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H2S regulates low oxygen signaling via integration with the unfolded protein response in Arabidopsis thaliana

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Abstract

Purpose

Hydrogen sulfide (H2S) is an important signaling molecule in prokaryotes and eukaryotes. In higher plants, H2S regulates different processes throughout development and stress responses. Here, we investigated the underlying mechanism of H2S in modulating hypoxia response signaling in Arabidopsis.

Methods

DAB (3,3-diaminobenzidine) and fluorescent probes were used to detect the accumulation of reactive oxygen species and H2S. Evans blue staining was conducted to observe the cell death. Quantitative RT-PCR was performed to measure the relative gene expression levels.

Results

Our data showed that endogenous H2S production was induced by anoxia and appropriate application of exogenous H2S mitigated the damage caused by submergence stress. Meanwhile, the histological staining, fluorescent microscope observation and molecular analysis demonstrated that H2S metabolism-related mutants oasa1 and lcddes1-1 accumulated different ROS levels and exhibited different low oxygen sensitivities compared with the wild type. In addition, we observed that ER stress response genes were up-regulated in wild type upon anoxia, and different ER stress response-related mutants ero1-2, ero1-3, ero2-1, ero2-2 and bzip28bzip60 were more sensitive to submergence or anoxia than wild type. Moreover, the exogenous H2S pretreatment could not alleviate submergence-induced leaf death in ero2-1 compared with wild type, indicating that hypoxia induced ER stress and activation of the unfolded protein response (UPR) signal pathway is important for plant hypoxia response.

Conclusion

Our work demonstrates that H2S regulates hypoxic stress response through the integration with UPR. This study provides new insights into H2S function during plant low oxygen stress response.

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Acknowledgements

We would like to thank Professor Dongping Lu for kindly providing the mutants ero1-2, ero1-3, ero2-1 and ero2-2. This work is supported by the National Thousand Youth Talents Plan to J. Cai; Talents Team Construction Fund of Northwestern Polytechnical University (NWPU) to J. Cai; the Fundamental Research Funds for the Central Universities (3102019JC007) to J. Cai and National Natural Science Foundation of China (NSFC) (31670254).

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Authors

Contributions

LZ, JC, XW and DAW conceived and designed the experiments. LZ and XG performed the experiments. LZ, XG and PZ produced the genotypes used in the current study and analyzed the data. LZ wrote the manuscript. All authors read and revised the final manuscript.

Corresponding author

Correspondence to Jing Cai.

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Conflict of interest

The authors have no conflicts of interest to declare.

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Responsible Editor: Gustavo Gabriel Striker.

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Zhou, L., Gao, X., Weits, D.A. et al. H2S regulates low oxygen signaling via integration with the unfolded protein response in Arabidopsis thaliana. Plant Soil 467, 531–547 (2021). https://doi.org/10.1007/s11104-021-05091-9

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  • DOI: https://doi.org/10.1007/s11104-021-05091-9

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