Rapid intracellular acidification is a novel plant defense response countered by the brown planthopper

Abstract

SUMMARYThe brown planthopper (BPH;Nilaparvata lugens) is the most destructive insect pest in rice. Through a stylet, BPH secrets a plethora of salivary proteins into rice phloem cells as a crucial step of infestation. However, how various salivary proteins function in rice cells to promote insect infestation is poorly understood. Among them, one of the salivary proteins is predicted to be a carbonic anhydrase (NlCA). The survival rate of theNlCA-RNA interference (RNAi) BPH insects was extremely low on rice, indicating a vital role of this salivary protein in BPH infestation. We generatedNICAtransgenic rice plants and found thatNlCAexpressed in rice plants could restore the ability ofNlCA-RNAi BPH to survive on rice. Next, we produced rice plants expressing the ratiometric pH sensor pHusion and found thatNlCA-RNAi BPH induced rapid intracellular acidification of rice cells during feeding. Further analysis revealed that bothNlCA-RNAi BPH feeding and artificial of lowering intracellular pH activated plant defense responses, and that NICA-mediated intracellular pH stabilization is linked to diminished defense responses, including reduced callose deposition at the phloem sieve plates and suppressed defense gene expression. Given the importance of pH homeostasis across the kingdoms of life, discovery of NICA-mediated intracellular pH modulation uncovered a new dimension in the interaction between plants and piecing/sucking insect pests. The crucial role of NICA for BPH infestation of rice suggests that NICA is a promising target for chemical or trans-kingdom RNAi-based inactivation for BPH control strategies in plants.HighlightsRapid intracellular acidification is a novel plant defense response.Brown planthopper delivers into rice tissues a major virulence protein, carbonic anhydrase (NlCA) critical for survival.NlCA counters intracellular acidification to suppress plant defense.Results suggest pH-sensitive intracellular regulators of defense responses in rice-brown planthopper interaction.