Abstract
Gene regulatory networks (GRNs) control development via cell type-specific gene expression and interactions between transcription factors (TFs) and regulatory promoter regions. Plant organ boundaries separate lateral organs from the apical meristem and harbor axillary meristems (AMs). AMs, as stem cell niches, make the shoot a ramifying system. Although AMs have important functions in plant development, our knowledge of organ boundary and AM formation remains rudimentary. Here, we generated a cellular-resolution genomewide gene expression map for low-abundance Arabidopsis thaliana organ boundary cells and constructed a genomewide protein–DNA interaction map focusing on genes affecting boundary and AM formation. The resulting GRN uncovers transcriptional signatures, predicts cellular functions, and identifies promoter hub regions that are bound by many TFs. Importantly, further experimental studies determined the regulatory effects of many TFs on their targets, identifying regulators and regulatory relationships in AM initiation. This systems biology approach thus enhances our understanding of a key developmental process.
Highlights
Systems biology aims to explain development, physiology, and pathology based on modular networks of expression, interaction, regulation, and metabolism (Long et al, 2008; Wellmer & Riechmann, 2010)
We introduced a reporter line carrying the fusion of the large subunit ribosomal protein L18 with N-terminal His and FLAG epitope tags (HF-RPL18) under the control of the pOp promoter (Jiao & Meyerowitz, 2010) into driver lines expressing the chimeric transcription factors (TFs) LhG4 under the control of the LATERAL SUPPRESSOR (LAS) promoter, and under the control of the ASYMMETRIC LEAVES1 (AS1) promoter
These driver lines were chosen because pLAS::LhG4 has boundary region-specific activity (Goldshmidt et al, 2008), and pAS1::LhG4 drives pOp reporter expression throughout emerging leaf primordia, but not in the shoot apical meristem (SAM) (Eshed et al, 2001) (Supplementary Fig S1)
Summary
Systems biology aims to explain development, physiology, and pathology based on modular networks of expression, interaction, regulation, and metabolism (Long et al, 2008; Wellmer & Riechmann, 2010). Gene expression is regulated in part by regulatory transcription factors (TFs) that bind to specific genomic regions. Each gene is likely regulated by multiple TFs, and each TF likely binds regulatory regions of multiple genes to activate or repress transcription. The majority of genes, including TF-encoding genes, show differential expression in various tissues and cell types in multicellular eukaryotes, including higher plants (Wang & Jiao, 2011). The combinatorial effect of tissue- and cell type-specific TF gene expression and the interaction between TFs and regulatory genomic regions of downstream genes results in qualitatively and quantitatively fine-tuned spatial and temporal gene expression. By integrating genomewide cellular-resolution expression and protein–DNA interaction (PDI) data, researchers can formulate hypotheses in biologically meaningful ways with higher confidence
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