Elucidating Drought-Tolerance Mechanisms in Plant Roots through 1H NMR Metabolomics in Parallel with MALDI-MS, and NanoSIMS Imaging Techniques

Linnea K. Honeker; Gina A. Hildebrand; Jane D. Fudyma; L. Erik Daber; David Hoyt; Sarah E. Flowers; Juliana Gil-Loaiza; Angelika Kübert; Ines Bamberger; Christopher R. Anderton; John Cliff; Sarah Leichty; Roya AminiTabrizi; Jürgen Kreuzwieser; Lingling Shi; Xuejuan Bai; Dusan Velickovic; Michaela A. Dippold; S. Nemiah Ladd; Christiane Werner; Laura K. Meredith; Malak M. Tfaily

doi:10.1021/acs.est.1c06772

Elucidating Drought-Tolerance Mechanisms in Plant Roots through ¹H NMR Metabolomics in Parallel with MALDI-MS, and NanoSIMS Imaging Techniques

Linnea K. Honeker, Gina A. Hildebrand, Jane D. Fudyma, L. Erik Daber, David Hoyt, Sarah E. Flowers, Juliana Gil-Loaiza, Angelika Kübert, Ines Bamberger, Christopher R. Anderton, John Cliff, Sarah Leichty, Roya AminiTabrizi, Jürgen Kreuzwieser, Lingling Shi, Xuejuan Bai, Dusan Velickovic, Michaela A. Dippold, S. Nemiah Ladd, Christiane WernerLaura K. Meredith, Malak M. Tfaily

Applied Materials Analysis

Research output: Contribution to journal › Article › peer-review

22 Scopus citations

Abstract

As direct mediators between plants and soil, roots play an important role in metabolic responses to environmental stresses such as drought, yet these responses are vastly uncharacterized on a plant-specific level, especially for co-occurring species. Here, we aim to examine the effects of drought on root metabolic profiles and carbon allocation pathways of three tropical rainforest species by combining cutting-edge metabolomic and imaging technologies in an in situ position-specific ¹³C-pyruvate root-labeling experiment. Further, washed (rhizosphere-depleted) and unwashed roots were examined to test the impact of microbial presence on root metabolic pathways. Drought had a species-specific impact on the metabolic profiles and spatial distribution in Piper sp. and Hibiscus rosa sinensis roots, signifying different defense mechanisms; Piper sp. enhanced root structural defense via recalcitrant compounds including lignin, while H. rosa sinensis enhanced biochemical defense via secretion of antioxidants and fatty acids. In contrast, Clitoria fairchildiana, a legume tree, was not influenced as much by drought but rather by rhizosphere presence where carbohydrate storage was enhanced, indicating a close association with symbiotic microbes. This study demonstrates how multiple techniques can be combined to identify how plants cope with drought through different drought-tolerance strategies and the consequences of such changes on below-ground organic matter composition.

Original language	English
Pages (from-to)	2021-2032
Number of pages	12
Journal	Environmental Science and Technology
Volume	56
Issue number	3
DOIs	https://doi.org/10.1021/acs.est.1c06772
State	Published - Feb 1 2022

Funding

A portion of this research was performed under the Facilities Integrating Collaborations for User Science (FICUS) exploratory effort and used resources at the US Department of Energy (DOE) Joint Genome Institute (proposal ID 1292415) and the Environmental Molecular Sciences Laboratory (proposal ID 50971), which are DOE Office of Science User Facilities. This research was supported, in part, by the European Research Council (ERC; Grant Number 647008) and the Department of Energy, Office of Science Biological and Environmental Research Grant (DE-SC0021349). L.H. was supported by Biosphere 2 through the office of the Senior Vice President for Research Innovation and Impact at the University of Arizona. The authors gratefully acknowledge financial support from the Philecology Foundation.

Keywords

abiotic plant stress
carbon cycle
drought
position-specific pyruvate labeling
tropical rainforest

Access to Document

10.1021/acs.est.1c06772

Cite this

Honeker, L. K., Hildebrand, G. A., Fudyma, J. D., Daber, L. E., Hoyt, D., Flowers, S. E., Gil-Loaiza, J., Kübert, A., Bamberger, I., Anderton, C. R., Cliff, J., Leichty, S., AminiTabrizi, R., Kreuzwieser, J., Shi, L., Bai, X., Velickovic, D., Dippold, M. A., Ladd, S. N., ... Tfaily, M. M. (2022). Elucidating Drought-Tolerance Mechanisms in Plant Roots through ¹H NMR Metabolomics in Parallel with MALDI-MS, and NanoSIMS Imaging Techniques. Environmental Science and Technology, 56(3), 2021-2032. https://doi.org/10.1021/acs.est.1c06772

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title = "Elucidating Drought-Tolerance Mechanisms in Plant Roots through 1H NMR Metabolomics in Parallel with MALDI-MS, and NanoSIMS Imaging Techniques",

abstract = "As direct mediators between plants and soil, roots play an important role in metabolic responses to environmental stresses such as drought, yet these responses are vastly uncharacterized on a plant-specific level, especially for co-occurring species. Here, we aim to examine the effects of drought on root metabolic profiles and carbon allocation pathways of three tropical rainforest species by combining cutting-edge metabolomic and imaging technologies in an in situ position-specific 13C-pyruvate root-labeling experiment. Further, washed (rhizosphere-depleted) and unwashed roots were examined to test the impact of microbial presence on root metabolic pathways. Drought had a species-specific impact on the metabolic profiles and spatial distribution in Piper sp. and Hibiscus rosa sinensis roots, signifying different defense mechanisms; Piper sp. enhanced root structural defense via recalcitrant compounds including lignin, while H. rosa sinensis enhanced biochemical defense via secretion of antioxidants and fatty acids. In contrast, Clitoria fairchildiana, a legume tree, was not influenced as much by drought but rather by rhizosphere presence where carbohydrate storage was enhanced, indicating a close association with symbiotic microbes. This study demonstrates how multiple techniques can be combined to identify how plants cope with drought through different drought-tolerance strategies and the consequences of such changes on below-ground organic matter composition.",

keywords = "abiotic plant stress, carbon cycle, drought, position-specific pyruvate labeling, tropical rainforest",

author = "Honeker, \{Linnea K.\} and Hildebrand, \{Gina A.\} and Fudyma, \{Jane D.\} and Daber, \{L. Erik\} and David Hoyt and Flowers, \{Sarah E.\} and Juliana Gil-Loaiza and Angelika K{\"u}bert and Ines Bamberger and Anderton, \{Christopher R.\} and John Cliff and Sarah Leichty and Roya AminiTabrizi and J{\"u}rgen Kreuzwieser and Lingling Shi and Xuejuan Bai and Dusan Velickovic and Dippold, \{Michaela A.\} and Ladd, \{S. Nemiah\} and Christiane Werner and Meredith, \{Laura K.\} and Tfaily, \{Malak M.\}",

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Honeker, LK, Hildebrand, GA, Fudyma, JD, Daber, LE, Hoyt, D, Flowers, SE, Gil-Loaiza, J, Kübert, A, Bamberger, I, Anderton, CR, Cliff, J, Leichty, S, AminiTabrizi, R, Kreuzwieser, J, Shi, L, Bai, X, Velickovic, D, Dippold, MA, Ladd, SN, Werner, C, Meredith, LK & Tfaily, MM 2022, 'Elucidating Drought-Tolerance Mechanisms in Plant Roots through ¹H NMR Metabolomics in Parallel with MALDI-MS, and NanoSIMS Imaging Techniques', Environmental Science and Technology, vol. 56, no. 3, pp. 2021-2032. https://doi.org/10.1021/acs.est.1c06772

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AU - Fudyma, Jane D.

AU - Daber, L. Erik

AU - Hoyt, David

AU - Flowers, Sarah E.

AU - Gil-Loaiza, Juliana

AU - Kübert, Angelika

AU - Bamberger, Ines

AU - Anderton, Christopher R.

AU - Cliff, John

AU - Leichty, Sarah

AU - AminiTabrizi, Roya

AU - Kreuzwieser, Jürgen

AU - Shi, Lingling

AU - Bai, Xuejuan

AU - Velickovic, Dusan

AU - Dippold, Michaela A.

AU - Ladd, S. Nemiah

AU - Werner, Christiane

AU - Meredith, Laura K.

AU - Tfaily, Malak M.

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AB - As direct mediators between plants and soil, roots play an important role in metabolic responses to environmental stresses such as drought, yet these responses are vastly uncharacterized on a plant-specific level, especially for co-occurring species. Here, we aim to examine the effects of drought on root metabolic profiles and carbon allocation pathways of three tropical rainforest species by combining cutting-edge metabolomic and imaging technologies in an in situ position-specific 13C-pyruvate root-labeling experiment. Further, washed (rhizosphere-depleted) and unwashed roots were examined to test the impact of microbial presence on root metabolic pathways. Drought had a species-specific impact on the metabolic profiles and spatial distribution in Piper sp. and Hibiscus rosa sinensis roots, signifying different defense mechanisms; Piper sp. enhanced root structural defense via recalcitrant compounds including lignin, while H. rosa sinensis enhanced biochemical defense via secretion of antioxidants and fatty acids. In contrast, Clitoria fairchildiana, a legume tree, was not influenced as much by drought but rather by rhizosphere presence where carbohydrate storage was enhanced, indicating a close association with symbiotic microbes. This study demonstrates how multiple techniques can be combined to identify how plants cope with drought through different drought-tolerance strategies and the consequences of such changes on below-ground organic matter composition.

KW - abiotic plant stress

KW - carbon cycle

KW - drought

KW - position-specific pyruvate labeling

KW - tropical rainforest

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