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ACL1-ROC4/5 complex reveals a common mechanism in rice response to brown planthopper infestation and drought

Author

Listed:
  • Zhihuan Tao

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Lin Zhu

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Haichao Li

    (Chinese Academy of Sciences)

  • Bo Sun

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Xue Liu

    (Beijing Academy of Agriculture and Forestry Science)

  • Dayong Li

    (Beijing Academy of Agriculture and Forestry Science)

  • Wenli Hu

    (Chinese Academy of Sciences)

  • Shanshan Wang

    (Chinese Academy of Sciences)

  • Xuexia Miao

    (Chinese Academy of Sciences)

  • Zhenying Shi

    (Chinese Academy of Sciences)

Abstract

Brown planthopper (BPH) is the most destructive insect pest of rice. Drought is the most detrimental environmental stress. BPH infestation causes adaxial leaf-rolling and bulliform cells (BCs) shrinkage similar to drought. The BC-related abaxially curled leaf1 (ACL1) gene negatively regulates BPH resistance and drought tolerance, with decreased cuticular wax in the gain-of-function mutant ACL1-D. ACL1 shows an epidermis-specific expression. The TurboID system and multiple biochemical assays reveal that ACL1 interacts with the epidermal-characteristic rice outermost cell-specific (ROC) proteins. ROC4 and ROC5 positively regulate BPH resistance and drought tolerance through modulating cuticular wax and BCs, respectively. Overexpression of ROC4 and ROC5 both rescue ACL1-D mutant in various related phenotypes. ACL1 competes with ROC4/ROC5 in homo-dimer and hetero-dimer formation, and interacts with the repressive TOPLESS-related proteins. Altogether, we illustrate that ACL1–ROC4/5 complexes synergistically mediate drought tolerance and BPH resistance through regulating cuticular wax content and BC development in rice, a mechanism that might facilitate BPH-resistant breeding.

Suggested Citation

  • Zhihuan Tao & Lin Zhu & Haichao Li & Bo Sun & Xue Liu & Dayong Li & Wenli Hu & Shanshan Wang & Xuexia Miao & Zhenying Shi, 2024. "ACL1-ROC4/5 complex reveals a common mechanism in rice response to brown planthopper infestation and drought," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52436-w
    DOI: 10.1038/s41467-024-52436-w
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    References listed on IDEAS

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    1. Jianping Guo & Huiying Wang & Wei Guan & Qin Guo & Jing Wang & Jing Yang & Yaxin Peng & Junhan Shan & Mingyang Gao & Shaojie Shi & Xinxin Shangguan & Bingfang Liu & Shengli Jing & Jing Zhang & Chunxue, 2023. "A tripartite rheostat controls self-regulated host plant resistance to insects," Nature, Nature, vol. 618(7966), pages 799-807, June.
    2. Yongliang Zhang & Gaoyuan Song & Neeraj K. Lal & Ugrappa Nagalakshmi & Yuanyuan Li & Wenjie Zheng & Pin-jui Huang & Tess C. Branon & Alice Y. Ting & Justin W. Walley & Savithramma P. Dinesh-Kumar, 2019. "TurboID-based proximity labeling reveals that UBR7 is a regulator of N NLR immune receptor-mediated immunity," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
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