Auxin-salicylic acid seesaw regulates the age-dependent balance between plant growth and herbivore defense.

Abstract

According to the plant vigor hypothesis, younger, more vigorous plants tend to be more susceptible to herbivores compared to older, mature plants, yet the molecular mechanisms underlying this dynamic remain elusive. Here, we uncover a hormonal cross-talk framework that orchestrates the age-related balance between plant growth and herbivore defense. We demonstrate that the accumulation of salicylic acid (SA), synthesized by <i>Nicotiana benthamiana</i> phenylalanine ammonia-lyase 6 (NbPAL6), dictates insect resistance in adult plants. <i>NbPAL6</i> expression is driven by the key transcription factor, NbMYB42, which is regulated by two interacting auxin response factors, NbARF18La/b. In juvenile plants, higher auxin levels activate <i>Nb</i>miR160c, a microRNA that simultaneously silences <i>NbARF18La/b</i>, subsequently reducing <i>NbMYB42</i> expression, lowering SA accumulation, and thus weakening herbivore defense. Excessive SA in juvenile plants enhances defense but antagonizes auxin signaling, impairing early growth. Our findings suggest a seesaw-like model that balances growth and defense depending on the plant's developmental stage.