Molecular basis of methyl-salicylate-mediated plant airborne defence

Aphids transmit viruses and are destructive crop pests1. Plants that have been attacked by aphids release volatile compounds to elicit airborne defence (AD) in neighbouring plants2-5. However, the mechanism underlying AD is unclear. Here we reveal that methyl-salicylate (MeSA), salicylic acid-binding protein-2 (SABP2), the transcription factor NAC2 and salicylic acid-carboxylmethyltransferase-1 (SAMT1) form a signalling circuit to mediate AD against aphids and viruses. Airborne MeSA is perceived and converted into salicylic acid by SABP2 in neighbouring plants. Salicylic acid then causes a signal transduction cascade to activate the NAC2-SAMT1 module for MeSA biosynthesis to induce plant anti-aphid immunity and reduce virus transmission. To counteract this, some aphid-transmitted viruses encode helicase-containing proteins to suppress AD by interacting with NAC2 to subcellularly relocalize and destabilize NAC2. As a consequence, plants become less repellent to aphids, and more suitable for aphid survival, infestation and viral transmission. Our findings uncover the mechanistic basis of AD and an aphid-virus co-evolutionary mutualism, demonstrating AD as a potential bioinspired strategy to control aphids and viruses. Aphid-transmitted viruses encode proteins that suppress the plant airborne defence response-which is triggered by volatile chemicals released by neighbouring plants after aphid attack-and the plants consequently become less repellent to aphids and more suitable for aphid survival, infestation and viral transmission.

Automated summary

This study reveals the mechanism of airborne defense (AD) against aphids and viruses. The volatile compound MeSA is perceived by neighboring plants and converted into salicylic acid, which activates a signaling cascade to induce plant anti-aphid immunity and reduce virus transmission. Aphid-transmitted viruses encode proteins that suppress AD, making plants less repellent to aphids and more suitable for aphid survival, infestation, and viral transmission.