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

Zhihuan Tao, Lin Zhu, Haichao Li, Bo Sun, Xue Liu, Dayong Li, Wenli Hu, Shanshan Wang, Xuexia Miao () and Zhenying Shi ()
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Zhihuan Tao: Chinese Academy of Sciences
Lin Zhu: Chinese Academy of Sciences
Haichao Li: Chinese Academy of Sciences
Bo Sun: 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

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-52436-w

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