Abstract
Key message
Hydrogen sulfide closed Arabidopsis thaliana stomata by increasing the transcription of melatonin-producing enzymes and the post-translational modification levels to combat osmotic stress.
Abstract
Hydrogen sulfide (H2S) and melatonin (MEL) reportedly have similar functions in many aspects of plant growth, development and stress response. They regulate stomatal movement and enhance drought resistance. However, their physiological relationship is not well understood. Here, their crosstalk involved in osmotic stress resistance in Arabidopsis thaliana was studied. Exogenous H2S and MEL closed stomata under normal or osmotic stress conditions and increased the relative water contents of plants under osmotic stress conditions. At the same time, exogenous H2S and MEL responded to osmotic stress by increasing the content of proline and soluble sugar, and reducing malondialdehyde (MDA) content and relative conductivity. Using mutants in the MEL-associated production of serotonin N-acetyltransferase (snat), caffeic acid O-methyltransferase (comt1) and N-acetylserotonin methyltransferase (asmt), we determined that H2S was partially dependent on MEL to close stomata. Additionally, the overexpression of ASMT promoted stomatal closure. Exogenous H2S increased the transcription levels of SNAT, ASMT and COMT1. Furthermore, exogenous H2S treatments increased the endogenous MEL content significantly. At the post-translational level, H2S sulfhydrated the SNAT and ASMT, but not COMT1, enzymes associated with MEL production. Thus, H2S appeared to promote stomatal closure in response to osmotic stress by increasing the transcription levels of MEL synthesis-related genes and the sulfhydryl modification of the encoded enzymes. These results increased our understanding of H2S and MEL functions and interactions under osmotic stress conditions.
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Acknowledgements
This work was supported by the Research Project Supported by Shanxi Scholarship Council of China (No. 2020-014 to Jin Z), National Natural Science Foundation of China (No. 31972428 to Pei Y) and Shanxi Province Excellent Talents Science and Technology Innovation Project (No. 2018050211016 to Jin Z).
Funding
This work was supported by the Research Project Supported by Shanxi Scholarship Council of China (No. 2020-014 to Jin Z), National Natural Science Foundation of China (No. 31972428 to Pei Y) and Shanxi Province Excellent Talents Science and Technology Innovation Project (No. 2018050211016 to Jin Z).
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YP and ZJ designed the experiments. ZW and YM performed the experiments and wrote the manuscript. XH, JY, DZ analyzed data. All authors read and approved the final manuscript.
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299_2021_2813_MOESM2_ESM.tif
Supplementary file2 Fig. S2 Expression analysis of LCD, DES1, SNAT, ASMT, COMT1. Total RNA was extracted from 4-week-old plants treated with dehydration for 0, 0.5, 1, 3, 6, 9,12 h. Data are represented as the mean ± SE of three biological repeats. Bars with different letters are significantly different among treatments (P < 0.05) (TIF 55891 KB)
299_2021_2813_MOESM3_ESM.tif
Supplementary file3 Fig. S3 The effect of stomatal aperture under different concentrations of melatonin treatment. Lower epidermis of rosette leaf from the col. was used. The samples were pre-incubated at 23 ℃ under light for 2 h. It was then incubated with 0, 10, 20, 50, 100, 150 μM MEL for 6 h before stomatal pore measurement. Observe the stomate under an optical microscope (200×) (bars=5 μm). Data between the different treament were measured from at least 60 guard cells. Error bars indicate the standard error of three biological repeats and different letters are significantly different among treatments (P < 0.05). (TIF 9872 KB)
299_2021_2813_MOESM5_ESM.docx
Supplementary file5 Table. S2 Relative water content data. The plants were weighed (M1) before the treatment and weighed (M2) after the different treatments. Then, the plants were placed at 110 ℃ for 30 min and dried at 55℃ overnight until quality (M3) no longer changed, calculated relative water content (%). Data are represented as the mean ± SE of three biological repeats. Bars with different letters are significantly different among treatments (P < 0.05). (DOCX 19 KB)
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Wang, Z., Mu, Y., Hao, X. et al. H2S aids osmotic stress resistance by S-sulfhydration of melatonin production-related enzymes in Arabidopsis thaliana. Plant Cell Rep 41, 365–376 (2022). https://doi.org/10.1007/s00299-021-02813-2
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DOI: https://doi.org/10.1007/s00299-021-02813-2