ACBP4-WRKY70-RAP2.12 module positively regulates submergence-induced hypoxia response in Arabidopsis thaliana

Mengyun Guo, Yingjun Yao, Kangqun Yin, Luna Tan, Meng Liu, Jing Hou, Han Zhang, Ruyun Liang, Xinran Zhang, Heng Yang, Xiaoxiao Chen, Jinrui Tan, Yan Song, Shangling Lou, Liyang Chen, Xuejing Liu, Si Tang, Yongqi Hu, Jin Yan, Wensen Fu, Kai Yang, Ruijia Zhang, Xuerui Li, Yao Liu, Zhen Yan, Wei Liu, Yu Han, Jianquan Liu, Kangshan Mao, Huanhuan Liu

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Journal of Integrative Plant Biology ›› 2024, Vol. 66 ›› Issue (6) : 1052-1067. DOI: 10.1111/jipb.13647
Research Article

ACBP4-WRKY70-RAP2.12 module positively regulates submergence-induced hypoxia response in Arabidopsis thaliana

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Abstract

ACYL-CoA-BINDING PROTEINs (ACBPs) play crucial regulatory roles during plant response to hypoxia, but their molecular mechanisms remain poorly understood. Our study reveals that ACBP4 serves as a positive regulator of the plant hypoxia response by interacting with WRKY70, influencing its nucleocytoplasmic shuttling in Arabidopsis thaliana. Furthermore, we demonstrate the direct binding of WRKY70 to the ACBP4 promoter, resulting in its upregulation and suggesting a positive feedback loop. Additionally, we pinpointed a phosphorylation site at Ser638 of ACBP4, which enhances submergence tolerance, potentially by facilitating WRKY70's nuclear shuttling. Surprisingly, a natural variation in this phosphorylation site of ACBP4 allowed A. thaliana to adapt to humid conditions during its historical demographic expansion. We further observed that both phosphorylated ACBP4 and oleoyl-CoA can impede the interaction between ACBP4 and WRKY70, thus promoting WRKY70's nuclear translocation. Finally, we found that the overexpression of orthologous BnaC5.ACBP4 and BnaA7.WRKY70 in Brassica napus increases submergence tolerance, indicating their functional similarity across genera. In summary, our research not only sheds light on the functional significance of the ACBP4 gene in hypoxia response, but also underscores its potential utility in breeding flooding-tolerant oilseed rape varieties.

Keywords

ACBP4 / Arabidopsis thaliana / humid adaptation / natural variation / RAP2.12 / WRKY70

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Mengyun Guo, Yingjun Yao, Kangqun Yin, Luna Tan, Meng Liu, Jing Hou, Han Zhang, Ruyun Liang, Xinran Zhang, Heng Yang, Xiaoxiao Chen, Jinrui Tan, Yan Song, Shangling Lou, Liyang Chen, Xuejing Liu, Si Tang, Yongqi Hu, Jin Yan, Wensen Fu, Kai Yang, Ruijia Zhang, Xuerui Li, Yao Liu, Zhen Yan, Wei Liu, Yu Han, Jianquan Liu, Kangshan Mao, Huanhuan Liu. ACBP4-WRKY70-RAP2.12 module positively regulates submergence-induced hypoxia response in Arabidopsis thaliana. Journal of Integrative Plant Biology, 2024, 66(6): 1052‒1067 https://doi.org/10.1111/jipb.13647

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2024 2024 The Authors. Journal of Integrative Plant Biology published by John Wiley & Sons Australia, Ltd on behalf of Institute of Botany, Chinese Academy of Sciences.
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