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A SAM oligomerization domain shapes the genomic binding landscape of the LEAFY transcription factor

ABSTRACT: Multicellular organisms develop new structures by initiating specific gene regulatory programs through coordinated changes at the transcriptional and chromatin levels. Master transcription factors orchestrate such global changes but the underlying molecular mechanisms remain unclear. Here we focus on LEAFY (LFY), a key regulator of flower development in angiosperms. The resolution of the crystallographic structure of its N-terminal domain shows that it forms an unanticipated Sterile Alpha Motif (SAM) domain. This domain drives LFY oligomerization, which we establish to be essential for LFY floral switch function. Combining in vitro and in vivo experiments, we demonstrate that oligomerization facilitates LFY binding to DNA regions with multiple binding sites. Moreover, genome-wide analyses reveal an additional prominent role for the oligomerization domain: it confers upon LFY the capacity to bind to closed chromatin regions. This novel property, combined with its previously demonstrated capacity to recruit chromatin remodelers, indicates that LFY controls floral fate by acting as a plant pioneer transcription factor.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE64245 | GEO | 2016/04/08

SECONDARY ACCESSION(S): PRJNA270526

REPOSITORIES: GEO

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The F-box cofactor UFO redirects the LEAFY floral regulator to novel cis-elements

Project description:In angiosperms, flower patterning requires the localized expression of the APETALA3 (AP3) floral homeotic gene involved in petal and stamen development. AP3 is synergistically induced by the master transcription factor LEAFY (LFY) and the F-box protein UNUSUAL FLORAL ORGANS (UFO), but the molecular mechanism underlying this synergy has remained unknown. Here we show that the connection to ubiquitination pathways suggested by the F-box domain of UFO is mostly dispensable and that UFO instead acts by forming a transcriptional complex with LFY on newly discovered regulatory elements. The cryo-electron microscopy structure of the UFO-LFY-DNA complex shows that UFO-DNA contacts allows relocating LFY to novel DNA sites. Finally, we show that this complex has a deep evolutionary origin, largely predating flowering plants. This work unravels an unsuspected role for a member of one of the largest protein families in plants as a modulator of the DNA binding specificity of a master TF.

2023-01-01 | GSE204793 | GEO

A biophysical DNA binding model for the LEAFY transcription factor reveals the evolutionary fluidity of its binding sites

Project description:Despite great advances in sequencing capacity, generating functional information for non-model organisms remains a challenge. One solution lies in an improved ability to predict genetic circuits based on primary DNA sequence combined with the characterization of regulatory molecules from model species. Here, we focus on the LEAFY (LFY) transcription factor, a conserved master regulator of floral development. Starting with biochemical and structural information, we built a biophysical model describing LFY DNA binding specificity in vitro that accurately predicts in vivo LFY binding sites in the Arabidopsis thaliana genome. Extending the model to other species, we show that it can correctly identify functional homologs of known LFY targets from Arabidopsis thaliana in other angiosperms, even if a functional shift between orthologs and paralogs has occurred. Moreover, this model demonstrates the evolutionary fluidity of the link between LFY and one of its target genes, underlining how this regulatory interaction can be conserved despite changes in position, sequence and affinity of the LFY binding sites. Our study shows that the cis-element fluidity recently illustrated in animals also exists in plants, and that it can be detected without any experimental work in each individual species, using a biophysical transcription factor model. A. thaliana LEAFY ChIP-seq w control, 2 replicates

2011-05-13 | E-GEOD-24568 | biostudies-arrayexpress

Transcription factor Interplay between LEAFY and APETALA1/ CAULIFLOWER during Floral Initiation

Project description:The transcription factors LEAFY (LFY) and APETALA1 (AP1)_together with the AP1 paralog CAULIFLOWER (CAL)_control the onRep_of flower development in a partially redundant manner. This redundancy is thought to be mediated_at least in part_through the regulation of a shared Rep_of target genes. However_whether these genes are independently or cooperatively regulated by LFY and AP1/CAL_is currently unknown. To better understand the regulatory relationship between LFY and AP1/CAL during floral initiation_we monitored the activity of LFY in the absence of AP1/CAL function. We found that the regulation of several known LFY target genes is unaffected by AP1/CAL perturbation_while others appear to require AP1/CAL activity. Furthermore_we obtained evidence that LFY and AP1/CAL control the expression of some genes in an antagonistic manner. Notably_these include key regulators of floral initiation such TERMINAL FLOWER1 (TFL1)_which had been previously reported to be directly repressed by both LFY and AP1. We show here that TFL1 expression is suppressed by AP1 but promoted by LFY. We further demonstrate that LFY has an inhibitory effect on flower formation in the absence of AP1/CAL activity. We propose that LFY and AP1/CAL may act as part of an incoherent feed-forward loop to control the establishment of a stable developmental program for the formation of flowers.

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Transcription factor Interplay between LEAFY and APETALA1/ CAULIFLOWER during Floral Initiation

Project description:The transcription factors LEAFY (LFY) and APETALA1 (AP1), together with the AP1 paralog CAULIFLOWER (CAL), control the onset of flower development in a partially redundant manner. This redundancy is thought to be mediated, at least in part, through the regulation of a shared set of target genes. However, whether these genes are independently or cooperatively regulated by LFY and AP1/CAL, is currently unknown. To better understand the regulatory relationship between LFY and AP1/CAL during floral initiation, we monitored the activity of LFY in the absence of AP1/CAL function. We found that the regulation of several known LFY target genes is unaffected by AP1/CAL perturbation, while others appear to require AP1/CAL activity. Furthermore, we obtained evidence that LFY and AP1/CAL control the expression of some genes in an antagonistic manner. Notably, these include key regulators of floral initiation such TERMINAL FLOWER1 (TFL1), which had been previously reported to be directly repressed by both LFY and AP1. We show here that TFL1 expression is suppressed by AP1 but promoted by LFY. We further demonstrate that LFY has an inhibitory effect on flower formation in the absence of AP1/CAL activity. We propose that LFY and AP1/CAL may act as part of an incoherent feed-forward loop to control the establishment of a stable developmental program for the formation of flowers.

2017-04-28 | GSE96806 | GEO

LEAFY target genes reveal a link between flower development and biotic stimulus response (II)

Project description:The transition from vegetative growth to flower formation is critical for the survival of flowering plants. The plant-specific transcription factor LEAFY (LFY) has central, evolutionarily conserved roles in this process, both in the formation of the first flower and later in floral patterning. We performed genome-wide binding and expression studies to elucidate the molecular mechanisms by which LFY executes these roles. Our study reveals that LFY directs an intricate regulatory network in control of floral homeotic gene expression and, unexpectedly, controls the expression of genes regulating the response to external stimuli in Arabidopsis. We further show that LFY dampens responses to a bacterial MAMP (microbe-associated molecular pattern) and to pathogen challenge. Our findings suggest a molecular mechanism for the coordination of reproductive stage development and disease response programs in plants. Regulation of these distinct survival programs by a single transcription factor may ensure optimal allocation of plant resources for reproductive fitness. Genome binding/occupancy profiling by genome tiling array used to identity genes bound by endogenous LFY in inflorescences.

2011-05-11 | GSE28061 | GEO

LEAFY target genes reveal a link between flower development and biotic stimulus response (I)

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LEAFY target genes reveal a link between flower development and biotic stimulus response (III)

Project description:The transition from vegetative growth to flower formation is critical for the survival of flowering plants. The plant-specific transcription factor LEAFY (LFY) has central, evolutionarily conserved roles in this process, both in the formation of the first flower and later in floral patterning. We performed genome-wide binding and expression studies to elucidate the molecular mechanisms by which LFY executes these roles. Our study reveals that LFY directs an intricate regulatory network in control of floral homeotic gene expression and, unexpectedly, controls the expression of genes regulating the response to external stimuli in Arabidopsis. We further show that LFY dampens responses to a bacterial MAMP (microbe-associated molecular pattern) and to pathogen challenge. Our findings suggest a molecular mechanism for the coordination of reproductive stage development and disease response programs in plants. Regulation of these distinct survival programs by a single transcription factor may ensure optimal allocation of plant resources for reproductive fitness. Expression array analysis used to identify genes differentially expressed upon LFY induction in 9-day-old shoot apices.

2011-05-11 | GSE28062 | GEO

LEAFY target genes reveal a link between flower development and biotic stimulus response (III)

Project description:The transition from vegetative growth to flower formation is critical for the survival of flowering plants. The plant-specific transcription factor LEAFY (LFY) has central, evolutionarily conserved roles in this process, both in the formation of the first flower and later in floral patterning. We performed genome-wide binding and expression studies to elucidate the molecular mechanisms by which LFY executes these roles. Our study reveals that LFY directs an intricate regulatory network in control of floral homeotic gene expression and, unexpectedly, controls the expression of genes regulating the response to external stimuli in Arabidopsis. We further show that LFY dampens responses to a bacterial MAMP (microbe-associated molecular pattern) and to pathogen challenge. Our findings suggest a molecular mechanism for the coordination of reproductive stage development and disease response programs in plants. Regulation of these distinct survival programs by a single transcription factor may ensure optimal allocation of plant resources for reproductive fitness. Expression array analysis used to identify genes differentially expressed upon LFY induction in 9-day-old shoot apices. Expression array analysis of 9-day-old 35S::LFY-GR dexamethasone-treated seedlings compared to 9-day-old WT dexamethasone-treated seedlings. Four biological replicate samples.

2011-05-11 | E-GEOD-28062 | biostudies-arrayexpress

A biophysical DNA binding model for the LEAFY transcription factor reveals the evolutionary fluidity of its binding sites

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