Chemical imaging reveals diverse functions of tricarboxylic acid metabolites in root growth and development

Abstract Understanding how plants grow is critical for agriculture and fundamental for illuminating principles of multicellular development. Here, we apply desorption electrospray ionization mass spectrometry imaging (DESI-MSI) to the chemical mapping of the developing maize root. This technique rev...

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Main Authors: Tao Zhang, Sarah E. Noll, Jesus T. Peng, Amman Klair, Abigail Tripka, Nathan Stutzman, Casey Cheng, Richard N. Zare, Alexandra J. Dickinson
Format: Article
Language:English
Published: Nature Portfolio 2023-05-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-023-38150-z
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author Tao Zhang
Sarah E. Noll
Jesus T. Peng
Amman Klair
Abigail Tripka
Nathan Stutzman
Casey Cheng
Richard N. Zare
Alexandra J. Dickinson
author_facet Tao Zhang
Sarah E. Noll
Jesus T. Peng
Amman Klair
Abigail Tripka
Nathan Stutzman
Casey Cheng
Richard N. Zare
Alexandra J. Dickinson
author_sort Tao Zhang
collection DOAJ
description Abstract Understanding how plants grow is critical for agriculture and fundamental for illuminating principles of multicellular development. Here, we apply desorption electrospray ionization mass spectrometry imaging (DESI-MSI) to the chemical mapping of the developing maize root. This technique reveals a range of small molecule distribution patterns across the gradient of stem cell differentiation in the root. To understand the developmental logic of these patterns, we examine tricarboxylic acid (TCA) cycle metabolites. In both Arabidopsis and maize, we find evidence that elements of the TCA cycle are enriched in developmentally opposing regions. We find that these metabolites, particularly succinate, aconitate, citrate, and α-ketoglutarate, control root development in diverse and distinct ways. Critically, the developmental effects of certain TCA metabolites on stem cell behavior do not correlate with changes in ATP production. These results present insights into development and suggest practical means for controlling plant growth.
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spelling doaj.art-5cc3e1f00a584ee393fc975ae7acb8062023-05-07T11:18:02ZengNature PortfolioNature Communications2041-17232023-05-0114111210.1038/s41467-023-38150-zChemical imaging reveals diverse functions of tricarboxylic acid metabolites in root growth and developmentTao Zhang0Sarah E. Noll1Jesus T. Peng2Amman Klair3Abigail Tripka4Nathan Stutzman5Casey Cheng6Richard N. Zare7Alexandra J. Dickinson8Cell and Developmental Biology, University of California San DiegoDepartment of Chemistry, Stanford UniversityCell and Developmental Biology, University of California San DiegoCell and Developmental Biology, University of California San DiegoCell and Developmental Biology, University of California San DiegoCell and Developmental Biology, University of California San DiegoCell and Developmental Biology, University of California San DiegoDepartment of Chemistry, Stanford UniversityCell and Developmental Biology, University of California San DiegoAbstract Understanding how plants grow is critical for agriculture and fundamental for illuminating principles of multicellular development. Here, we apply desorption electrospray ionization mass spectrometry imaging (DESI-MSI) to the chemical mapping of the developing maize root. This technique reveals a range of small molecule distribution patterns across the gradient of stem cell differentiation in the root. To understand the developmental logic of these patterns, we examine tricarboxylic acid (TCA) cycle metabolites. In both Arabidopsis and maize, we find evidence that elements of the TCA cycle are enriched in developmentally opposing regions. We find that these metabolites, particularly succinate, aconitate, citrate, and α-ketoglutarate, control root development in diverse and distinct ways. Critically, the developmental effects of certain TCA metabolites on stem cell behavior do not correlate with changes in ATP production. These results present insights into development and suggest practical means for controlling plant growth.https://doi.org/10.1038/s41467-023-38150-z
spellingShingle Tao Zhang
Sarah E. Noll
Jesus T. Peng
Amman Klair
Abigail Tripka
Nathan Stutzman
Casey Cheng
Richard N. Zare
Alexandra J. Dickinson
Chemical imaging reveals diverse functions of tricarboxylic acid metabolites in root growth and development
Nature Communications
title Chemical imaging reveals diverse functions of tricarboxylic acid metabolites in root growth and development
title_full Chemical imaging reveals diverse functions of tricarboxylic acid metabolites in root growth and development
title_fullStr Chemical imaging reveals diverse functions of tricarboxylic acid metabolites in root growth and development
title_full_unstemmed Chemical imaging reveals diverse functions of tricarboxylic acid metabolites in root growth and development
title_short Chemical imaging reveals diverse functions of tricarboxylic acid metabolites in root growth and development
title_sort chemical imaging reveals diverse functions of tricarboxylic acid metabolites in root growth and development
url https://doi.org/10.1038/s41467-023-38150-z
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