Phytol-induced interplant signaling in maize facilitates EXP-A20-driven resistance through ACO31-dependent ethylene accumulation against Ostrinia furnacalis.

Abstract

Plants have evolved sophisticated defense mechanisms against insect herbivores, including cell wall fortification through lignin biosynthesis. Insect attack primes systemic acquired resistance in plants, preparing them to respond more swiftly and vigorously to subsequent insect assaults. Here, we found that Beauveria bassiana-exposed maize plants can emit phytol upon infestation by Spodoptera frugiperda, inducing plant-to-plant (PTP) communication of alert signals for neighboring plants, and revealed the expansin protein EXP-A20 as a pivotal node mediating maize defense responses in neighboring plants against the destructive pest Ostrinia furnacalis via stimulation of ethylene (ET) synthesis and lignin production. Through virus-induced gene silencing, we showed that EXP-A20 is essential for maize resistance, while downregulating ET and lignin pathways. Critically, protein-protein interactions determined via luciferase complementation and yeast two-hybrid assays demonstrated that EXP-A20 binds to and likely activates the ET-forming enzyme gene ACO31 to initiate defense signaling cascades, representing a novel signaling modality for expansins. Treatment with the plant volatile phytol has known insecticidal/priming activity, but we found that its effectiveness requires EXP-A20. This finding highlights the importance of EXP-A20 upstream of hormone-cell wall crosstalk in defense activation by volatiles. Overall, our multifaceted dissection of EXP-A20 revealed key molecular intersections underlying inducible maize immunity against herbivores. Furthermore, we provide functional evidence that extensive cell growth processes directly stimulate defense programs in plants. Our work opens new avenues for enhancing durable, broad-spectrum pest resistance in maize through the use of volatile organic compounds and PTP interactions.