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

IF 14.7 1区综合性期刊 Q1 MULTIDISCIPLINARY SCIENCES

Nature Communications Pub Date : 2024-09-16 DOI:10.1038/s41467-024-52436-w

Zhihuan Tao, Lin Zhu, Haichao Li, Bo Sun, Xue Liu, Dayong Li, Wenli Hu, Shanshan Wang, Xuexia Miao, Zhenying Shi

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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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ACL1-ROC4/5 复合物揭示了水稻应对褐飞虱和干旱的共同机制

褐飞虱 (BPH) 是对水稻最具破坏性的害虫。干旱是最有害的环境胁迫。BPH 侵害造成的正面卷叶和牛皮状细胞（BC）萎缩与干旱类似。与BC相关的背面卷曲叶片1（ACL1）基因对BPH的抗性和耐旱性有负向调节作用，在功能增益突变体ACL1-D中，叶片的角质蜡减少。ACL1 具有表皮特异性表达。TurboID 系统和多种生化检测发现，ACL1 与具有表皮特征的水稻最外层细胞特异性蛋白（ROC）相互作用。ROC4 和 ROC5 分别通过调节角质蜡质和 BCs 积极调控抗 BPH 和耐旱性。过表达 ROC4 和 ROC5 都能挽救 ACL1-D 突变体的各种相关表型。ACL1 与 ROC4/ROC5 竞争形成同源二聚体和异源二聚体，并与抑制性 TOPLESS 相关蛋白相互作用。综上所述，我们发现 ACL1-ROC4/5 复合物通过调节水稻的角质蜡含量和 BC 发育，协同介导了水稻的耐旱性和抗 BPH 性，这一机制可能有助于抗 BPH 育种。

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来源期刊

Nature Communications Biological Science Disciplines-

CiteScore

24.90

自引率

2.40%

发文量

6928

审稿时长

3.7 months

期刊介绍： Nature Communications, an open-access journal, publishes high-quality research spanning all areas of the natural sciences. Papers featured in the journal showcase significant advances relevant to specialists in each respective field. With a 2-year impact factor of 16.6 (2022) and a median time of 8 days from submission to the first editorial decision, Nature Communications is committed to rapid dissemination of research findings. As a multidisciplinary journal, it welcomes contributions from biological, health, physical, chemical, Earth, social, mathematical, applied, and engineering sciences, aiming to highlight important breakthroughs within each domain.