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Hydrogen sulfide improves salt tolerance through persulfidation of PMA1 in Arabidopsis

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Abstract

Key message

A new interaction was found between PMA1 and GRF4. H2S promotes the interaction through persulfidated Cys446 of PMA1. H2S activates PMA1 to maintain K+/Na+ homeostasis through persulfidation under salt stress.

Abstract

Plasma membrane H+-ATPase (PMA) is a transmembrane transporter responsible for pumping protons, and its contribution to salt resistance is indispensable in plants. Hydrogen sulfide (H2S), a small signaling gas molecule, plays the important roles in facilitating adaptation of plants to salt stress. However, how H2S regulates PMA activity remains largely unclear. Here, we show a possible original mechanism for H2S to regulate PMA activity. PMA1, a predominant member in the PMA family of Arabidopsis, has a non-conservative persulfidated cysteine (Cys) residue (Cys446), which is exposed on the surface of PMA1 and located in cation transporter/ATPase domain. A new interaction of PMA1 and GENERAL REGULATORY FACTOR 4 (GRF4, belongs to the 14-3-3 protein family) was found by chemical crosslinking coupled with mass spectrometry (CXMS) in vivo. H2S-mediated persulfidation promoted the binding of PMA1 to GRF4. Further studies showed that H2S enhanced instantaneous H+ efflux and maintained K+/Na+ homeostasis under salt stress. In light of these findings, we suggest that H2S promotes the binding of PMA1 to GRF4 through persulfidation, and then activating PMA, thus improving the salt tolerance of Arabidopsis.

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The data supporting this study’s findings are available from the corresponding author upon reasonable request.

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Acknowledgements

This work was supported by the Shaanxi Province Natural Science Foundation of China (2021JZ-14). We are very grateful for the equipment support provided by Ms. Yingcui Yu in College of Natural Resources and Environment, Northwest A&F University. We are very grateful to Dr. Xueling Huang of State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University for assistance with PCR instrument. The authors thank the Teaching and Research Core Facility at College of Life Science (Ningjuan Fan).

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  1. Ying Ma, Fali Li, and Yuying Yi are the Co-first authors.

Authors and Affiliations

  1. College of Life Sciences, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Ying Ma, Fali Li, Yuying Yi, Tian Li, Xiuyu Wang, Haotian Sun, Sirui Han, Luan Zhang & Jisheng Li

  2. WuXi AppTec, Shanghai, 200131, China

    Xiaofeng Wang, Ying Chen & Haiqing Tang

  3. Division of Laboratory Safety and Services, Life Science Research Core Services, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Luqi Li & Meijuan Ren

  4. School of Environmental Science and Engineering, Shaanxi University of Science and Technology, Xi’an, 710021, Shaanxi, China

    Honglei Jia

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Contributions

JSL. and HLJ. conceived and designed the experiments; YM., FLL, YYY., XYW., HTS., MJR., LQL, TL., SRH., LZ., YC, and HQT. performed the experiments; YM., XFW. YYY. and XYW. analyzed data; YM. and JSL. wrote the article.

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Correspondence to Honglei Jia or Jisheng Li.

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Ma, Y., Li, F., Yi, Y. et al. Hydrogen sulfide improves salt tolerance through persulfidation of PMA1 in Arabidopsis. Plant Cell Rep 42, 1265–1277 (2023). https://doi.org/10.1007/s00299-023-03029-2

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