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Genome-Wide binding sites of two MADS-domain transcription factors SOC1 and SVP in Arabidopsis during the floral transition

ABSTRACT: The floral transition in Arabidopsis is tightly controlled by complex genetic regulatory networks in response to endogenous and environmental flowering signals. SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) and SHORT VEGETATIVE PHASE (SVP), two key MADS-domain transcription factors, perceive these signals and function as antagonistic flowering regulators. To understand how they mediate the floral transition, we mapped in vivo binding sites of SOC1 and SVP using chromatin immunoprecipitation followed by hybridization to whole-genome tiling arrays (ChIP-chip). Genes encoding proteins with transcription regulator activity and transcription factor activity were the most enriched groups of genes bound by SOC1 and SVP, indicating their central roles in flowering regulatory networks. In combination with gene expression microarray studies, we further identified the genes whose expression was directly regulated by SOC1 or SVP. Among the common direct targets identified, APETALA2 (AP2)-like genes that repress FT and SOC1 expression were downregulated by SOC1, but upregulated by SVP, revealing a complex feedback regulation among key genes determining the integration of flowering signals. SOC1 regulatory regions were also accessed by SOC1 itself and SVP, suggesting that self-activation and repression by SVP contribute to the regulation of SOC1 expression. In addition, ChIP-chip analysis demonstrated that miR156e and miR172a, which are involved in the regulation of AP2-like genes, were direct targets of SOC1 and SVP, respectively. Taken together, these findings reveal that feedback regulatory loops mediated by SOC1 and SVP are essential components of the gene regulatory networks underpinning the integration of flowering signals during the floral transition.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE33297 | GEO | 2012/02/01

SECONDARY ACCESSION(S): PRJNA149273

REPOSITORIES: GEO

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Project description:The transition to flowering in plants is controlled by a regulatory network that responds to both developmental and environmental signals. The MADS-box genes FLOWERING LOCUS C (FLC) and SHORT VEGETATIVE PHASE (SVP) are major flowering repressors that enhance responses to environmental cues such as winter temperatures, high ambient temperatures and photoperiod. FLC and SVP physically interact in vivo and mutation of each gene causes early flowering while the double mutant is more extreme. The molecular mechanisms underlying these genetic interactions are mostly unknown. We addressed the regulatory input of these two key transcription factors (TFs) both individually and as a complex at the genome-wide level through ChIP-seq and microarray expression analysis in single and double mutants. Analysis of each TF demonstrated that the complex acts predominantly via functional redundancy in the repression of flowering. SVP and FLC bind to the same regions of the flowering genes SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) and FLOWERING LOCUS T (FT) but do not require the presence of the other to bind. However, genome-wide identification of SVP and FLC occupancy events revealed that their binding scenarios are quantitatively and qualitatively affected by the presence of the cognate partner. A subgroup of genes whose regulation by these TFs depends exclusively on combinatorial binding of both proteins was identified, demonstrating a qualitatively essential role of the SVP-FLC complex. Some of these genes are involved in the control of flowering through direct and indirect regulation of Gibberellin-related processes. Cis-regulatory elements enriched only at such complex-bound sites were identified. Thus the regulatory output mediated by SVP and FLC reveals substantial flexibility, leading to dependent and independent DNA binding that enables additive, cooperative and repressive modes of co-regulation. In total 48 samples; 24 leaf samples corresponding to two different growing conditions, 24 apex samples corresponding to two different growing conditions.

Project description:Optimised flowering time is an important trait ensuring successful plant adaptation and crop productivity. SOC1-like genes encode MADS transcription factors known to play important roles in flowering control in many plants. This includes the best characterised eudicot model Arabidopsis thaliana (Arabidopsis) where SOC1 promotes flowering and functions as a floral integrator gene integrating signals from different flowering time regulatory pathways. Medicago truncatula (Medicago) is a temperate reference legume with strong genomic and genetic resources used to study flowering pathways in legumes. Interestingly, despite responding to the similar floral-inductive cues of extended cold (vernalisation) followed by warm long days, as winter annual Arabidopsis, Medicago lacks FLC and CO which are key regulators of flowering in Arabidopsis. Unlike Arabidopsis with one SOC1 gene, multiple gene duplication events have given rise to three MtSOC1 paralogs within the Medicago genus in legumes; one Fabaceae group A SOC1 gene, MtSOC1a, and two tandemly-repeated Fabaceae group B SOC1 genes, MtSOC1b and MtSOC1c. Previously, we showed that MtSOC1a has unique functions in floral promotion in Medicago. The Mtsoc1a Tnt1 retroelement insertion single mutant showed moderately delayed flowering in long and short day photoperiods, with and without prior vernalization, compared with wild type. On the other hand, Mtsoc1b Tnt1 single mutants did not have altered flowering time or flower development, indicating that it was redundant in an otherwise wild type background. Here, we describe the generation of Mtsoc1 triple mutant plants by CRISPR-Cas9 gene editing. Two independent Mtsoc1 homozygous triple mutants were non-flowering and bushy in floral inductive VLD. Phenotyping and gene expression analyses by RNA-seq and RT-qPCR indicate that the Mtsoc1 triple mutants remain vegetative. Thus overall, the Mtsoc1 triple mutants are dramatically different from the single Mtsoc1a mutant and the Arabidopsis soc1 mutant; implicating multiple MtSOC1 genes in critical overlapping roles in the transition to flowering in Medicago.

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Genome-Wide binding sites of two MADS-domain transcription factors SOC1 and SVP in Arabidopsis during the floral transition

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