Abstract
Abiotic stresses cause oxidative damage in plants. Here, we demonstrate that foliar application of an extract from the seaweed Ascophyllum nodosum, SuperFifty (SF), largely prevents paraquat (PQ)-induced oxidative stress in Arabidopsis thaliana. While PQ-stressed plants develop necrotic lesions, plants pre-treated with SF (i.e., primed plants) were unaffected by PQ. Transcriptome analysis revealed induction of reactive oxygen species (ROS) marker genes, genes involved in ROS-induced programmed cell death, and autophagy-related genes after PQ treatment. These changes did not occur in PQ-stressed plants primed with SF. In contrast, upregulation of several carbohydrate metabolism genes, growth, and hormone signaling as well as antioxidant-related genes were specific to SF-primed plants. Metabolomic analyses revealed accumulation of the stress-protective metabolite maltose and the tricarboxylic acid cycle intermediates fumarate and malate in SF-primed plants. Lipidome analysis indicated that those lipids associated with oxidative stress-induced cell death and chloroplast degradation, such as triacylglycerols (TAGs), declined upon SF priming. Our study demonstrated that SF confers tolerance to PQ-induced oxidative stress in A. thaliana, an effect achieved by modulating a range of processes at the transcriptomic, metabolic, and lipid levels.
Highlights
Oxidative stress in plants occurs as a consequence of many abiotic stresses including extreme temperatures, drought, salinity, osmotic stress, and pollutants [1,2,3,4,5].Abiotic stress-induced oxidative stress, manifested as an increased production of reactive oxygen species (ROS), has detrimental effects on plant growth, inhibits photosynthesis, leads to cell damage, and, in the most severe cases, results in the activation of programmed cell death [6]
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Summary
Oxidative stress in plants occurs as a consequence of many abiotic stresses including extreme temperatures, drought, salinity, osmotic stress, and pollutants (e.g., heavy metals or herbicides) [1,2,3,4,5].Abiotic stress-induced oxidative stress, manifested as an increased production of reactive oxygen species (ROS), has detrimental effects on plant growth, inhibits photosynthesis, leads to cell damage, and, in the most severe cases, results in the activation of programmed cell death [6]. Application of hydrogen peroxide (H2O2) at low doses can lead to tolerance against oxidative stress induced during chilling, high light, and toxicity due to the presence of heavy metals and pathogens in many plant species [5,16,17,18,19,20]. Molecular priming is similar to the process of acclimation, where application of a mild stress, for example, at a low temperature can protect plants against subsequent, more severe stress events (e.g., chilling/freezing) [3,4]. Both molecular priming and acclimation alter transcriptomes and metabolomes, resulting in molecular re-adjustments that are necessary and sufficient to provide stress protection [21]. Not deeply studied yet, a re-adjustment of the lipidome is an important part of the metabolome that captures the entirety of lipids in a biological system [22,23]
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