Methyl 3-indolyacetate produced by a gut bacterium of the tephritid gall fly is implicated in controlling Crofton weed by reducing its lignin synthesis.

Eupatorium adenophorum, an invasive plant species of global concern, imposes substantial ecological and economic burdens across its introduced range. This study investigated the tripartite interaction between E. adenophorum, its obligate phytophagous insect Procecidochares utilis, and the insect's enteric microbiota. We isolated Kluyvera ascorbata ZLSY22, a gut-associated bacterium from P. utilis larvae, demonstrating potent herbicidal activity against the host plant. Bioactivity-guided characterization identified methyl 3-indolyacetate (MeIAA) as the principal phytotoxin, exhibiting concentration-dependent inhibition of seed germination and induction of systemic morphological aberrations including stem spiralization, petiole epinasty, and eventual plant death. Histological examination revealed MeIAA-induced cytological disorganization in vascular tissues, manifesting as cellular pleomorphism and expanded intercellular lacunae. Transcriptomic profiling revealed significant down-regulation of phenylpropanoid pathway genes (PAL, 4CL, LiP), corroborated by enzymatic assays showing lignin reduction versus control. Paradoxical up-regulation of C4H expression suggests compensatory feedback mechanisms insufficient to maintain lignification. These findings establish MeIAA as a novel bioherbicide disrupting lignocellulosic integrity through targeted pathway modulation. Furthermore, this work elucidates the evolutionary arms race between E. adenophorum and P. utilis, highlighting the underappreciated role of insect-associated microbiota in mediating plant-insect interactions. The results provide a framework for developing microbiome-informed biocontrol strategies.