Trichoderma afroharzianum behaves differently with respect to the host transcriptome and microbial communities under varying iron availability in pea plants

ABSTRACT Aims Trichoderma afroharzianum T22 is widely recognized for enhancing plant stress resilience, yet its effects in pea plants may vary depending on iron (Fe) availability. Methods and Results We assessed the impact of T22 on pea grown under differential Fe status through integrated physiological and omics analyses. We found that the benefits of T22 are highly context dependent, providing significant improvements in photosynthesis and Fe/N accumulation under Fe deficiency but minimal effects under sufficiency. RNA-seq identified 262 DEGs under Fe deficiency and 555 DEGs under Fe sufficiency following T22 inoculation, with the latter primarily associated with basal metabolic functions, indicating potential colonization costs rather than adaptive responses. Particularly, T22 inoculation upregulated symbiosis-related genes ( Nodule-specific GRPs , Major facilitator, sugar transporter-like ), Fe transporters ( NRAMPs , HMAs ), and redox-associated genes ( Glutathione S-transferase , Glutathione peroxidase ) in the roots under Fe shortage, reflecting a coordinated response to enhance nutrient acquisition and stress tolerance. Microbiome profiling revealed that under Fe deficiency, T22 reshaped the root community by enriching several bacterial taxa such as Comamonadaceae, Pseudomonadaceae and Mitsuaria . These enriched bacterial taxa may act as potential ‘helpers’ to T22 by providing complementary thereby amplifying its beneficial effects under Fe deficiency. In contrast, under Fe sufficiency, community restructuring was primarily limited to the enrichment of Rhizobiaceae, Pararhizobium . Fungal taxa showed minimal overall changes, with the exception of a significant enrichment of Paecilomyces in response to T22 under Fe-deficient soil conditions. Conclusions These findings indicate that T22 functions in a context-dependent manner, with bacterial enrichment varying with Fe availability, while fungal helper effects were not prominent following T22 inoculation in pea plants. Impact Statement Beneficial microbes do not function uniformly across environments. This study highlights how Fe availability determines whether Trichoderma acts as a strong mutualist or a neutral colonizer in pea plants. Our findings advance a precision bioinoculant framework for deploying microbial consortia specifically in Fe-deficient soils to enhance legume resilience and sustainable crop production.