Progressive drought alters the root exudate metabolome and differentially activates metabolic pathways in cotton (Gossypium hirsutum)

Root exudates comprise various primary and secondary metabolites that are responsive to plant stressors, including drought. As increasing drought episodes are predicted with climate change, identifying shifts in the metabolome profile of drought-induced root exudation is necessary to understand the...

Full description

Bibliographic Details
Main Authors: Heng-An Lin, Harrison R. Coker, Julie A. Howe, Malak M. Tfaily, Elek M. Nagy, Sanjay Antony-Babu, Steve Hague, A. Peyton Smith
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-08-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1244591/full
_version_ 1797730990779531264
author Heng-An Lin
Harrison R. Coker
Julie A. Howe
Malak M. Tfaily
Elek M. Nagy
Sanjay Antony-Babu
Steve Hague
A. Peyton Smith
author_facet Heng-An Lin
Harrison R. Coker
Julie A. Howe
Malak M. Tfaily
Elek M. Nagy
Sanjay Antony-Babu
Steve Hague
A. Peyton Smith
author_sort Heng-An Lin
collection DOAJ
description Root exudates comprise various primary and secondary metabolites that are responsive to plant stressors, including drought. As increasing drought episodes are predicted with climate change, identifying shifts in the metabolome profile of drought-induced root exudation is necessary to understand the molecular interactions that govern the relationships between plants, microbiomes, and the environment, which will ultimately aid in developing strategies for sustainable agriculture management. This study utilized an aeroponic system to simulate progressive drought and recovery while non-destructively collecting cotton (Gossypium hirsutum) root exudates. The molecular composition of the collected root exudates was characterized by untargeted metabolomics using Fourier-Transform Ion Cyclotron Resonance Mass Spectrometry (FT-ICR MS) and mapped to the Kyoto Encyclopedia of Genes and Genomes (KEGG) databases. Over 700 unique drought-induced metabolites were identified throughout the water-deficit phase. Potential KEGG pathways and KEGG modules associated with the biosynthesis of flavonoid compounds, plant hormones (abscisic acid and jasmonic acid), and other secondary metabolites were highly induced under severe drought, but not at the wilting point. Additionally, the associated precursors of these metabolites, such as amino acids (phenylalanine and tyrosine), phenylpropanoids, and carotenoids, were also mapped. The potential biochemical transformations were further calculated using the data generated by FT-ICR MS. Under severe drought stress, the highest number of potential biochemical transformations, including methylation, ethyl addition, and oxidation/hydroxylation, were identified, many of which are known reactions in some of the mapped pathways. With the application of FT-ICR MS, we revealed the dynamics of drought-induced secondary metabolites in root exudates in response to drought, providing valuable information for drought-tolerance strategies in cotton.
first_indexed 2024-03-12T11:52:07Z
format Article
id doaj.art-fabfbbdaef904b43882aaf20eebdb0f5
institution Directory Open Access Journal
issn 1664-462X
language English
last_indexed 2024-03-12T11:52:07Z
publishDate 2023-08-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Plant Science
spelling doaj.art-fabfbbdaef904b43882aaf20eebdb0f52023-08-31T06:29:10ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-08-011410.3389/fpls.2023.12445911244591Progressive drought alters the root exudate metabolome and differentially activates metabolic pathways in cotton (Gossypium hirsutum)Heng-An Lin0Harrison R. Coker1Julie A. Howe2Malak M. Tfaily3Elek M. Nagy4Sanjay Antony-Babu5Steve Hague6A. Peyton Smith7Department of Soil and Crop Sciences, Texas A&M University and Texas A&M AgriLife Research, College Station, TX, United StatesDepartment of Soil and Crop Sciences, Texas A&M University and Texas A&M AgriLife Research, College Station, TX, United StatesDepartment of Soil and Crop Sciences, Texas A&M University and Texas A&M AgriLife Research, College Station, TX, United StatesDepartment of Environmental Science, University of Arizona, Tucson, AZ, United StatesDepartment of Plant Pathology and Microbiology, Texas A&M University and Texas A&M AgriLife Research, College Station, TX, United StatesDepartment of Plant Pathology and Microbiology, Texas A&M University and Texas A&M AgriLife Research, College Station, TX, United StatesDepartment of Soil and Crop Sciences, Texas A&M University and Texas A&M AgriLife Research, College Station, TX, United StatesDepartment of Soil and Crop Sciences, Texas A&M University and Texas A&M AgriLife Research, College Station, TX, United StatesRoot exudates comprise various primary and secondary metabolites that are responsive to plant stressors, including drought. As increasing drought episodes are predicted with climate change, identifying shifts in the metabolome profile of drought-induced root exudation is necessary to understand the molecular interactions that govern the relationships between plants, microbiomes, and the environment, which will ultimately aid in developing strategies for sustainable agriculture management. This study utilized an aeroponic system to simulate progressive drought and recovery while non-destructively collecting cotton (Gossypium hirsutum) root exudates. The molecular composition of the collected root exudates was characterized by untargeted metabolomics using Fourier-Transform Ion Cyclotron Resonance Mass Spectrometry (FT-ICR MS) and mapped to the Kyoto Encyclopedia of Genes and Genomes (KEGG) databases. Over 700 unique drought-induced metabolites were identified throughout the water-deficit phase. Potential KEGG pathways and KEGG modules associated with the biosynthesis of flavonoid compounds, plant hormones (abscisic acid and jasmonic acid), and other secondary metabolites were highly induced under severe drought, but not at the wilting point. Additionally, the associated precursors of these metabolites, such as amino acids (phenylalanine and tyrosine), phenylpropanoids, and carotenoids, were also mapped. The potential biochemical transformations were further calculated using the data generated by FT-ICR MS. Under severe drought stress, the highest number of potential biochemical transformations, including methylation, ethyl addition, and oxidation/hydroxylation, were identified, many of which are known reactions in some of the mapped pathways. With the application of FT-ICR MS, we revealed the dynamics of drought-induced secondary metabolites in root exudates in response to drought, providing valuable information for drought-tolerance strategies in cotton.https://www.frontiersin.org/articles/10.3389/fpls.2023.1244591/fullroot exudatesuntargeted metabolomicsdroughtFT-ICR MSupland cottonnondestructive sampling
spellingShingle Heng-An Lin
Harrison R. Coker
Julie A. Howe
Malak M. Tfaily
Elek M. Nagy
Sanjay Antony-Babu
Steve Hague
A. Peyton Smith
Progressive drought alters the root exudate metabolome and differentially activates metabolic pathways in cotton (Gossypium hirsutum)
Frontiers in Plant Science
root exudates
untargeted metabolomics
drought
FT-ICR MS
upland cotton
nondestructive sampling
title Progressive drought alters the root exudate metabolome and differentially activates metabolic pathways in cotton (Gossypium hirsutum)
title_full Progressive drought alters the root exudate metabolome and differentially activates metabolic pathways in cotton (Gossypium hirsutum)
title_fullStr Progressive drought alters the root exudate metabolome and differentially activates metabolic pathways in cotton (Gossypium hirsutum)
title_full_unstemmed Progressive drought alters the root exudate metabolome and differentially activates metabolic pathways in cotton (Gossypium hirsutum)
title_short Progressive drought alters the root exudate metabolome and differentially activates metabolic pathways in cotton (Gossypium hirsutum)
title_sort progressive drought alters the root exudate metabolome and differentially activates metabolic pathways in cotton gossypium hirsutum
topic root exudates
untargeted metabolomics
drought
FT-ICR MS
upland cotton
nondestructive sampling
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1244591/full
work_keys_str_mv AT henganlin progressivedroughtalterstherootexudatemetabolomeanddifferentiallyactivatesmetabolicpathwaysincottongossypiumhirsutum
AT harrisonrcoker progressivedroughtalterstherootexudatemetabolomeanddifferentiallyactivatesmetabolicpathwaysincottongossypiumhirsutum
AT julieahowe progressivedroughtalterstherootexudatemetabolomeanddifferentiallyactivatesmetabolicpathwaysincottongossypiumhirsutum
AT malakmtfaily progressivedroughtalterstherootexudatemetabolomeanddifferentiallyactivatesmetabolicpathwaysincottongossypiumhirsutum
AT elekmnagy progressivedroughtalterstherootexudatemetabolomeanddifferentiallyactivatesmetabolicpathwaysincottongossypiumhirsutum
AT sanjayantonybabu progressivedroughtalterstherootexudatemetabolomeanddifferentiallyactivatesmetabolicpathwaysincottongossypiumhirsutum
AT stevehague progressivedroughtalterstherootexudatemetabolomeanddifferentiallyactivatesmetabolicpathwaysincottongossypiumhirsutum
AT apeytonsmith progressivedroughtalterstherootexudatemetabolomeanddifferentiallyactivatesmetabolicpathwaysincottongossypiumhirsutum