title: Hit-and-run transcriptional control by bZIP1 mediates rapid nutrient signaling in Arabidopsis.
abstract: 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.
authors: Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY 10003;
authors: Alessia
authors: A
authors: Para
authors: Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY 10003;
authors: Ying
authors: Y
authors: Li
authors: Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY 10003;
authors: Amy
authors: A
authors: Marshall-Colón
authors: Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY 10003;
authors: Kranthi
authors: K
authors: Varala
authors: Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY 10003;
authors: Nancy J
authors: NJ
authors: Francoeur
authors: Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY 10003;
authors: Tara M
authors: TM
authors: Moran
authors: Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY 10003;
authors: Molly B
authors: MB
authors: Edwards
authors: Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY 10003;
authors: Christopher
authors: C
authors: Hackley
authors: Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY 10003;
authors: Bastiaan O R
authors: BO
authors: Bargmann
authors: Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY 10003;
authors: Kenneth D
authors: KD
authors: Birnbaum
authors: Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724; and.
authors: W Richard
authors: WR
authors: McCombie
authors: Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY 10003;Biochimie et Physiologie Moléculaire des Plantes, Unité Mixte de Recherche 5004, Centre National de la Recherche Scientifique/Institut National de la Recherche Agronomique/SupAgro/Université Montpellier 2, Institut de Biologie Intégrative des Plantes-Claude Grignon, 34060 Montpellier, France.
authors: Gabriel
authors: G
authors: Krouk
authors: Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY 10003; gloria.coruzzi@nyu.edu.
authors: Gloria M
authors: GM
authors: Coruzzi
mesh_terms: D027321:Anion Transport Proteins / Q000096:biosynthesis / Q000235:genetics; D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000096:biosynthesis / Q000235:genetics / Q000378:metabolism*; D050976:Basic-Leucine Zipper Transcription Factors / Q000235:genetics / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant / Q000502:physiology*; D009584:Nitrogen / Q000378:metabolism*; D010940:Plant Proteins / Q000096:biosynthesis / Q000235:genetics; D020218:Response Elements / Q000502:physiology*; D015398:Signal Transduction / Q000502:physiology*; D013997:Time Factors
chemical_list: D027321:Anion Transport Proteins; D029681:Arabidopsis Proteins; D050976:Basic-Leucine Zipper Transcription Factors; D009584:Nitrogen; D010940:Plant Proteins; C101492:NRT1.1 protein, Arabidopsis; C553903:bZIP1 protein, Arabidopsis; C477335:NRT2.1 protein, Arabidopsis
keywords: gene networks; nitrogen signaling; systems biology; transcription regulation