Abstract
Floral homeotic transcription factors (TFs) act in a combinatorial manner to specify the organ identities in the flower. However, the architecture and the function of the gene regulatory network (GRN) controlling floral organ specification is still poorly understood. In particular, the interconnections of homeotic TFs, microRNAs (miRNAs) and other factors controlling organ initiation and growth have not been studied systematically so far. Here, using a combination of genome-wide TF binding, mRNA and miRNA expression data, we reconstruct the dynamic GRN controlling floral meristem development and organ differentiation. We identify prevalent feed-forward loops (FFLs) mediated by floral homeotic TFs and miRNAs that regulate common targets. Experimental validation of a coherent FFL shows that petal size is controlled by the SEPALLATA3-regulated miR319/TCP4 module. We further show that combinatorial DNA-binding of homeotic factors and selected other TFs is predictive of organ-specific patterns of gene expression. Our results provide a valuable resource for studying molecular regulatory processes underlying floral organ specification in plants.
Highlights
Floral homeotic transcription factors (TFs) act in a combinatorial manner to specify the organ identities in the flower
Principal component analysis (PCA) of Chromatin immunoprecipitation (ChIP)-seq signal profiles revealed that replicate datasets, or datasets for TFs with similar functions, tend to group together (Supplementary Fig. 2)
The results showed that deletion of SEP3 ChIP-seq peak in the MIR319a promoter, and of the far-upstream SEP3 ChIP-seq peak in the TCP4 promoter could significantly reduce the effect of SEP3 on luciferase expression (Supplementary Fig. 11)
Summary
Floral homeotic transcription factors (TFs) act in a combinatorial manner to specify the organ identities in the flower. According to the “floral quartet model”, floral homeotic proteins form organ-specific tetrameric protein complexes, and the higher-order interactions are mediated by the redundantly acting SEPALLATA (SEP) proteins (including SEP1, SEP2, SEP3, and SEP4)[14] In this model, sepals are specified by a complex consisting of AP1 and SEP proteins, while AP1, AP3, PISTILLATA (PI), and SEP form a higher-order complex that determines petal identity. A systematic analysis of the target gene networks of these master regulators is still lacking, and our knowledge towards the associated network components that control floral organ development is incomplete In this regard, the combination of genomic binding and expression data provide an opportunity to shed light on the regulatory “code” underlying floral organ specification
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