Augmenting rice ANNEXIN expression to counter planthopper NlAnnexin-like5 as an antivirulence strategy against a major crop pest

• 成果类型: Article
• 署名作者: Zhang, Xiao-Ya; Li, Shaoqin; Opachaloemphan, Comzit; Zhang, Chuan-Xi; He, Sheng Yang; Jiang, Yanjuan
• 署名单位: Zhejiang University; Michigan State University; Yunnan University; Chinese Academy of Sciences; Xishuangbanna Tropical Botanical Garden, CAS; Duke University; Ningbo University; Howard Hughes Medical Institute; Duke University
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.2505698122
• 发表日期: 2025-10-14
• 页码: e2505698122
• 关键词: brown planthopper; annexins; calcium dynamics; insect effector; plant immunity; TRIGGERED IMMUNITY; MOLECULAR-PATTERNS; brown planthopper; SECRETED SALIVA; plant defense; calcium; resistance; arabidopsis; channel; signals

摘要

The brown planthopper (BPH) is the most devastating insect pest in rice, posing a serious threat to global rice production. One attractive control strategy would be based on the understanding of the virulence mechanisms of BPH at the molecular level and then designing targeted methods to neutralize such mechanisms. Salivary proteins of BPH are important players in mediating rice-BPH interactions. Here, we describe a pivotal role of a watery saliva protein, Nilaparvata lugens Annexin-like5 (NlANX5), in the rice-BPH interaction. RNA interference (RNAi) of NlANX5 greatly compromised BPH feeding performance and survival rate on rice plants. NlANX5-RNAi BPH triggered rapid calcium ion influx in rice cells. The feeding and survival defects ofNlANX5-RNAi BPH can be restored in NlANX5-expressing transgenic rice plants. NlANX5 targets rice annexin (OsANN) proteins, including OsANN2 and OsANN8. Further analysis with NlANX5 and OsANN2 as well as OsANN8 showed that NlANX5 displaces OsANN2 and OsANN8 from the rice cell membrane. The osann2 osann8 mutant rice plants are hypersusceptible to BPH infestation. In contrast, enhanced expression of OsANN2 and OsANN8 genes resulted in robust rice resistance against BPH. This study highlights a successful example of identifying and augmenting the expression of the host targets of a major BPH virulence effector as a promising antivirulence strategy against an important crop pest.