Dual-action MINPP1 effectors enable Riptortus pedestris to overcome phytic acid antinutritional defense and suppress pattern-triggered immunity.

Abstract

Phytic acid (IP6) serves as the primary phosphorus reservoir in plant seeds and functions as a potent antinutritional defense to inhibit herbivore growth. Despite this formidable barrier, the bean bug Riptortus pedestris preferentially feeds on IP6-rich leguminous seeds, yet the molecular mechanisms underlying this dietary adaptation have remained elusive. Here, we demonstrate that R. pedestris overcomes this nutritional defense by co-opting the ancient, highly conserved multiple inositol polyphosphate phosphatase 1 (MINPP1) family. We identified four RPMINPP1 paralogs abundantly expressed in both the salivary glands and the midgut. Using 3 1P NMR spectroscopy, we showed that these enzymes completely dephosphorylate IP6 to inorganic phosphate. Functional analyses revealed a sophisticated dual-action detoxification strategy: salivary RPMINPP1 is secreted into host tissues to degrade IP6 in planta, whereas midgut-localized RPMINPP1Ls mediate IP6 hydrolysis in vivo. RNA interference experiments confirmed that RPMINPP1Ls are essential for insect feeding and survival on soybean hosts. Remarkably, RPMINPP1 also functions as a broad-spectrum suppressor of pattern-triggered immunity (PTI) triggered by diverse elicitors, acting independently of its catalytic activity. Collectively, our findings uncover a dual-pronged strategy in which an herbivore repurposes MINPP1 family effectors to simultaneously neutralize phytic acid-based antinutritional defense and suppress host plant immunity.