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Formyl tetrahydrofolate deformylase affects hydrogen peroxide accumulation and leaf senescence by regulating the folate status and redox homeostasis in rice

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Abstract

It is well established that an abnormal tetrahydrofolate (THF) cycle causes the accumulation of hydrogen peroxide (H2O2) and leaf senescence, however, the molecular mechanism underlying this relationship remains largely unknown. Here, we reported a novel rice tetrahydrofolate cycle mutant, which exhibited H2O2 accumulation and early leaf senescence phenotypes. Map-based cloning revealed that HPA1 encodes a tetrahydrofolate deformylase, and its deficiency led to the accumulation of tetrahydrofolate, 5-formyl tetrahydrofolate and 10-formyl tetrahydrofolate, in contrast, a decrease in 5,10-methenyl-tetrahydrofolate. The expression of tetrahydrofolate cycle-associated genes encoding serine hydroxymethyl transferase, glycine decarboxylase and 5-formyl tetrahydrofolate cycloligase was significantly down-regulated. In addition, the accumulation of H2O2 in hpa1 was not caused by elevated glycolate oxidation. Proteomics and enzyme activity analyses further revealed that mitochondria oxidative phosphorylation complex I and complex V were differentially expressed in hpa1, which was consistent with the H2O2 accumulation in hpa1. In a further feeding assay with exogenous glutathione (GSH), a non-enzymatic antioxidant that consumes H2O2, the H2O2 accumulation and leaf senescence phenotypes of hpa1 were obviously compensated. Taken together, our findings suggest that the accumulation of H2O2 in hpa1 may be mediated by an altered folate status and redox homeostasis, subsequently triggering leaf senescence.

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Acknowledgements

This work was supported by the National Key Research and Development Program of China (2016YFD0101801), the National Natural Science Foundation of China (91735303 and 91335103), the Natural Science Foundation of Zhejiang (LY18C130010, LY18C130009, and LY20C130004), the Science and Technology Project of Hangzhou (20180432B03, 20180432B09, and 20180432B04) and the Foundation of Zhejiang Education Department (Y201431296).

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Authors and Affiliations

  1. College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, 311121, China

    Erhui Xiong, Fei Chen, Chen Zhang, Shan Li, Yanli Zhang, Limin Wu & Yanchun Yu

  2. State Key Laboratory for Rice Biology, China National Rice Research Institute, Hangzhou, 310006, China

    Guojun Dong & Qian Qian

  3. Ministry of Education Key Laboratory of Environmental Remediation and Ecosystem Health, College of Environmental and Resources Science, Zhejiang University, Hangzhou, 310058, China

    Jahidul Islam Shohag & Xiaoe Yang

  4. State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China

    Yihua Zhou

  5. Laboratory of Rice Biology in Henan Province, Collaborative Innovation Center of Henan Grain Crops, College of Agronomy, Henan Agricultural University, Zhengzhou, 450000, China

    Erhui Xiong

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  1. Erhui Xiong
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Correspondence to Qian Qian, Limin Wu or Yanchun Yu.

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Xiong, E., Dong, G., Chen, F. et al. Formyl tetrahydrofolate deformylase affects hydrogen peroxide accumulation and leaf senescence by regulating the folate status and redox homeostasis in rice. Sci. China Life Sci. 64, 720–738 (2021). https://doi.org/10.1007/s11427-020-1773-7

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  • DOI: https://doi.org/10.1007/s11427-020-1773-7

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