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

Trichoderma afroharzianum T22 is recognized for promoting plant growth and stress resilience. However, it remains unclear how its effects vary with Fe nutritional status in pea plants. In this study, we investigated the impact of T22 on pea grown under Fe-sufficient and Fe-deficient conditions by integrating physiological measurements with transcriptomic and microbiome analyses. Our results reveal 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, consistent with conditional mutualism theory. RNA-seq analysis revealed that T22 inoculation induced 262 differentially expressed genes (DEGs) under Fe deficiency, whereas under Fe sufficiency, 555 DEGs were identified, largely linked to basal metabolic functions, suggesting 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 showed that under Fe deficiency, T22 reshaped the root-associated community by enriching Pseudomonas, Variovorax, Mitsuaria, and Acidovorax, along with increased fungal richness and diversity, whereas under Fe sufficiency, restructuring was minimal and largely limited to the enrichment of Pararhizobium. These enriched bacterial taxa may act as helpers to T22 by providing complementary thereby amplifying its beneficial effects under Fe deficiency. These findings demonstrate that T22 acts in a context-dependent manner, exerting strong beneficial effects under Fe deficiency while having little influence when Fe is sufficient. These findings may establish T22 as a targeted bioinoculant for Fe-deficient soil and open avenues for designing microbial consortia to enhance legume resilience and sustainability in future agriculture.