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

Alessia Para, Ying Li, Amy Marshall-Coloń, Kranthi Varala, Nancy J. Francoeur, Tara M. Moran, Molly B. Edwards, Christopher Hackley, Bastiaan O R Bargmann, Kenneth Birnbaum, W. Richard McCombie, Gabriel Krouk, Gloria Coruzzi

Research output: Contribution to journalArticle

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. transcription regulation, nitrogen signaling, systems biology, gene networks.

Original languageEnglish (US)
Pages (from-to)10371-10376
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume111
Issue number28
DOIs
StatePublished - Jul 15 2014

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Leucine Zippers
Arabidopsis
Transcription Factors
Food
Gene Regulatory Networks
Genes
Nitrogen
Basic-Leucine Zipper Transcription Factors
Systems Biology

ASJC Scopus subject areas

  • General

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Hit-and-run transcriptional control by bZIP1 mediates rapid nutrient signaling in Arabidopsis. / Para, Alessia; Li, Ying; Marshall-Coloń, Amy; Varala, Kranthi; Francoeur, Nancy J.; Moran, Tara M.; Edwards, Molly B.; Hackley, Christopher; Bargmann, Bastiaan O R; Birnbaum, Kenneth; Richard McCombie, W.; Krouk, Gabriel; Coruzzi, Gloria.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, No. 28, 15.07.2014, p. 10371-10376.

Research output: Contribution to journalArticle

Para, A, Li, Y, Marshall-Coloń, A, Varala, K, Francoeur, NJ, Moran, TM, Edwards, MB, Hackley, C, Bargmann, BOR, Birnbaum, K, Richard McCombie, W, Krouk, G & Coruzzi, G 2014, 'Hit-and-run transcriptional control by bZIP1 mediates rapid nutrient signaling in Arabidopsis', Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 28, pp. 10371-10376. https://doi.org/10.1073/pnas.1404657111
Para, Alessia ; Li, Ying ; Marshall-Coloń, Amy ; Varala, Kranthi ; Francoeur, Nancy J. ; Moran, Tara M. ; Edwards, Molly B. ; Hackley, Christopher ; Bargmann, Bastiaan O R ; Birnbaum, Kenneth ; Richard McCombie, W. ; Krouk, Gabriel ; Coruzzi, Gloria. / Hit-and-run transcriptional control by bZIP1 mediates rapid nutrient signaling in Arabidopsis. In: Proceedings of the National Academy of Sciences of the United States of America. 2014 ; Vol. 111, No. 28. pp. 10371-10376.
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