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

Abstract

Plants must fine-tune their needs for growth and defense. 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 crosstalk framework that orchestrates the age-related balance between plant growth and herbivore defense. We demonstrate that the accumulation of salicylic acid (SA), synthesized by Nicotiana benthamiana phenylalanine ammonia-lyase 6 (NbPAL6), dictates insect resistance in adult plants. The expression of NbPAL6 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 NbmiR160c, a microRNA that simultaneously silences NbARF18La/b, subsequently reducing NbMYB42 expression, lowering SA accumulation, and thus weakening herbivore defense. Furthermore, excessive SA accumulation in juvenile plants enhances defense but antagonizes auxin signaling, impairing early growth. Our findings suggest a seesaw-like model that balances growth and herbivore defense depending on the plants developmental stage.