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Hydrogen sulfide enhances poplar tolerance to high-temperature stress by increasing S-nitrosoglutathione reductase (GSNOR) activity and reducing reactive oxygen/nitrogen damage

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Abstract

Poplar (Populus trichocarpa) is an important woody tree for landscape and agricultural use worldwide. Nitric oxide (NO) and hydrogen sulfide (H2S) are essential messengers that enhance tolerance to environmental stress in herbaceous plants; however, the role of these messengers in modifying environmental stress in woody plants is poorly understood. Here we found that high temperature (HT) rapidly induced the generation of H2S, accompanied by increased activity of enzymes involved in H2S biosynthesis. HT also induced the accumulation of reactive nitrogen species (RNS) and reactive oxygen species (ROS), including S-nitrosothiols, H2O2, and O2 −, which damage the leaves. S-nitrosoglutathione reductase (GSNOR) has a critical role in preventing RNS and ROS damage in plants. We found that HT gradually increased the transcriptional level and the activity of GSNOR, resulting in increased scavenging of the over-accumulated ROS and RNS and, ultimately, increased adaptation to HT stress. Pharmacological experiments showed that suppressing H2S biosynthesis reduced GSNOR activity, thereby increasing RNS- and ROS-mediated damage to the leaves. Based on these data, we propose that H2S influences the response of woody plants to HT by modulating the NO signal and GSNOR activity.

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Acknowledgements

This work was supported by the National High Technology Research and Development Program of China (863 Program, No. 2013AA102705), National High-level Personnel of Special Support Program, the Qinglan Project of Jiangsu province, the Nature Science Foundation of Jiangsu Province (BK20151097), the Talent Project by the Ministry of Science and Technology, and Priority Academic Program Development of Jiangsu Higher Education Institutions. Funding was provided by National Key Basic Research Program of China (No. 2012B114500) and the National Science Foundation of China (No. 31170619).

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Authors and Affiliations

  1. College of Biology and the Environment, Nanjing Forestry University, Nanjing, China

    Tielong Cheng & Ye Peng

  2. Co-Innovation Center for the Sustainable Forestry in Southern China, Nanjing, China

    Tielong Cheng, Jisen Shi & Jinhui Chen

  3. Key Laboratory of Forest Genetics and Biotechnology, Ministry of Education, Nanjing Forestry University, Nanjing, China

    Jisen Shi, Yini Dong & Jinhui Chen

  4. College of Horticulture, Jinling Institute of Technology, Nanjing, China

    Yan Ma

  5. Shanghai Key Laboratory of Bio-Energy Crops, School of Life Sciences, Shanghai University, Shanghai, China

    Xiangyang Hu

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  1. Tielong Cheng
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Tielong Cheng, Yan Ma, Ye Peng and Jinhui Chen performed most of the experiments; Jisen Shi Yini Dong and Jinhui Chen analyzed results; Xiangyang Hu and Jinhui Chen conceptualized the research program and revised the manuscript.

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Correspondence to Jinhui Chen.

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Cheng, T., Shi, J., Dong, Y. et al. Hydrogen sulfide enhances poplar tolerance to high-temperature stress by increasing S-nitrosoglutathione reductase (GSNOR) activity and reducing reactive oxygen/nitrogen damage. Plant Growth Regul 84, 11–23 (2018). https://doi.org/10.1007/s10725-017-0316-x

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