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H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses.

ABSTRACT: The production of H2O2 is critical for brassinosteroid (BR)- and abscisic acid (ABA)-induced stress tolerance in plants. In this study, the relationship between BR and ABA in the induction of H2O2 production and their roles in response to heat and paraquat (PQ) oxidative stresses were studied in tomato. Both BR and ABA induced increases in RBOH1 gene expression, NADPH oxidase activity, apoplastic H2O2 accumulation, and heat and PQ stress tolerance in wild-type plants. BR could only induced transient increases in these responses in the ABA biosynthetic mutant notabilis (not), whereas ABA induced strong and prolonged increases in these responses in the BR biosynthetic mutant d (^im) compared with wild-type plants. ABA levels were reduced in the BR biosynthetic mutant but could be elevated by exogenous BR. Silencing of RBOH1 compromised BR-induced apoplastic H2O2 production, ABA accumulation, and PQ stress responses; however, ABA-induced PQ stress responses were largely unchanged in the RBOH1-silenced plants. BR induces stress tolerance involving a positive feedback mechanism in which BR induces a rapid and transient H2O2 production by NADPH oxidase. The process in turn triggers increased ABA biosynthesis, leading to further increases in H2O2 production and prolonged stress tolerance. ABA induces H2O2 production in both the apoplastic and chloroplastic compartments.

SUBMITTER: Zhou J

PROVIDER: S-EPMC4112640 | biostudies-literature | 2014 Aug

REPOSITORIES: biostudies-literature

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H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses.

Zhou Jie J Wang Jian J Li Xin X Xia Xiao-Jian XJ Zhou Yan-Hong YH Shi Kai K Chen Zhixiang Z Yu Jing-Quan JQ

Journal of experimental botany 20140604 15

The production of H2O2 is critical for brassinosteroid (BR)- and abscisic acid (ABA)-induced stress tolerance in plants. In this study, the relationship between BR and ABA in the induction of H2O2 production and their roles in response to heat and paraquat (PQ) oxidative stresses were studied in tomato. Both BR and ABA induced increases in RBOH1 gene expression, NADPH oxidase activity, apoplastic H2O2 accumulation, and heat and PQ stress tolerance in wild-type plants. BR could only induced trans ...[more]

PMID: 24899077

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Project description:BackgroundHeat stress is a major abiotic stress affecting the growth and development of plants, including crop species. Plants have evolved various adaptive strategies to help them survive heat stress, including maintaining membrane stability, encoding heat shock proteins (HSPs) and ROS-scavenging enzymes, and inducing molecular chaperone signaling. Brassinosteroids (BRs) are phytohormones that regulate various aspects of plant development, which have been implicated also in plant responses to heat stress, and resistance to heat in Arabidopsis thaliana is enhanced by adding exogenous BR. Brassinazole resistant 1 (BZR1), a transcription factor and positive regulator of BR signal, controls plant growth and development by directly regulating downstream target genes. However, the molecular mechanism at the basis of BR-mediated heat stress response is poorly understood. Here, we report the identification of a new factor critical for BR-regulated heat stress tolerance.ResultsWe identified ERF49 in a genetic screen for proteins required for BR-regulated gene expression. We found that ERF49 is the direct target gene of BZR1 and that overexpressing ERF49 enhanced sensitivity of transgenic plants to heat stress. The transcription levels of heat shock factor HSFA2, heat stress-inducible gene DREB2A, and three heat shock protein (HSP) were significantly reduced under heat stress in ERF49-overexpressed transgenic plants. Transcriptional activity analysis in protoplast revealed that BZR1 inhibits ERF49 expression by binding to the promoter of ERF49. Our genetic analysis showed that dominant gain-of-function brassinazole resistant 1-1D mutant (bzr1-1D) exhibited lower sensitivity to heat stress compared with wild-type. Expressing ERF49-SRDX (a dominant repressor reporter of ERF49) in bzr1-1D significantly decreased the sensitivity of ERF49-SRDX/bzr1-1D transgenic plants to heat stress compared to bzr1-1D.ConclusionsOur data provide clear evidence that BR increases thermotolerance of plants by repressing the expression of ERF49 through BZR1, and this process is dependent on the expression of downstream heat stress-inducible genes. Taken together, our work reveals a novel molecular mechanism mediating plant response to high temperature stress.

Project description:BackgroundWheat embryo and endosperm play important roles in seed germination, seedling survival, and subsequent vegetative growth. ABA can positively regulate dormancy induction and negatively regulates seed germination at low concentrations, while low H2O2 concentrations promote seed germination of cereal plants. In this report, we performed the first integrative transcriptome analysis of wheat embryo and endosperm responses to ABA and H2O2 stresses.ResultsWe used the GeneChip® Wheat Genome Array to conduct a comparative transcriptome microarray analysis of the embryo and endosperm of elite Chinese bread wheat cultivar Zhengmai 9023 in response to ABA and H2O2 treatments during seed germination. Transcriptome profiling showed that after H2O2 and ABA treatments, the 64 differentially expressed genes in the embryo were closely related to DNA synthesis, CHO metabolism, hormone metabolism, and protein degradation, while 121 in the endosperm were involved mainly in storage reserves, transport, biotic and abiotic stresses, hormone metabolism, cell wall metabolism, signaling, and development. Scatter plot analysis showed that ABA treatment increased the similarity of regulated patterns between the two tissues, whereas H2O2 treatment decreased the global expression similarity. MapMan analysis provided a global view of changes in several important metabolism pathways (e.g., energy reserves mobilization, cell wall metabolism, and photosynthesis), as well as related functional groups (e.g., cellular processes, hormones, and signaling and transport) in the embryo and endosperm following exposure of seeds to ABA and H2O2 treatments during germination. Quantitative RT-PCR analysis was used to validate the expression patterns of nine differentially expressed genes.ConclusionsWheat seed germination involves regulation of a large number of genes involved in many functional groups. ABA/H2O2 can repress/promote seed germination by coordinately regulating related gene expression. Our results provide novel insights into the transcriptional regulation mechanisms of embryo and endosperm in response to ABA and H2O2 treatments during seed germination.

Dataset Information

H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses.

Publications

H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses.

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