Colletotrichum sp. H8-derived volatile organic compounds reshape Arabidopsis root system architecture associated with auxin-related responses

Microbial volatile organic compounds (VOCs) are key non-contact signals regulating plant root system architecture (RSA). However, the underlying mechanisms of how they coordinate plant hormone signals remain largely unclear. A fungal strain, Colletotrichum sp H8, was isolated from the rhizosphere of Lycium barbarum L . and its VOCs were found to promote growth in multiple plant species. In Arabidopsis , H8 VOCs induced a dual RSA response characterized by reduced primary root elongation and enhanced lateral root formation. Cytological analyses showed reduced cell proliferation in the primary root meristem and accelerated initiation of lateral root primordia. Physiological and genetic evidence demonstrated that H8 VOCs were associated with increased endogenous auxin levels and enhanced expression of genes involved in auxin biosynthesis. Auxin biosynthesis-defective mutants ( taa1 and yuc1/2/4/6 ) showed attenuated responses to VOCs treatment, supporting the contribution of auxin biosynthetic capacity to H8 VOCs-induced root remodeling. In addition, H8 VOCs affected polar auxin transport (PAT)-associated responses, with reduced PIN1/2/3/4 abundance in the primary root tip and increased PIN reporter activity in stele tissues surrounding lateral root primordia. These observations, together with auxin transport inhibition assays using NPA and TIBA, suggest that auxin transport-related processes are involved in H8 VOCs-induced RSA remodeling. GC-MS analysis and bioassays identified cedrene as a candidate volatile compound associated with the biological activity of H8 VOCs. Collectively, these results demonstrate that fungal VOCs promote plant growth and induce RSA remodeling, accompanied by changes in auxin-associated regulatory processes, providing insights into plant–microbe interactions and their potential relevance for understanding VOCs-mediated plant growth regulation.