Rhizosphere microbial shifts drive amygdalin detoxification and jasmonate-mediated alleviation of peach autotoxicity

Abstract

Plant-associated microbes play essential roles in maintaining plant health and modulating responses to environmental stresses. Autotoxicity from allelopathic compounds is a major constraint on perennial crop production, yet the potential for plants to recruit microbiota to counteract such toxicity remains understudied. Our research combined field sampling from a multi-replant peach system, multi-omics, pot, and hydroponic experiments to elucidate plant-microbe interactions that alleviate amygdalin-induced autotoxicity. Metabolomic analysis of peach orchard soils showed that amygdalin accumulated progressively in the rhizosphere with longer continuous cultivation. Exogenous amygdalin inhibited plant growth, with stronger suppression observed in sterilized soil, suggesting a protective role of soil microbes. Amygdalin application altered rhizobacterial community structure and enriched several taxa, including Burkholderia-Caballeronia-Paraburkholderia and Sinomonas. In vitro assays confirmed that amygdalin serves as a selective substrate for these enriched bacteria. We further found that three strains isolated from the amygdalin-stressed peach rhizosphere significantly alleviated autotoxic inhibition, and their co-inoculation showed the greatest enhancement of plant performance. Metabolomic and transcriptomic analyses revealed activation of plant jasmonic acid (JA) pathway. Its involvement was confirmed by the alleviation of amygdalin-induced stress upon exogenous JA application and by the attenuation of microbiota-mediated stress relief upon JA pathway inhibition. Our study reveals a critical mechanism by which host plants enrich specialized microbes that can alleviate autotoxicity by direct amygdalin degradation, activation of the JA pathway, and modulation of redox homeostasis in peach. These findings provide new insights into plant-microbe interactions in perennial systems and highlight the potential of microbiome-informed microbial interventions for mitigating replant disease.