Modulation of Energy Metabolism Is Important for Low-Oxygen Stress Adaptation in Brassicaceae Species

Low-oxygen stress, mainly caused by soil flooding, is a serious abiotic stress affecting crop productivity worldwide. To understand the mechanisms of low-oxygen stress responses and adaptation of plants, we characterized and compared low-oxygen responses in six species with different accessions of t...

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Published in:International Journal of Molecular Sciences
Main Authors: Ji-Hye Hwang, Si-in Yu, Byeong-ha Lee, Dong-Hee Lee
Format: Text
Language:English
Published: Multidisciplinary Digital Publishing Institute 2020
Subjects:
Online Access:https://doi.org/10.3390/ijms21051787
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spelling ftmdpi:oai:mdpi.com:/1422-0067/21/5/1787/ 2023-08-20T04:09:28+02:00 Modulation of Energy Metabolism Is Important for Low-Oxygen Stress Adaptation in Brassicaceae Species Ji-Hye Hwang Si-in Yu Byeong-ha Lee Dong-Hee Lee agris 2020-03-05 application/pdf https://doi.org/10.3390/ijms21051787 EN eng Multidisciplinary Digital Publishing Institute Molecular Plant Sciences https://dx.doi.org/10.3390/ijms21051787 https://creativecommons.org/licenses/by/4.0/ International Journal of Molecular Sciences; Volume 21; Issue 5; Pages: 1787 low oxygen hypoxia energy metabolism Brassicaceae gene set enrichment analysis (GSEA) Text 2020 ftmdpi https://doi.org/10.3390/ijms21051787 2023-07-31T23:11:50Z Low-oxygen stress, mainly caused by soil flooding, is a serious abiotic stress affecting crop productivity worldwide. To understand the mechanisms of low-oxygen stress responses and adaptation of plants, we characterized and compared low-oxygen responses in six species with different accessions of the Brassicaceae family. Based on the growth and survival responses to submergence or low-oxygen condition, these accessions could be divided into three groups: (i) Highly tolerant species (Rorippa islandica and Arabis stelleri); (ii) moderately tolerant species (Arabidopsis thaliana [esk-1, Ler, Ws and Col-0 ecotype]); and (iii) intolerant species (Thlaspi arvense, Thellungiella salsuginea [Shandong and Yukon ecotype], and Thellungiella parvula). Gene expression profiling using Operon Arabidopsis microarray was carried out with RNA from roots of A. thaliana (Col-0), A. stelleri, R. islandica, and T. salsuginea (Shandong) treated with low-oxygen stress (0.1% O2/99.9% N2) for 0, 1, 3, 8, 24, and 72 h. We performed a comparative analysis of the gene expression profiles using the gene set enrichment analysis (GSEA) method. Our comparative analysis suggested that under low-oxygen stress each species distinctively reconfigures the energy metabolic pathways including sucrose–starch metabolism, glycolysis, fermentation and nitrogen metabolism, tricarboxylic acid flow, and fatty acid degradation via beta oxidation and glyoxylate cycle. In A. thaliana, a moderately tolerant species, the dynamical reconfiguration of energy metabolisms occurred in the early time points of low-oxygen treatment, but the energy reconfiguration in the late time points was not as dynamic as in the early time points. Highly tolerant A. stelleri appeared to have high photosynthesis capacity that could produce more O2 and in turn additional ATP energy to cope with energy depletion caused by low-oxygen stress. R. islandica seemed to retain some ATP energy produced by anaerobic energy metabolism during a prolonged period of low-oxygen conditions. ... Text Rorippa islandica Yukon MDPI Open Access Publishing Yukon International Journal of Molecular Sciences 21 5 1787
institution Open Polar
collection MDPI Open Access Publishing
op_collection_id ftmdpi
language English
topic low oxygen
hypoxia
energy metabolism
Brassicaceae
gene set enrichment analysis (GSEA)
spellingShingle low oxygen
hypoxia
energy metabolism
Brassicaceae
gene set enrichment analysis (GSEA)
Ji-Hye Hwang
Si-in Yu
Byeong-ha Lee
Dong-Hee Lee
Modulation of Energy Metabolism Is Important for Low-Oxygen Stress Adaptation in Brassicaceae Species
topic_facet low oxygen
hypoxia
energy metabolism
Brassicaceae
gene set enrichment analysis (GSEA)
description Low-oxygen stress, mainly caused by soil flooding, is a serious abiotic stress affecting crop productivity worldwide. To understand the mechanisms of low-oxygen stress responses and adaptation of plants, we characterized and compared low-oxygen responses in six species with different accessions of the Brassicaceae family. Based on the growth and survival responses to submergence or low-oxygen condition, these accessions could be divided into three groups: (i) Highly tolerant species (Rorippa islandica and Arabis stelleri); (ii) moderately tolerant species (Arabidopsis thaliana [esk-1, Ler, Ws and Col-0 ecotype]); and (iii) intolerant species (Thlaspi arvense, Thellungiella salsuginea [Shandong and Yukon ecotype], and Thellungiella parvula). Gene expression profiling using Operon Arabidopsis microarray was carried out with RNA from roots of A. thaliana (Col-0), A. stelleri, R. islandica, and T. salsuginea (Shandong) treated with low-oxygen stress (0.1% O2/99.9% N2) for 0, 1, 3, 8, 24, and 72 h. We performed a comparative analysis of the gene expression profiles using the gene set enrichment analysis (GSEA) method. Our comparative analysis suggested that under low-oxygen stress each species distinctively reconfigures the energy metabolic pathways including sucrose–starch metabolism, glycolysis, fermentation and nitrogen metabolism, tricarboxylic acid flow, and fatty acid degradation via beta oxidation and glyoxylate cycle. In A. thaliana, a moderately tolerant species, the dynamical reconfiguration of energy metabolisms occurred in the early time points of low-oxygen treatment, but the energy reconfiguration in the late time points was not as dynamic as in the early time points. Highly tolerant A. stelleri appeared to have high photosynthesis capacity that could produce more O2 and in turn additional ATP energy to cope with energy depletion caused by low-oxygen stress. R. islandica seemed to retain some ATP energy produced by anaerobic energy metabolism during a prolonged period of low-oxygen conditions. ...
format Text
author Ji-Hye Hwang
Si-in Yu
Byeong-ha Lee
Dong-Hee Lee
author_facet Ji-Hye Hwang
Si-in Yu
Byeong-ha Lee
Dong-Hee Lee
author_sort Ji-Hye Hwang
title Modulation of Energy Metabolism Is Important for Low-Oxygen Stress Adaptation in Brassicaceae Species
title_short Modulation of Energy Metabolism Is Important for Low-Oxygen Stress Adaptation in Brassicaceae Species
title_full Modulation of Energy Metabolism Is Important for Low-Oxygen Stress Adaptation in Brassicaceae Species
title_fullStr Modulation of Energy Metabolism Is Important for Low-Oxygen Stress Adaptation in Brassicaceae Species
title_full_unstemmed Modulation of Energy Metabolism Is Important for Low-Oxygen Stress Adaptation in Brassicaceae Species
title_sort modulation of energy metabolism is important for low-oxygen stress adaptation in brassicaceae species
publisher Multidisciplinary Digital Publishing Institute
publishDate 2020
url https://doi.org/10.3390/ijms21051787
op_coverage agris
geographic Yukon
geographic_facet Yukon
genre Rorippa islandica
Yukon
genre_facet Rorippa islandica
Yukon
op_source International Journal of Molecular Sciences; Volume 21; Issue 5; Pages: 1787
op_relation Molecular Plant Sciences
https://dx.doi.org/10.3390/ijms21051787
op_rights https://creativecommons.org/licenses/by/4.0/
op_doi https://doi.org/10.3390/ijms21051787
container_title International Journal of Molecular Sciences
container_volume 21
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