Augmenting rice <i>ANNEXIN</i> expression to counter planthopper <i>Nl</i> Annexin-like5 as an antivirulence strategy against a major crop pest

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, <i>Nilaparvata lugens</i> Annexin-like5 (<i>Nl</i>ANX5), in the rice-BPH interaction. RNA interference (RNAi) of <i>NlANX5</i> greatly compromised BPH feeding performance and survival rate on rice plants. <i>NlANX5</i>-RNAi BPH triggered a rapid calcium ion influx in rice cells. The feeding and survival defects of <i>NlANX5</i>-RNAi BPH can be restored in <i>NlANX5</i>-expressing transgenic rice plants. <i>Nl</i>ANX5 targets rice annexin (<i>Os</i>ANN) proteins, including <i>Os</i>ANN2 and <i>Os</i>ANN8. Further analysis with <i>Nl</i>ANX5 and <i>Os</i>ANN2 as well as <i>Os</i>ANN8 showed that <i>Nl</i>ANX5 displaces <i>Os</i>ANN2 and <i>Os</i>ANN8 from the rice cell membrane. The <i>osann2 osann8</i> mutant rice plants are hypersusceptible to BPH infestation. In contrast, enhanced expression of <i>OsANN2</i> and <i>OsANN8</i> 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.