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Jasmonic acid-induced hydrogen sulfide activates MEK1/2 in regulating the redox state of ascorbate in Arabidopsis thaliana leaves.

ABSTRACT: In this paper, we investigated the relationship between hydrogen sulfide (H2S) and mitogen-activated protein kinase kinase (MEK1/2) in jasmonic acid (JA)-regulated the redox state of ascorbate in the leaves of Arabidopsis thaliana. The results showed that JA significantly enhanced the phosphorylation level of MEK1/2, the production of endogenous H2S and the ratio of reduced ascorbate (AsA) to dehydroascorbate (DHA) (AsA/DHA) in wild type of A. thaliana (WT). However, there were no obvious effects of JA on above indicators in H2S synthetic mutant of A. thaliana (MT). H2S scavenger hypotaurine (HT) markedly reduced JA-induced the phosphorylation level of MEK1/2, AsA/DHA ratio and the production of endogenous H2S in WT. Application of H2S donor sodium hydrosulfide (NaHS) to JA-treated MT plants increased above indicators. Application of NaHS to (HT+JA)-treated MT plants did not reverse the effects of HT on above JA-induced indicators. MEK1/2 inhibitor PD98059 decreased JA-induced AsA/DHA ratio and the transcript levels and the activities of ascorbate peroxidase (APX), glutathione reductase (GR), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR) and L-galactono-1,4-lactone dehydrogenase (GalLDH) in WT. However, PD98059 had no effect on JA-induced the production of endogenous H2S in WT. Compared with Control-MT, there were no obvious effects of JA on the production of endogenous H2S, AsA/DHA ratio and the transcript levels and activities of above enzymes in MT. However, application of PD98059 reduced above JA-induced indicators except the production of endogenous H2S and DHA content in MT. Our results suggested that H2S activated MEK1/2 in JA-regulated AsA/DHA ratio in A. thaliana leaves through enzymes in ascorbate metabolism.

SUBMITTER: Shan C

PROVIDER: S-EPMC6619967 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Jasmonic acid-induced hydrogen sulfide activates MEK1/2 in regulating the redox state of ascorbate in Arabidopsis thaliana leaves.

Shan C C Sun H H Zhou Y Y Wang W W

Plant signaling & behavior 20190612 8

In this paper, we investigated the relationship between hydrogen sulfide (H2S) and mitogen-activated protein kinase kinase (MEK1/2) in jasmonic acid (JA)-regulated the redox state of ascorbate in the leaves of Arabidopsis thaliana. The results showed that JA significantly enhanced the phosphorylation level of MEK1/2, the production of endogenous H2S and the ratio of reduced ascorbate (AsA) to dehydroascorbate (DHA) (AsA/DHA) in wild type of A. thaliana (WT). H ...[more]

PMID: 31187685

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Project description:The aim of this study was to gain insight into the compartment-specific roles of ascorbate and glutathione in leaf senescence in Arabidopsis thaliana. The subcellular distribution of ascorbate, glutathione, and hydrogen peroxide (H2O2) was analyzed by transmission electron microscopy and correlated with the activity of antioxidative enzymes in wildtype plants and the ascorbate- and glutathione-deficient mutants vtc2-1 and pad2-1, respectively. Both mutants showed earlier and stronger senescence than the wildtype indicating the importance of a functioning ascorbate and glutathione cycle in the induction and regulation of senescence. Glutathione levels dropped drastically and up to 93 % in all cell compartments of wildtype plants and the vtc2-1 mutant within the first day of dark-induced senescence while ascorbate contents remained unchanged until the very end. Glutathione contents in mitochondria of pad2-1 mutants decreased more slowly over the first 7 days than compared to the other plants indicating an important role of glutathione in mitochondria in this mutant during senescence. The strongest decrease (84 %) of glutathione contents in wildtype plants at this time point was found in mitochondria indicating an important role of mitochondria for the induction of senescence and cell death events. Due to the general decrease of the antioxidative capacity, a strong accumulation of H2O2 was observed in cell walls, plastids, and the cytosol in all plants. Activities of glutathione reductase, dehydroascorbate reductase and catalase were strongly reduced while ascorbate peroxidase and monodehydroascorbate reductase were increased. The initial rapid drop of glutathione levels seemed to be the trigger for senescence, while ascorbate appeared to be the key factor in regulating senescence through controlling H2O2 levels by the oxidation of reduced ascorbate to monodehydroascorbate and the subsequent reduction to ascorbate by monodehydroascorbate reductase.

Project description:Hydrogen sulfide (H2S) has been shown to participate in various stress responses in plants, including drought, salinity, extreme temperatures, osmotic stress, and heavy metal stress. Manganese (Mn), as a necessary nutrient for plant growth, plays an important role in photosynthesis, growth, development, and enzymatic activation of plants. However, excessive Mn2+ in the soil can critically affect plant growth, particularly in acidic soil. In this study, the model plant Arabidopsis thaliana was used to explore the mechanism of H2S participation and alleviation of Mn stress. First, using wild-type Arabidopsis with excessive Mn2+ treatment, the following factors were increased: H2S content, the main H2S synthetase L-cysteine desulfhydrase enzyme (AtLCD) activity, and the expression level of the AtLCD gene. Further, using the wild-type, AtLCD deletion mutant (lcd) and overexpression lines (OE5 and OE32) as materials, the phenotype of Arabidopsis seedlings was observed by exogenous application of hydrogen sulfide donor sodium hydrosulfide (NaHS) and scavenger hypotaurine (HT) under excessive Mn2+ treatment. The results showed that NaHS can significantly alleviate the stress caused by Mn2+, whereas HT aggravates this stress. The lcd mutant is more sensitive to Mn stress than the wild type, and the overexpression lines are more resistant. Moreover, the mechanism of H2S alleviating Mn stress was determined. The Mn2+ content and the expression of the Mn transporter gene in the mutant were significantly higher than those of the wild-type and overexpression lines. The accumulation of reactive oxygen species was significantly reduced in NaHS-treated Arabidopsis seedlings and AtLCD overexpression lines, and the activities of various antioxidant enzymes (SOD, POD, CAT, APX) also significantly increased. In summary, H2S is involved in the response of Arabidopsis to Mn stress and may alleviate the inhibition of Mn stress on Arabidopsis seedling growth by reducing Mn2+ content, reducing reactive oxygen species content, and enhancing antioxidant enzyme activity. This study provides an important basis for further study of plant resistance to heavy metal stress.

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Jasmonic acid-induced hydrogen sulfide activates MEK1/2 in regulating the redox state of ascorbate in Arabidopsis thaliana leaves.

Publications

Jasmonic acid-induced hydrogen sulfide activates MEK1/2 in regulating the redox state of ascorbate in <i>Arabidopsis thaliana</i> leaves.

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