Reactive electrophilic oxylipins trigger a heat stress-like response through HSFA1 transcription factors

Muench, Miriam; Hsin, Chih-Hsuan; Ferber, Elena; Berger, Susanne; Mueller, Martin J.

doi:10.1093/jxb/erw376

Cited by 23 publications

(23 citation statements)

References 41 publications

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“…Downregulation of H 2 O 2 signalling in HL-treated pgr5 plants reiterates the signalling role of PSI and stromal factor(s) independently of the PQ redox state [ 48 , 61 ], which is similarly over-reduced in both pgr5 and npq4 mutants in HL ( figure 2 c ; [ 21 ]). Under-production of H 2 O 2 and the altered reduction state of the chloroplast likely impair many redox-regulated signalling pathways that operate through reduction of signalling intermediates, such as TGA transcription factors that regulate detoxification networks [ 31 , 62 ] or nonexpressor of pathogenesis-related 1 (NPR1) required for pathogenesis response (reviewed in [ 63 ]).…”

Section: Discussionmentioning

confidence: 99%

Interaction between photosynthetic electron transport and chloroplast sinks triggers protection and signalling important for plant productivity

Gollan¹,

Lima‐Melo²,

Tiwari³

et al. 2017

Phil. Trans. R. Soc. B

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The photosynthetic light reactions provide energy that is consumed and stored in electron sinks, the products of photosynthesis. A balance between light reactions and electron consumption in the chloroplast is vital for plants, and is protected by several photosynthetic regulation mechanisms. Photosystem I (PSI) is particularly susceptible to photoinhibition when these factors become unbalanced, which can occur in low temperatures or in high light. In this study we used the pgr5 Arabidopsis mutant that lacks ΔpH-dependent regulation of photosynthetic electron transport as a model to study the consequences of PSI photoinhibition under high light. We found that PSI damage severely inhibits carbon fixation and starch accumulation, and attenuates enzymatic oxylipin synthesis and chloroplast regulation of nuclear gene expression after high light stress. This work shows that modifications to regulation of photosynthetic light reactions, which may be designed to improve yield in crop plants, can negatively impact metabolism and signalling, and thereby threaten plant growth and stress tolerance.This article is part of the themed issue ‘Enhancing photosynthesis in crop plants: targets for improvement’.

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Section: Discussionmentioning

confidence: 99%

Interaction between photosynthetic electron transport and chloroplast sinks triggers protection and signalling important for plant productivity

Gollan¹,

Lima‐Melo²,

Tiwari³

et al. 2017

Phil. Trans. R. Soc. B

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“…In Arabidopsis, oxidized lipids are produced enzymatically through the action of lipoxygenase as well as non-enzymatically through the action of ROS [ 19 ]. Similar to ROS, oxidized lipids may act as signaling molecules that initiate stress responses in plants [ 20 – 24 ]. Earlier studies have shown that triacylglycerols (TAGs) are accumulated under HT stress [ 25 ]; however, the changes in the saturation index of these TAG under HT stress are not known.…”

Section: Introductionmentioning

confidence: 99%

Decreased photosynthetic rate under high temperature in wheat is due to lipid desaturation, oxidation, acylation, and damage of organelles

et al. 2018

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BackgroundHigh temperature is a major abiotic stress that limits wheat (Triticum aestivum L.) productivity. Variation in levels of a wide range of lipids, including stress-related molecular species, oxidative damage, cellular organization and ultrastructural changes were analyzed to provide an integrated view of the factors that underlie decreased photosynthetic rate under high temperature stress. Wheat plants of cultivar Chinese Spring were grown at optimum temperatures (25/15 °C, maximum/minimum) until the onset of the booting stage. Thereafter, plants were exposed to high temperature (35/25 °C) for 16 d.ResultsCompared with optimum temperature, a lower photosynthetic rate was observed at high temperature which is an interplay between thylakoid membrane damage, thylakoid membrane lipid composition, oxidative damage of cell organelle, and stomatal and non-stomatal limitations. Triacylglycerol levels were higher under high temperature stress. Polar lipid fatty acyl unsaturation was lower at high temperature, while triacylglycerol unsaturation was the same at high temperature and optimum temperature. The changes in lipid species indicates increases in activities of desaturating, oxidizing, glycosylating and acylating enzymes under high temperature stress. Cumulative effect of high temperature stress led to generation of reactive oxygen species, cell organelle and membrane damage, and reduced antioxidant enzyme activity, and imbalance between reactive oxygen species and antioxidant defense system.ConclusionsTaken together with recent findings demonstrating that reactive oxygen species are formed from and are removed by thylakoid lipids, the data suggest that reactive oxygen species production, reactive oxygen species removal, and changes in lipid metabolism contribute to decreased photosynthetic rate under high temperature stress.Electronic supplementary materialThe online version of this article (10.1186/s12870-018-1263-z) contains supplementary material, which is available to authorized users.

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“…Indeed, several ITCs (Hara et al, 2010) and structurally different RES oxylipins (Mueller et al, 2008;Muench et al, 2016) have been shown to induce expression of heat shock and detoxification genes at low concentrations while spraying higher concentrations were highly toxic. The magnitude of gene induction and cell death varied when different ITCs were tested.…”

Section: Introductionmentioning

confidence: 99%

Chemical Priming by Isothiocyanates Protects Against Intoxication by Products of the Mustard Oil Bomb

et al. 2020

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In Brassicaceae, tissue damage triggers the mustard oil bomb i.e., activates the degradation of glucosinolates by myrosinases leading to a rapid accumulation of isothiocyanates at the site of damage. Isothiocyanates are reactive electrophilic species (RES) known to covalently bind to thiols in proteins and glutathione, a process that is not only toxic to herbivores and microbes but can also cause cell death of healthy plant tissues. Previously, it has been shown that subtoxic isothiocyanate concentrations can induce transcriptional reprogramming in intact plant cells. Glutathione depletion by RES leading to breakdown of the redox potential has been proposed as a central and common RES signal transduction mechanism. Using transcriptome analyses, we show that after exposure of Arabidopsis seedlings (grown in liquid culture) to subtoxic concentrations of sulforaphane hundreds of genes were regulated without depletion of the cellular glutathione pool. Heat shock genes were among the most highly up-regulated genes and this response was found to be dependent on the canonical heat shock factors A1 (HSFA1). HSFA1-deficient plants were more sensitive to isothiocyanates than wild type plants. Moreover, pretreatment of Arabidopsis seedlings with subtoxic concentrations of isothiocyanates increased resistance against exposure to toxic levels of isothiocyanates and, hence, may reduce the autotoxicity of the mustard oil bomb by inducing cell protection mechanisms.

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Reactive electrophilic oxylipins trigger a heat stress-like response through HSFA1 transcription factors

Abstract: HighlightElectrophilic oxylipins trigger a heat-shock-like response in the absence of heat through the canonical heat-shock transcription factor A1, thereby helping to cope with stresses associated with protein damage.

Cited by 23 publications

References 41 publications

Interaction between photosynthetic electron transport and chloroplast sinks triggers protection and signalling important for plant productivity

Interaction between photosynthetic electron transport and chloroplast sinks triggers protection and signalling important for plant productivity

Decreased photosynthetic rate under high temperature in wheat is due to lipid desaturation, oxidation, acylation, and damage of organelles

Chemical Priming by Isothiocyanates Protects Against Intoxication by Products of the Mustard Oil Bomb

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