A genome‐scale TF–DNA interaction network of transcriptional regulation of Arabidopsis primary and specialized metabolism

Abstract Plant metabolism is more complex relative to individual microbes. In single‐celled microbes, transcriptional regulation by single transcription factors (TFs) is sufficient to shift primary metabolism. Corresponding genome‐level transcriptional regulatory maps of metabolism reveal the underl...

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Main Authors: Michelle Tang, Baohua Li, Xue Zhou, Tayah Bolt, Jia Jie Li, Neiman Cruz, Allison Gaudinier, Richard Ngo, Caitlin Clark‐Wiest, Daniel J Kliebenstein, Siobhan M Brady
Format: Article
Language:English
Published: Springer Nature 2021-11-01
Series:Molecular Systems Biology
Subjects:
Online Access:https://doi.org/10.15252/msb.202110625
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author Michelle Tang
Baohua Li
Xue Zhou
Tayah Bolt
Jia Jie Li
Neiman Cruz
Allison Gaudinier
Richard Ngo
Caitlin Clark‐Wiest
Daniel J Kliebenstein
Siobhan M Brady
author_facet Michelle Tang
Baohua Li
Xue Zhou
Tayah Bolt
Jia Jie Li
Neiman Cruz
Allison Gaudinier
Richard Ngo
Caitlin Clark‐Wiest
Daniel J Kliebenstein
Siobhan M Brady
author_sort Michelle Tang
collection DOAJ
description Abstract Plant metabolism is more complex relative to individual microbes. In single‐celled microbes, transcriptional regulation by single transcription factors (TFs) is sufficient to shift primary metabolism. Corresponding genome‐level transcriptional regulatory maps of metabolism reveal the underlying design principles responsible for these shifts as a model in which master regulators largely coordinate specific metabolic pathways. Plant primary and specialized metabolism occur within innumerable cell types, and their reactions shift depending on internal and external cues. Given the importance of plants and their metabolites in providing humanity with food, fiber, and medicine, we set out to develop a genome‐scale transcriptional regulatory map of Arabidopsis metabolic genes. A comprehensive set of protein–DNA interactions between Arabidopsis thaliana TFs and gene promoters in primary and specialized metabolic pathways were mapped. To demonstrate the utility of this resource, we identified and functionally validated regulators of the tricarboxylic acid (TCA) cycle. The resulting network suggests that plant metabolic design principles are distinct from those of microbes. Instead, metabolism appears to be transcriptionally coordinated via developmental‐ and stress‐conditional processes that can coordinate across primary and specialized metabolism. These data represent the most comprehensive resource of interactions between TFs and metabolic genes in plants.
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spelling doaj.art-962340fd55334b9da50d9b05a1caff5c2024-03-02T10:01:08ZengSpringer NatureMolecular Systems Biology1744-42922021-11-011711n/an/a10.15252/msb.202110625A genome‐scale TF–DNA interaction network of transcriptional regulation of Arabidopsis primary and specialized metabolismMichelle Tang0Baohua Li1Xue Zhou2Tayah Bolt3Jia Jie Li4Neiman Cruz5Allison Gaudinier6Richard Ngo7Caitlin Clark‐Wiest8Daniel J Kliebenstein9Siobhan M Brady10Department of Plant Biology and Genome Center University of California, Davis Davis CA USADepartment of Plant Sciences University of California, Davis Davis CA USADepartment of Plant Sciences University of California, Davis Davis CA USADepartment of Plant Sciences University of California, Davis Davis CA USADepartment of Plant Sciences University of California, Davis Davis CA USADepartment of Plant Biology and Genome Center University of California, Davis Davis CA USADepartment of Plant Biology and Genome Center University of California, Davis Davis CA USADepartment of Plant Biology and Genome Center University of California, Davis Davis CA USADepartment of Plant Biology and Genome Center University of California, Davis Davis CA USADepartment of Plant Sciences University of California, Davis Davis CA USADepartment of Plant Biology and Genome Center University of California, Davis Davis CA USAAbstract Plant metabolism is more complex relative to individual microbes. In single‐celled microbes, transcriptional regulation by single transcription factors (TFs) is sufficient to shift primary metabolism. Corresponding genome‐level transcriptional regulatory maps of metabolism reveal the underlying design principles responsible for these shifts as a model in which master regulators largely coordinate specific metabolic pathways. Plant primary and specialized metabolism occur within innumerable cell types, and their reactions shift depending on internal and external cues. Given the importance of plants and their metabolites in providing humanity with food, fiber, and medicine, we set out to develop a genome‐scale transcriptional regulatory map of Arabidopsis metabolic genes. A comprehensive set of protein–DNA interactions between Arabidopsis thaliana TFs and gene promoters in primary and specialized metabolic pathways were mapped. To demonstrate the utility of this resource, we identified and functionally validated regulators of the tricarboxylic acid (TCA) cycle. The resulting network suggests that plant metabolic design principles are distinct from those of microbes. Instead, metabolism appears to be transcriptionally coordinated via developmental‐ and stress‐conditional processes that can coordinate across primary and specialized metabolism. These data represent the most comprehensive resource of interactions between TFs and metabolic genes in plants.https://doi.org/10.15252/msb.202110625CCPs central carbon promotersGSL glucosinolateTF transcription factorY1H yeast one‐hybrid
spellingShingle Michelle Tang
Baohua Li
Xue Zhou
Tayah Bolt
Jia Jie Li
Neiman Cruz
Allison Gaudinier
Richard Ngo
Caitlin Clark‐Wiest
Daniel J Kliebenstein
Siobhan M Brady
A genome‐scale TF–DNA interaction network of transcriptional regulation of Arabidopsis primary and specialized metabolism
Molecular Systems Biology
CCPs central carbon promoters
GSL glucosinolate
TF transcription factor
Y1H yeast one‐hybrid
title A genome‐scale TF–DNA interaction network of transcriptional regulation of Arabidopsis primary and specialized metabolism
title_full A genome‐scale TF–DNA interaction network of transcriptional regulation of Arabidopsis primary and specialized metabolism
title_fullStr A genome‐scale TF–DNA interaction network of transcriptional regulation of Arabidopsis primary and specialized metabolism
title_full_unstemmed A genome‐scale TF–DNA interaction network of transcriptional regulation of Arabidopsis primary and specialized metabolism
title_short A genome‐scale TF–DNA interaction network of transcriptional regulation of Arabidopsis primary and specialized metabolism
title_sort genome scale tf dna interaction network of transcriptional regulation of arabidopsis primary and specialized metabolism
topic CCPs central carbon promoters
GSL glucosinolate
TF transcription factor
Y1H yeast one‐hybrid
url https://doi.org/10.15252/msb.202110625
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