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

  • Nat Commun. 2024 Sep 16;15(1):8107. doi: 10.1038/s41467-024-52436-w.
Zhihuan Tao  1  2 ,  Lin Zhu  1  2 ,  Haichao Li  1 ,  Bo Sun  1  2 ,  Xue Liu  3 ,  Dayong Li  3 ,  Wenli Hu  1 ,  Shanshan Wang  1 ,  Xuexia Miao  4 ,  Zhenying Shi  5
Affiliations
  • 1. Key Laboratory of Plant Design, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, China.
  • 2. University of Chinese Academy of Sciences, Beijing, China.
  • 3. National Engineering Research Center for Vegetables, Beijing Vegetable Research Center, Beijing Academy of Agriculture and Forestry Science, Beijing, P. R. China.
  • 4. Key Laboratory of Plant Design, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, China. [email protected].
  • 5. Key Laboratory of Plant Design, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, China. [email protected].
PMID: 39285171 DOI: 10.1038/s41467-024-52436-w
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.

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