Syntaxin of plants71 plays essential roles in plant development and stress response via regulating pH homeostasis

Hailong Zhang; Jingwen Zhou; Xiaoyue Kou; Yuqi Liu; Xiaonan Zhao; Guochen Qin; Mingyu Wang; Guangtao Qian; Wen Li; Yongshun Huang; Xiaoting Wang; Zhenjie Zhao; Shuang Li; Xiaoqian Wu; Lixi Jiang; Xianzhong Feng; Jian-Kang Zhu; Lixin Li

doi:10.3389/fpls.2023.1198353

Syntaxin of plants71 plays essential roles in plant development and stress response via regulating pH homeostasis

Front Plant Sci. 2023 Jun 5:14:1198353. doi: 10.3389/fpls.2023.1198353. eCollection 2023.

Authors

Hailong Zhang¹, Jingwen Zhou¹, Xiaoyue Kou¹, Yuqi Liu¹, Xiaonan Zhao^{1

2}, Guochen Qin³, Mingyu Wang¹, Guangtao Qian¹, Wen Li¹, Yongshun Huang¹, Xiaoting Wang¹, Zhenjie Zhao¹, Shuang Li⁴, Xiaoqian Wu⁴, Lixi Jiang², Xianzhong Feng⁵, Jian-Kang Zhu^{6

7}, Lixin Li¹

Affiliations

¹ Key Laboratory of Saline-Alkali Vegetation Ecology Restoration, Ministry of Education, College of Life Sciences, Northeast Forestry University, Harbin, China.
² Institute of Crop Science, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China.
³ Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences, Peking University, Weifang, China.
⁴ State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, China.
⁵ Key Laboratory of Soybean Molecular Design Breeding, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, China.
⁶ Institute of Advanced Biotechnology and School of Life Sciences, Southern University of Science and Technology, Shenzhen, China.
⁷ Center for Advanced Bioindustry Technologies, Chinese Academy of Agricultural Sciences, Beijing, China.

Abstract

SYP71, a plant-specific Qc-SNARE with multiple subcellular localization, is essential for symbiotic nitrogen fixation in nodules in Lotus, and is implicated in plant resistance to pathogenesis in rice, wheat and soybean. Arabidopsis SYP71 is proposed to participate in multiple membrane fusion steps during secretion. To date, the molecular mechanism underlying SYP71 regulation on plant development remains elusive. In this study, we clarified that AtSYP71 is essential for plant development and stress response, using techniques of cell biology, molecular biology, biochemistry, genetics, and transcriptomics. AtSYP71-knockout mutant atsyp71-1 was lethal at early development stage due to the failure of root elongation and albinism of the leaves. AtSYP71-knockdown mutants, atsyp71-2 and atsyp71-3, had short roots, delayed early development, and altered stress response. The cell wall structure and components changed significantly in atsyp71-2 due to disrupted cell wall biosynthesis and dynamics. Reactive oxygen species homeostasis and pH homeostasis were also collapsed in atsyp71-2. All these defects were likely resulted from blocked secretion pathway in the mutants. Strikingly, change of pH value significantly affected ROS homeostasis in atsyp71-2, suggesting interconnection between ROS and pH homeostasis. Furthermore, we identified AtSYP71 partners and propose that AtSYP71 forms distinct SNARE complexes to mediate multiple membrane fusion steps in secretory pathway. Our findings suggest that AtSYP71 plays an essential role in plant development and stress response via regulating pH homeostasis through secretory pathway.

Keywords: AtSYP71; ROS homeostasis; cell wall biosynthesis and dynamics; pH homeositasis; root development; vesicle trafficking.

Grants and funding

This work was supported by the National Natural Science Foundation of China (32170279) and Fundamental Research Funds for the Central Universities (2572019CT03). The funders have no role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.