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Waterlogging tolerance rendered by oxylipin-mediated metabolic reprogramming in Arabidopsis.

ABSTRACT: Environmental stresses induce production of oxylipins synthesized by the two main biosynthetic branches, allene oxide synthase (AOS) and hydroperoxide lyase (HPL). Here, we investigate how waterlogging-mediated alteration of AOS- and HPL-derived metabolic profile results in modulation of central metabolism and ultimately enhanced tolerance to this environmental stress in Arabidopsis thaliana. Waterlogging leads to increased levels of AOS- and HPL-derived metabolites, and studies of genotypes lacking either one or both branches further support the key function of these oxylipins in waterlogging tolerance. Targeted quantitative metabolic profiling revealed oxylipin-dependent alterations in selected primary metabolites, and glycolytic and citric acid cycle intermediates, as well as a prominent shift in sucrose cleavage, hexose activation, the methionine salvage pathway, shikimate pathway, antioxidant system, and energy metabolism in genotypes differing in the presence of one or both functional branches of the oxylipin biosynthesis pathway. Interestingly, despite some distinct metabolic alterations caused specifically by individual branches, overexpression of HPL partially or fully alleviates the majority of altered metabolic profiles observed in AOS-depleted lines. Collectively, these data identify the key role of AOS- and HPL-derived oxylipins in altering central metabolism, and further provide a metabolic platform targeted at identification of gene candidates for enhancing plant tolerance to waterlogging.

SUBMITTER: Savchenko T

PROVIDER: S-EPMC6506769 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Waterlogging tolerance rendered by oxylipin-mediated metabolic reprogramming in Arabidopsis.

Savchenko Tatyana T Rolletschek Hardy H Heinzel Nicolas N Tikhonov Konstantin K Dehesh Katayoon K

Journal of experimental botany 20190501 10

Environmental stresses induce production of oxylipins synthesized by the two main biosynthetic branches, allene oxide synthase (AOS) and hydroperoxide lyase (HPL). Here, we investigate how waterlogging-mediated alteration of AOS- and HPL-derived metabolic profile results in modulation of central metabolism and ultimately enhanced tolerance to this environmental stress in Arabidopsis thaliana. Waterlogging leads to increased levels of AOS- and HPL-derived metabolites, and studies of genotypes lac ...[more]

PMID: 30854562

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Project description:Melatonin (MT), polyamines (PAs), and ethylene have been suggested to play key roles in plant growth and development in response to environmental abiotic stresses. However, the effect of melatonin on polyamine and ethylene metabolism under waterlogging stress has rarely been elucidated. The main purpose of this study was to investigate the effect of melatonin pretreatment on waterlogging stress in alfalfa. The experiment was arranged into four treatment groups control with water pretreatment (CK-MT), control with melatonin pretreatment (CK+MT), waterlogging pretreated with water (WL-MT) and waterlogging pretreated with melatonin (WL+MT), with three replications. Six-week-old alfalfa seedlings were pretreated with 100 μM melatonin and exposed to waterlogging stress for 10 days. Plant growth rate, different physiological characteristics, and gene expression level were measured. Results showed that waterlogging induced melatonin accumulation, and melatonin pretreatment increased endogenous MT levels for the control and water-logged plants. Waterlogging stress caused a significant reduction in plant growth, chlorophyll content, photochemical efficiency (Fv/Fm) and net photosynthetic rate (Pn), while also causing increased leaf electrolyte leakage (EL) and malondialdehyde (MDA) content. Pretreatment with melatonin alleviated the waterlogging-induced damage and reduction in plant growth, chlorophyll content, Fv/Fm and Pn. Waterlogging stress significantly increased leaf polyamines (Put, Spd, Spm) and ethylene levels, and the increased PAs and ethylene levels are coupled with higher metabolic enzymes and gene expressions. While pretreatment with melatonin further increased Put, Spd and Spm levels, it also decreased ethylene levels under waterlogging, and those increased PAs levels or decreased ethylene levels are regulated by the metabolic enzymes and gene expressions. The results in this study provide more comprehensive insight into the physiological and molecular mechanisms of melatonin-improved waterlogging tolerance in alfalfa. Furthermore, they suggested that melatonin improved waterlogging tolerance in alfalfa at least partially by reprogramming ethylene and PA biosynthesis, attributable to the increased PAs and decreased ethylene levels, which leads to more enhanced membrane stability and photosynthesis as well as less leaf senescence caused by ethylene.

Dataset Information

Waterlogging tolerance rendered by oxylipin-mediated metabolic reprogramming in Arabidopsis.

Publications

Waterlogging tolerance rendered by oxylipin-mediated metabolic reprogramming in Arabidopsis.

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