Hit-and-run transcriptional control by bZIP1 mediates rapid nutrient signaling in Arabidopsis

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 111; no. 28; pp. 10371 - 10376
• Main Authors: Para, Alessia, Li, Ying, Marshall-Colón, Amy, Varala, Kranthi, Francoeur, Nancy J., Moran, Tara M., Edwards, Molly B., Hackley, Christopher, Bargmann, Bastiaan O. R., Birnbaum, Kenneth D., McCombie, W. Richard, Krouk, Gabriel, Coruzzi, Gloria M.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 15.07.2014; National Acad Sciences
• Subjects: Anion Transport Proteins - biosynthesis; Anion Transport Proteins - genetics; Arabidopsis; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - biosynthesis; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Basic-Leucine Zipper Transcription Factors - genetics; Basic-Leucine Zipper Transcription Factors - metabolism; Binding sites; Biological Sciences; Catalysts; Datasets; Environmental changes; Eukaryotic cells; Gene expression; Gene expression regulation; Gene Expression Regulation, Plant - physiology; Genes; leucine zipper; Life Sciences; Nitrates; Nitrogen; Nitrogen - metabolism; Plant Proteins - biosynthesis; Plant Proteins - genetics; Protoplasts; regulator genes; Response Elements - physiology; Signal transduction; Signal Transduction - physiology; Time Factors; transcription (genetics); Transcription factors; Vegetal Biology; systems biology; transcription regulation; nitrogen signaling; gene networks; transcriptome; root; Local signalling; split-root; systemic signalling; phytohormone; nitrogen response; long-distance messenger
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.1404657111

The dynamic nature of gene regulatory networks allows cells to rapidly respond to environmental change. However, the underlying temporal connections are missed, even in kinetic studies, as transcription factor (TF) binding within at least one time point is required to identify primary targets. The TF-regulated but unbound genes are dismissed as secondary targets. Instead, we report that these genes comprise transient TF-target interactions most relevant to rapid signal transduction. We temporally perturbed a master TF (Basic Leucine Zipper 1, bZIP1) and the nitrogen (N) signal it transduces and integrated TF regulation and binding data from the same cell samples. Our enabling approach could identify primary TF targets based solely on gene regulation, in the absence of TF binding. We uncovered three classes of primary TF targets: (i) poised (TF-bound but not TF-regulated), (ii) stable (TF-bound and TF-regulated), and (iii) transient (TF-regulated but not TF-bound), the largest class. Unexpectedly, the transient bZIP1 targets are uniquely relevant to rapid N signaling in planta, enriched in dynamic N-responsive genes, and regulated by TF and N signal interactions. These transient targets include early N responders nitrate transporter 2.1 and NIN-like protein 3, bound by bZIP1 at 1—5 min, but not at later time points following TF perturbation. Moreover, promoters of these transient targets are uniquely enriched with cis-regulatory motifs coinherited with bZIP1 binding sites, suggesting a recruitment role for bZIP1. This transient mode of TF action supports a classic, but forgotten, "hit-and-run" transcription model, which enables a "catalyst TF" to activate a large set of targets within minutes of signal perturbation.