Chemical distance outweighs phylogeny in VOC-mediated cross-species plant defense communication

Plants can detect and respond to airborne volatile organic compounds (VOCs) from neighboring species, enhancing their defenses against herbivore attack. While such interspecific communication has been documented, how induced-resistance strength varies across species and what factors drive this variation remain unclear. We hypothesized that phylogenetic relatedness or chemical similarity in VOC profiles between plant species influences the effectiveness of plant-plant communication. We tested the hypothesis by exposing nine receiver plant species from two classes and six families to constitutive plant volatiles (CPVs) and herbivore-induced plant volatiles (HIPVs) emitted by Phytolacca americana. VOC exposure did not directly induce defenses but primed the diverse receiver species for stronger responses to subsequent herbivory, leading to reduced larval growth, feeding, and oviposition. Defense priming was characterized by a stronger induction of Calmodulin-like (CML) genes in Ca²⁺ signaling upon subsequent herbivore attack across species. Furthermore, in our study system, resistance strength declined with increasing chemical distance between emitter and receiver species, whereas phylogenetic distance was a weaker and inconsistent predictor. These findings identify chemical similarity as a stronger predictor than evolutionary relatedness for interspecific resistance in VOC-mediated plant-plant communication, advancing our understanding of how plants interpret chemical cues in diverse communities.