Laura Gutiérrez-Manso

Root development is highly responsive to microbial interactions, yet the mechanisms by which beneficial fungi promote root growth remain incompletely understood. Here, we identified Penicillium melinii ‘isolate 2’ through a screen of endophytic fungi isolated from Arabidopsis and characterized it as a promoter of root development in both Arabidopsis and crop species. We combined phenotyping in vitro, rhizotron, greenhouse, and field assays with reporter and mutant analyses, transcriptomics, phytohormone profiling and sequencing, and annotation of the fungal genome to investigate the basis of this interaction. Penicillium melinii consistently stimulated root growth and modified root architecture across experimental systems and host species. These effects were associated with subtle but reproducible host transcriptional reprogramming, supporting a model in which the fungus fine-tunes endogenous developmental programmes rather than broadly perturbing stress or growth pathways. Genetic and reporter analyses further suggested that this interaction modulates root branching through localized developmental reprogramming. Genomic analysis provided a framework for understanding the fungal traits associated with this beneficial interaction. The conservation of the response across model and crop species supports the relevance of P. melinii as both a useful experimental system to study beneficial plant–fungus interactions and a promising candidate for improving root traits and crop performance.

This study characterizes Penicillium melinii, an endophytic fungus isolated from Arabidopsis thaliana 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 P. melinii enhances root system development and to assess its applicability across different crops. Phenotypic assays were conducted in Arabidopsis, quinoa and tomato under in vitro, 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. P. melinii consistently promoted root growth and increased plant biomass across species and environments, both in vitro 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 SLR-ARF-LBD 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. P. melinii 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.

Rising temperatures driven by climate change put crops under stress, and threaten their productivity by exacerbating both abiotic and biotic challenges. While research has traditionally focused on aboveground plant responses, the role of roots in heat stress adaptation is often overlooked. The primary objective of this review is to synthesize current knowledge on how root development and root–microbiome interactions contribute to plant resilience under elevated atmospheric temperatures. The interest in this topic is driven by growing evidence that belowground traits play a pivotal role in determining plant performance under thermal stress. In addition, new findings indicate that epigenetic regulation might influence root development and microbial effects to significantly enhance heat tolerance. Additionally, we emphasize how research often underscores the importance of using experimental approaches for plant growth, whether in vitro or in greenhouses, that better replicate natural conditions, to ensure the translational relevance of laboratory findings. By integrating physiological, molecular, and ecological insights, this review offers insights for the development of more heat-resilient crops in the face of a warming climate scenario.