J Integr Plant Biol ›› 2022, Vol. 64 ›› Issue (11): 2060-2074.DOI: 10.1111/jipb.13349

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  • 收稿日期:2022-02-23 接受日期:2022-08-19 出版日期:2022-11-01 发布日期:2022-11-17

NUCLEAR PORE ANCHOR and EARLY IN SHORT DAYS 4 negatively regulate abscisic acid signaling by inhibiting Snf1-related protein kinase2 activity and stability in Arabidopsis

Ya‐Nan Chang1,2†, Zhijuan Wang3†, Ziyin Ren3, Chun‐Han Wang1, Pengcheng Wang1, Jian‐Kang Zhu1,4, Xia Li3* and Cheng‐Guo Duan1,2*   

  1. 1 Shanghai Center for Plant Stress Biology and Center of Excellence in Molecular Plant Sciences, the Chinese Academy of Science, Shanghai 201602, China
    2 University of Chinese Academy of Sciences, Beijing 100049, China
    3 National Key Laboratory of Crop Genetic and Improvement, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, China
    4 Department of Horticulture and Architecture Landscape, Purdue University, West Lafayette, IN 47907, USA

    † These authors contributed equally to this study.
    * Correspondences: Cheng‐Guo Duan (cgduan@cemps.ac.cn, Dr. Duan is fully responsible for the distribution of all materials associated with this article); Xia Li (xli@mail.hzau.edu.cn)
  • Received:2022-02-23 Accepted:2022-08-19 Online:2022-11-01 Published:2022-11-17

Abstract: Abscisic acid (ABA) is a key regulator of plant responses to abiotic stresses, such as drought. Abscisic acid receptors and coreceptors perceive ABA to activate Snf1-related protein kinase2s (SnRK2s) that phosphorylate downstream effectors, thereby activating ABA signaling and the stress response. As stress responses come with fitness penalties for plants, it is crucial to tightly control SnRK2 kinase activity to restrict ABA signaling. However, how SnRK2 kinases are inactivated remains elusive. Here, we show that NUCLEAR PORE ANCHOR (NUA), a nuclear pore complex (NPC) component, negatively regulates ABA-mediated inhibition of seed germination and post-germination growth, and drought tolerance in Arabidopsis thaliana. The role of NUA in response to ABA depends on SnRK2.2 and SnRK2.3 for seed germination and on SnRK2.6 for drought. NUA does not directly inhibit the phosphorylation of these SnRK2s or affects their abundance. However, the NUA-interacting protein EARLY IN SHORT DAYS 4 (ESD4), a SUMO protease, negatively regulates ABA signaling by directly interacting with and inhibiting SnRK2 phosphorylation and protein levels. More importantly, we demonstrated that SnRK2.6 can be SUMOylated in vitro, and ESD4 inhibits its SUMOylation. Taken together, we identified NUA and ESD4 as SnRK2 kinase inhibitors that block SnRK2 activity, and reveal a mechanism whereby NUA and ESD4 negatively regulate plant responses to ABA and drought stress possibly through SUMOylation-dependent regulation of SnRK2s.

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