Soil Microbe-Induced Plant Volatiles Can Alert Neighboring Plants to Heavy Metal Stress

While the alerting effects of microbe-induced plant volatiles (MIPVs) to biotic stressors have been extensively studied, the ecological functions of MIPVs responding to abiotic stressors have received less attention. Using an interplant communication assay setup, we employed Phytolacca americana as a study species to investigate whether heavy metal-induced MIPVs released by the emitter plants contribute to metal tolerance in neighboring receiver plants. We found that high levels of manganese (Mn) stress increased the total MIPV emissions of plants cultivated in non-sterilized soil, in contrast to volatile organic compounds emitted by plants in sterilized soil. MIPVs produced by the Mn-stressed plants notably altered the hormonal profiles of the receiver plants, leading to increased similarity in soil microbial assembles and modification of competitive, stress-tolerant, ruderal strategies. Consequently, the receiver plants exhibited enhanced tolerance to subsequent Mn stress, as evidenced by improved growth performance, increased antioxidant enzyme activities and reduced membrane damage. By unraveling the mechanism underlying MIPV-mediated tolerance priming for neighboring plants, we reveal a key signal role of soil microorganisms involved in plant-plant communication. This study represents one of the initial efforts to elucidate the alerting effects of MIPVs induced by heavy metal stress on neighboring plants and its ecological consequences.