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The emerald ash borer (EAB), Agrilus planipennis, is a destructive invasive insect of North American ash (Fraxinus). While microorganisms associated with the beetle may contribute to tree decline and death, the microbial community succession during an EAB attack is unknown. We repeatedly sampled the bottom two meters of green ash (Fraxinus pennsylvanica) and black ash (Fraxinus nigra) in seven stands across an infestation gradient over four years. Amplicon libraries were sequenced from control phloem tissue of trees showing no symptoms of infestation, uninfested phloem of trees with EAB, infested phloem (galleries), frass, and larvae to determine if there are shifts in the fungal and bacterial communities as trees succumb to EAB attack. We found that the control phloem communities significantly differed from the beetle-infested phloem in both tree species. Furthermore, as EAB progressed in its attack from the top limbs to the tree’s base, the microbial communities in uninfested phloem outside the galleries shifted away from communities in phloem of control trees. In infested phloem, more than 80% of the detected taxa were absent from control trees (i.e., most taxa were non-latent). However, the relative abundance of latent taxa in infested phloem was higher than the relative abundance of the non-latent taxa, especially for potential canker-causing fungi, which increased 21-fold and 32-fold in black ash and green ash trees, respectively. These findings provide valuable insight into how a woodboring beetle shapes the microbial environment within trees over time, influencing the overall microbial diversity, such as canker-causing and wood decay taxa. 

ABSTRACT Plants have coevolved with herbivorous insects for millions of years, resulting in variation in resistance both within and between species. Using a manipulative experiment combined with untargeted metabolomics, microbiome sequencing and transcriptomics approaches, we investigated the roles of plant metabolites and the microbiome in defence mechanisms in native resistant Manchurian ash (Fraxinus mandshurica) trees and non‐native susceptible velvet ash (Fraxinus velutina) trees against the highly invasive emerald ash borer (EAB,Agrilus planipennis). Comparative transcriptomics and metabolomics analyses show that the phenylpropanoid pathway, which is enriched in differentially expressed genes and differentially abundant metabolites, may serve as a potential regulator of resistance. Additionally, the microbiome is distinctly shifted in two ash species. Indicator taxa analysis reveals that the distinct genera are dominant in the galleries of two ash species, for example,Pseudomonasin velvet, andHafnia‐Obesumbacteriumin Manchurian. The strong correlation between indicator taxa and metabolites suggests that the chemical compounds might impact the microbial community in phloem directly or indirectly, or vice versa. This study significantly enhances our understanding of the variation in resistance between ash species and its contribution to the invasion success of EAB, providing valuable insights for the development of pest management strategies.