DOI: 10.1093/jxb/erag396 ISSN: 0022-0957

Penicillium melinii promotes root growth through subtle host reprogramming across model and crop species

Laura Gutierrez-Manso, Iván Devesa-Aranguren, Carlos M Conesa, Gonzalo Monteoliva-García, Sandra González-Sáyer, Alberto Lozano-Enguita, Francesco Blasio, Rodrigo Cao-García, Lydia Ugena, José Nolasco, Ana Vázquez-Mora, Camila C B Levy, Enrique Ariel Otero, Patricia Fernández-Calvo, Miguel Ángel Moreno-Risueno, Ivan Petrik, Aleš Pěnčík, María Reguera, Sara González-Bodí, Jaime Huerta-Cepas, Soledad Sacristán, Juan Carlos del Pozo, Javier Cabrera

Abstract

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. P. 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.

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