Diffusive Phyllosphere Microbiome Potentially Regulates Harm and Defence Interactions Between Stephanitis nashi and Its Crabapple Host

ABSTRACT Pear lace bug (Stephanitis nashi) is a significant herbivorous pest, harbouring a diverse microbiome crucial for crabapple (Malus sp.) host adaptation. However, the mutual influence of S. nashi‐ and plant‐associated microbiomes on plant responses to pest damage remains unclear. This study found that S. nashi damage significantly altered bacterial community structure and reduced bacterial evenness in the crabapple phyllosphere. Notably, bacterial diversity within S. nashi was significantly lower than that in the environment, potentially influenced by insect developmental stage, bacterial diffusion stage and endosymbiont species number and abundance. Extensive bacterial correlation and diffusion effect between S. nashi and adjacent plant environments were observed, evident in a gradual decrease in bacterial diversity and an increase in bacterial acquisition ratio from soil to phyllosphere to S. nashi. Correspondingly, S. nashi significantly impacted the metabolic response of crabapple leaves, altering pathways involved in vitamin, amino acid and lipid metabolism and so forth. Furthermore, association analysis linked these metabolic changes to phyllosphere bacterial alterations, emphasizing the important role of diffusive phyllosphere microbiome in regulating S. nashi‐crabapple interactions. This study highlights bacterial diffusion effect between insect and plants and their potential role in regulating insect adaptability and plant defence responses, providing new insights into plant−insect−microbiome interactions. Summary statement The mutual influence of the microbiome associated with both Stephanitis nashi and plants on plant responses to pest damage remains unclear. This study uncovered a microbial diffusion effect between S. nashi and its crabapple host and highlighted the potential role of microorganisms in regulating insect adaptability and plant defence responses. These findings provide new insights into the complex interactions among plants, insects and their associated microbiomes.