Network Walking charts transcriptional dynamics of nitrogen signaling by integrating validated and predicted genome-wide interactions

Matthew D. Brooks, Jacopo Cirrone, Angelo V. Pasquino, Jose M. Alvarez, Joseph Swift, Shipra Mittal, Che Lun Juang, Kranthi Varala, Rodrigo A. Gutiérrez, Gabriel Krouk, Dennis Shasha, Gloria Coruzzi

Research output: Contribution to journalArticle

Abstract

Charting a temporal path in gene networks requires linking early transcription factor (TF)-triggered events to downstream effects. We scale-up a cell-based TF-perturbation assay to identify direct regulated targets of 33 nitrogen (N)-early response TFs encompassing 88% of N-responsive Arabidopsis genes. We uncover a duality where each TF is an inducer and repressor, and in vitro cis-motifs are typically specific to regulation directionality. Validated TF-targets (71,836) are used to refine precision of a time-inferred root network, connecting 145 N-responsive TFs and 311 targets. These data are used to chart network paths from direct TF 1 -regulated targets identified in cells to indirect targets responding only in planta via Network Walking. We uncover network paths from TGA1 and CRF4 to direct TF 2 targets, which in turn regulate 76% and 87% of TF 1 indirect targets in planta, respectively. These results have implications for N-use and the approach can reveal temporal networks for any biological system.

Original languageEnglish (US)
Article number1569
JournalNature Communications
Volume10
Issue number1
DOIs
StatePublished - Dec 1 2019

Fingerprint

walking
genome
charts
Walking
Transcription Factors
Nitrogen
Genes
Genome
nitrogen
interactions
genes
Gene Regulatory Networks
Biological systems
cells
Arabidopsis
Assays
perturbation

ASJC Scopus subject areas

  • Chemistry(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physics and Astronomy(all)

Cite this

Network Walking charts transcriptional dynamics of nitrogen signaling by integrating validated and predicted genome-wide interactions. / Brooks, Matthew D.; Cirrone, Jacopo; Pasquino, Angelo V.; Alvarez, Jose M.; Swift, Joseph; Mittal, Shipra; Juang, Che Lun; Varala, Kranthi; Gutiérrez, Rodrigo A.; Krouk, Gabriel; Shasha, Dennis; Coruzzi, Gloria.

In: Nature Communications, Vol. 10, No. 1, 1569, 01.12.2019.

Research output: Contribution to journalArticle

Brooks, MD, Cirrone, J, Pasquino, AV, Alvarez, JM, Swift, J, Mittal, S, Juang, CL, Varala, K, Gutiérrez, RA, Krouk, G, Shasha, D & Coruzzi, G 2019, 'Network Walking charts transcriptional dynamics of nitrogen signaling by integrating validated and predicted genome-wide interactions', Nature Communications, vol. 10, no. 1, 1569. https://doi.org/10.1038/s41467-019-09522-1
Brooks, Matthew D. ; Cirrone, Jacopo ; Pasquino, Angelo V. ; Alvarez, Jose M. ; Swift, Joseph ; Mittal, Shipra ; Juang, Che Lun ; Varala, Kranthi ; Gutiérrez, Rodrigo A. ; Krouk, Gabriel ; Shasha, Dennis ; Coruzzi, Gloria. / Network Walking charts transcriptional dynamics of nitrogen signaling by integrating validated and predicted genome-wide interactions. In: Nature Communications. 2019 ; Vol. 10, No. 1.
@article{bf7954859407435db64db30daf8aa5b4,
title = "Network Walking charts transcriptional dynamics of nitrogen signaling by integrating validated and predicted genome-wide interactions",
abstract = "Charting a temporal path in gene networks requires linking early transcription factor (TF)-triggered events to downstream effects. We scale-up a cell-based TF-perturbation assay to identify direct regulated targets of 33 nitrogen (N)-early response TFs encompassing 88{\%} of N-responsive Arabidopsis genes. We uncover a duality where each TF is an inducer and repressor, and in vitro cis-motifs are typically specific to regulation directionality. Validated TF-targets (71,836) are used to refine precision of a time-inferred root network, connecting 145 N-responsive TFs and 311 targets. These data are used to chart network paths from direct TF 1 -regulated targets identified in cells to indirect targets responding only in planta via Network Walking. We uncover network paths from TGA1 and CRF4 to direct TF 2 targets, which in turn regulate 76{\%} and 87{\%} of TF 1 indirect targets in planta, respectively. These results have implications for N-use and the approach can reveal temporal networks for any biological system.",
author = "Brooks, {Matthew D.} and Jacopo Cirrone and Pasquino, {Angelo V.} and Alvarez, {Jose M.} and Joseph Swift and Shipra Mittal and Juang, {Che Lun} and Kranthi Varala and Guti{\'e}rrez, {Rodrigo A.} and Gabriel Krouk and Dennis Shasha and Gloria Coruzzi",
year = "2019",
month = "12",
day = "1",
doi = "10.1038/s41467-019-09522-1",
language = "English (US)",
volume = "10",
journal = "Nature Communications",
issn = "2041-1723",
publisher = "Nature Publishing Group",
number = "1",

}

TY - JOUR

T1 - Network Walking charts transcriptional dynamics of nitrogen signaling by integrating validated and predicted genome-wide interactions

AU - Brooks, Matthew D.

AU - Cirrone, Jacopo

AU - Pasquino, Angelo V.

AU - Alvarez, Jose M.

AU - Swift, Joseph

AU - Mittal, Shipra

AU - Juang, Che Lun

AU - Varala, Kranthi

AU - Gutiérrez, Rodrigo A.

AU - Krouk, Gabriel

AU - Shasha, Dennis

AU - Coruzzi, Gloria

PY - 2019/12/1

Y1 - 2019/12/1

N2 - Charting a temporal path in gene networks requires linking early transcription factor (TF)-triggered events to downstream effects. We scale-up a cell-based TF-perturbation assay to identify direct regulated targets of 33 nitrogen (N)-early response TFs encompassing 88% of N-responsive Arabidopsis genes. We uncover a duality where each TF is an inducer and repressor, and in vitro cis-motifs are typically specific to regulation directionality. Validated TF-targets (71,836) are used to refine precision of a time-inferred root network, connecting 145 N-responsive TFs and 311 targets. These data are used to chart network paths from direct TF 1 -regulated targets identified in cells to indirect targets responding only in planta via Network Walking. We uncover network paths from TGA1 and CRF4 to direct TF 2 targets, which in turn regulate 76% and 87% of TF 1 indirect targets in planta, respectively. These results have implications for N-use and the approach can reveal temporal networks for any biological system.

AB - Charting a temporal path in gene networks requires linking early transcription factor (TF)-triggered events to downstream effects. We scale-up a cell-based TF-perturbation assay to identify direct regulated targets of 33 nitrogen (N)-early response TFs encompassing 88% of N-responsive Arabidopsis genes. We uncover a duality where each TF is an inducer and repressor, and in vitro cis-motifs are typically specific to regulation directionality. Validated TF-targets (71,836) are used to refine precision of a time-inferred root network, connecting 145 N-responsive TFs and 311 targets. These data are used to chart network paths from direct TF 1 -regulated targets identified in cells to indirect targets responding only in planta via Network Walking. We uncover network paths from TGA1 and CRF4 to direct TF 2 targets, which in turn regulate 76% and 87% of TF 1 indirect targets in planta, respectively. These results have implications for N-use and the approach can reveal temporal networks for any biological system.

UR - http://www.scopus.com/inward/record.url?scp=85064013202&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85064013202&partnerID=8YFLogxK

U2 - 10.1038/s41467-019-09522-1

DO - 10.1038/s41467-019-09522-1

M3 - Article

VL - 10

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

IS - 1

M1 - 1569

ER -