Molecular defense strategy of volatile organic compound-emitting plants (order Piperales) against herbivorous mammals.

Plants have evolved diverse strategies to defend against herbivores, including structural barriers such as trichomes and tough leaves, the production of toxic secondary metabolites, the emission of volatile organic compounds (VOCs), and the recruitment of natural predators to deter herbivory. However, the molecular mechanisms underlying their ability to deter large herbivorous mammals remain poorly understood. In this study, we demonstrate that the order Piperales, which is particularly rich in VOCs, employs a conserved chemical defense strategy targeting herbivorous mammals. Behavioral assays, transgenic models, and electrophysiological analyses revealed that VOCs from Piperales species, particularly Houttuynia cordata, activate TRPA1-a sensory ion channel critical for detecting irritants-in mice and herbivores such as cattle and goats. A stable derivative of the key VOC houttuynin, sodium houttuyfonate (SH), selectively activated TRPA1 by binding conserved cysteine residues, triggering aversion in herbivorous mammals. Crucially, TRPA1 activation sites upon VOC application were conserved across herbivorous species, suggesting that Piperales plants employ a conserved evolutionary strategy to defend against herbivorous mammals. Our findings reveal a compelling case of lineage-specific defensive adaptation within Piperales, providing novel insights into plant-herbivore interactions. This research deepens our understanding of the critical role of chemical defenses in plant survival, adaptation, and ecological niche specialization.