Nitrogen sensing and regulatory networks: it's about time and space

Author:

Shanks Carly M1ORCID,Rothkegel Karin23ORCID,Brooks Matthew D4ORCID,Cheng Chia-Yi5ORCID,Alvarez José M26ORCID,Ruffel Sandrine7ORCID,Krouk Gabriel7ORCID,Gutiérrez Rodrigo A23ORCID,Coruzzi Gloria M1ORCID

Affiliation:

1. Department of Biology, Center for Genomics and Systems Biology, New York University , New York, NY 10003 , USA

2. Agencia Nacional de Investigación y Desarrollo-Millennium Science Initiative Program, Millennium Institute for Integrative Biology (iBio) , 7500565 Santiago , Chile

3. Center for Genome Regulation (CRG), Institute of Ecology and Biodiversity (IEB), Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile , 8331010 Santiago , Chile

4. Global Change and Photosynthesis Research Unit, USDA-ARS , Urbana, IL 61801 , USA

5. Department of Life Science, National Taiwan University , Taipei 10663 , Taiwan

6. Centro de Biotecnología Vegetal, Facultad de Ciencias, Universidad Andrés Bello , 8370035 Santiago , Chile

7. Institute for Plant Sciences of Montpellier (IPSiM), Centre National de la Recherche Scientifique (CNRS), Institut National de Recherche pour l’Agriculture, l’Alimentation, et l'Environnement (INRAE), Université de Montpellier , Montpellier 34090 , France

Abstract

Abstract A plant's response to external and internal nitrogen signals/status relies on sensing and signaling mechanisms that operate across spatial and temporal dimensions. From a comprehensive systems biology perspective, this involves integrating nitrogen responses in different cell types and over long distances to ensure organ coordination in real time and yield practical applications. In this prospective review, we focus on novel aspects of nitrogen (N) sensing/signaling uncovered using temporal and spatial systems biology approaches, largely in the model Arabidopsis. The temporal aspects span: transcriptional responses to N-dose mediated by Michaelis-Menten kinetics, the role of the master NLP7 transcription factor as a nitrate sensor, its nitrate-dependent TF nuclear retention, its “hit-and-run” mode of target gene regulation, and temporal transcriptional cascade identified by “network walking.” Spatial aspects of N-sensing/signaling have been uncovered in cell type-specific studies in roots and in root-to-shoot communication. We explore new approaches using single-cell sequencing data, trajectory inference, and pseudotime analysis as well as machine learning and artificial intelligence approaches. Finally, unveiling the mechanisms underlying the spatial dynamics of nitrogen sensing/signaling networks across species from model to crop could pave the way for translational studies to improve nitrogen-use efficiency in crops. Such outcomes could potentially reduce the detrimental effects of excessive fertilizer usage on groundwater pollution and greenhouse gas emissions.

Funder

Zegar Family Foundation

NIH NIGMS Fellowship

ANID-FONDECYT Postdoctorado

MOST research

ANID-Millennium Science Initiative Program-Millennium Institute for Integrative Biology

Center for Genome Regulation

FONDECYT

ANID-Millennium Science Initiative Program-Millennium Institute

ANID FONDECYT

Metaprogram DIGIT-BIO from INRAE

ANR Plan de Relance TravelPep

MUSE University of Montpellier

French National Research Agency

Publisher

Oxford University Press (OUP)

Reference150 articles.

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4. Time-based systems biology approaches to capture and model dynamic gene regulatory networks;Alvarez;Annu Rev Plant Biol,2021

5. Transient genome-wide interactions of the master transcription factor NLP7 initiate a rapid nitrogen-response cascade;Alvarez;Nat Commun,2020

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