Root growth promotion by <i>Penicillium melinii</i> : mechanistic insights and agricultural applications

This study characterizes <i>Penicillium melinii</i> , an endophytic fungus isolated from <i>Arabidopsis thaliana</i> roots, as a plant growth-promoting fungus with potential use as a model to study root development and as a biostimulant for sustainable agriculture. Although endophytes are known to promote plant growth, the underlying molecular mechanisms often remain poorly understood. Here, we aimed to elucidate how <i>P. melinii</i> enhances root system development and to assess its applicability across different crops. Phenotypic assays were conducted in Arabidopsis, quinoa and tomato under <i>in vitro</i> , greenhouse and field conditions. Root architecture and biomass were quantified using image-based phenotyping. Transcriptomic and phytohormone profiling assessed plant responses, and fungal genome sequencing coupled with secretome analysis was used to identify candidate effectors and metabolic traits. <i>P. melinii</i> consistently promoted root growth and increased plant biomass across species and environments, both <i>in vitro</i> and in the greenhouse. In tomato field trials, this translated into a significant increase in yield. The fungus colonized root surfaces without vascular penetration and triggered a mild transcriptomic response: early activation of stress-response genes followed by their attenuation and sustained upregulation of auxin-related pathways. Notably, the interaction modulates the <i>SLR-ARF-LBD</i> pathway and the number of pre-branch sites probably through increased auxin signalling in the oscillation zone. Additional hormonal changes were limited and mainly associated with the attenuation of the plant response to microorganisms. <i>P. melinii</i> enhances lateral root formation through a subtle molecular and metabolic dialogue with the host plant, underscoring its relevance as a model for studying root developmental plasticity. Its strong and reproducible growth-promoting effect, demonstrated with different fungal strains and under controlled and field conditions, supports its potential as a biostimulant for sustainable crop production.