transition in Arabidopsis. Here, we characterized the expression pattern and function of JMJ18, a novel JmjC domain-containing histone H3K4 demethylase gene in Arabidopsis. JMJ18 was dominantly expressed in companion cells; its temporal expression pattern was negatively and positively correlated with that of FLC and FT, respectively, during vegetative development. Mutations in JMJ18 resulted in a weak late-flowering phenotype, while JMJ18 overexpressors exhibited an obvious early-flowering phenotype. JMJ18 displayed demethylase activity toward H3K4me3 and H3K4me2, and bound FLC chromatin directly. The levels of H3K4me3 and H3K4me2 in chromatins of FLC clade genes and the expression of FLC clade genes were reduced, whereas FT expression was induced and the protein expression of FT increased in JMJ18 overexpressor lines. The early-flowering phenotype caused by the overexpression of JMJ18 was mainly dependent on the functional FT. Our findings suggest that the companion cell–dominant and developmentally regulated JMJ18 binds directly to the FLC locus, reducing the level of H3K4 methylation in FLC chromatin and repressing the expression of FLC, thereby promoting the expression of FT in companion cells to stimulate flowering.
Author Summary
Flowering is an important developmental transition during plant life cycle and the key process for production of the next generation. Flowering time is controlled by both intrinsic developmental and environmental signals. FLC and its target FT work as repressor and activator, respectively, to regulate flowering time in Arabidopsis; thus the regulation of FLC and FT expression is the key for the control of floral transition. Epigenetic modifications are critical for transcription regulation. Here, we show that a novel JmjC domain-containing histone H3K4 demethylase, JMJ18, is a key regulator for the expression of FLC and FT in companion cells and flowering time. JMJ18 is dominantly expressed in vascular tissue; its temporal expression pattern was developmentally regulated, and negatively and positively correlated with FLC and FT, respectively. JMJ18 mutation leads to weak late-flowering, while JMJ18 overexpressor exhibited an obvious early-flowering phenotype. JMJ18 binds to chromatin of FLC, represses its expression, and releases expression of FT in companion cells. Our results suggest that JMJ18 is a developmentally regulated companion cell–dominantly expressed signal to control flowering time by binding to FLC—reducing level of H3K4 methylation in FLC and repressing expression of FLC—thereby promoting expression of FT in companion cells during vegetative development in Arabidopsis.
doi:10.1371/journal.pgen.1002664
PMCID: PMC3334889  PMID: 22536163
21.  Comparative genomic analysis of light-regulated transcripts in the Solanaceae 
BMC Genomics  2009;10:60.
Background
Plants use different light signals to adjust their growth and development to the prevailing environmental conditions. Studies in the model species Arabidopsis thaliana and rice indicate that these adjustments are mediated by large changes in the transcriptome. Here we compared transcriptional responses to light in different species of the Solanaceae to investigate common as well as species-specific changes in gene expression.
Results
cDNA microarrays were used to identify genes regulated by a transition from long days (LD) to short days (SD) in the leaves of potato and tobacco plants, and by phytochrome B (phyB), the photoreceptor that represses tuberization under LD in potato. We also compared transcriptional responses to photoperiod in Nicotiana tabacum Maryland Mammoth (MM), which flowers only under SD, with those of Nicotiana sylvestris, which flowers only under LD conditions. Finally, we identified genes regulated by red compared to far-red light treatments that promote germination in tomato.
Conclusion
Most of the genes up-regulated in LD were associated with photosynthesis, the synthesis of protective pigments and the maintenance of redox homeostasis, probably contributing to the acclimatization to seasonal changes in irradiance. Some of the photoperiodically regulated genes were the same in potato and tobacco. Others were different but belonged to similar functional categories, suggesting that conserved as well as convergent evolutionary processes are responsible for physiological adjustments to seasonal changes in the Solanaceae. A β-ZIP transcription factor whose expression correlated with the floral transition in Nicotiana species with contrasting photoperiodic responses was also regulated by photoperiod and phyB in potato, and is a candidate gene to act as a general regulator of photoperiodic responses. Finally, GIGANTEA, a gene that controls flowering time in Arabidopsis thaliana and rice, was regulated by photoperiod in the leaves of potato and tobacco and by red compared to far-light treatments that promote germination in tomato seeds, suggesting that a conserved light signaling cascade acts across developmental contexts and species.
doi:10.1186/1471-2164-10-60
PMCID: PMC2644711  PMID: 19192291
22.  Use of transcriptome sequencing to understand the pistillate flowering in hickory (Carya cathayensis Sarg.) 
BMC Genomics  2013;14:691.
Background
Different from herbaceous plants, the woody plants undergo a long-period vegetative stage to achieve floral transition. They then turn into seasonal plants, flowering annually. In this study, a preliminary model of gene regulations for seasonal pistillate flowering in hickory (Carya cathayensis) was proposed. The genome-wide dynamic transcriptome was characterized via the joint-approach of RNA sequencing and microarray analysis.
Results
Differential transcript abundance analysis uncovered the dynamic transcript abundance patterns of flowering correlated genes and their major functions based on Gene Ontology (GO) analysis. To explore pistillate flowering mechanism in hickory, a comprehensive flowering gene regulatory network based on Arabidopsis thaliana was constructed by additional literature mining. A total of 114 putative flowering or floral genes including 31 with differential transcript abundance were identified in hickory. The locations, functions and dynamic transcript abundances were analyzed in the gene regulatory networks. A genome-wide co-expression network for the putative flowering or floral genes shows three flowering regulatory modules corresponding to response to light abiotic stimulus, cold stress, and reproductive development process, respectively. Totally 27 potential flowering or floral genes were recruited which are meaningful to understand the hickory specific seasonal flowering mechanism better.
Conclusions
Flowering event of pistillate flower bud in hickory is triggered by several pathways synchronously including the photoperiod, autonomous, vernalization, gibberellin, and sucrose pathway. Totally 27 potential flowering or floral genes were recruited from the genome-wide co-expression network function module analysis. Moreover, the analysis provides a potential FLC-like gene based vernalization pathway and an 'AC’ model for pistillate flower development in hickory. This work provides an available framework for pistillate flower development in hickory, which is significant for insight into regulation of flowering and floral development of woody plants.
doi:10.1186/1471-2164-14-691
PMCID: PMC3853572  PMID: 24106755
Co-expression network; Carya cathayensis Sarg; Floral development; Seasonal flowering; Hickory; High-throughput data analysis
23.  An assessment of morphogenetic fluctuation during reproductive phase change in Arabidopsis 
Annals of Botany  2011;107(6):1017-1027.
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.
Methods
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.
Key Results
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.
Conclusions
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.
doi:10.1093/aob/mcr039
PMCID: PMC3080622  PMID: 21367754
Arabidopsis; bolting; early flowering mutants; flowering time; internode patterning; phase change; photoperiod; phytomer identity
24.  Identification of flowering genes in strawberry, a perennial SD plant 
BMC Plant Biology  2009;9:122.
Background
We are studying the regulation of flowering in perennial plants by using diploid wild strawberry (Fragaria vesca L.) as a model. Wild strawberry is a facultative short-day plant with an obligatory short-day requirement at temperatures above 15°C. At lower temperatures, however, flowering induction occurs irrespective of photoperiod. In addition to short-day genotypes, everbearing forms of wild strawberry are known. In 'Baron Solemacher' recessive alleles of an unknown repressor, SEASONAL FLOWERING LOCUS (SFL), are responsible for continuous flowering habit. Although flower induction has a central effect on the cropping potential, the molecular control of flowering in strawberries has not been studied and the genetic flowering pathways are still poorly understood. The comparison of everbearing and short-day genotypes of wild strawberry could facilitate our understanding of fundamental molecular mechanisms regulating perennial growth cycle in plants.
Results
We have searched homologs for 118 Arabidopsis flowering time genes from Fragaria by EST sequencing and bioinformatics analysis and identified 66 gene homologs that by sequence similarity, putatively correspond to genes of all known genetic flowering pathways. The expression analysis of 25 selected genes representing various flowering pathways did not reveal large differences between the everbearing and the short-day genotypes. However, putative floral identity and floral integrator genes AP1 and LFY were co-regulated during early floral development. AP1 mRNA was specifically accumulating in the shoot apices of the everbearing genotype, indicating its usability as a marker for floral initiation. Moreover, we showed that flowering induction in everbearing 'Baron Solemacher' and 'Hawaii-4' was inhibited by short-day and low temperature, in contrast to short-day genotypes.
Conclusion
We have shown that many central genetic components of the flowering pathways in Arabidopsis can be identified from strawberry. However, novel regulatory mechanisms exist, like SFL that functions as a switch between short-day/low temperature and long-day/high temperature flowering responses between the short-day genotype and the everbearing 'Baron Solemacher'. The identification of putative flowering gene homologs and AP1 as potential marker gene for floral initiation will strongly facilitate the exploration of strawberry flowering pathways.
doi:10.1186/1471-2229-9-122
PMCID: PMC2761920  PMID: 19785732
25.  In the Light of Evolution: A Reevaluation of Conservation in the CO–FT Regulon and Its Role in Photoperiodic Regulation of Flowering Time 
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.
doi:10.3389/fpls.2011.00081
PMCID: PMC3355682  PMID: 22639612
flowering time; CONSTANS; FLOWERING LOCUS T; photoperiod

Results 1-25 (1063370)