Local signal from Trichoderma afroharzianum T22 induces host transcriptome and endophytic microbiome leading to growth promotion in sorghum.

Trichoderma, a highly abundant soil fungus, may benefit plants, yet it remains understudied in sorghum (Sorghum bicolor). In this study, sorghum plants were grown for 5 weeks in pots of soil with or without inoculation of T. afroharzianum T22. Inoculation with T. afroharzianum T22 significantly increased growth parameters and nutrient levels, demonstrating its beneficial role in sorghum. A split-root assay demonstrated that T. afroharzianum T22 is essential in both compartments of the pot for promoting plant growth, suggesting that local signals from this fungus drive symbiotic benefits in sorghum. RNA-seq analysis revealed that inoculation with T. afroharzianum T22 induced genes responsible for mineral transport (such as nitrate and aquaporin transporters), auxin response, sugar assimilation (hexokinase), and disease resistance (thaumatin) in sorghum roots. Microbial community analysis further unveiled the positive role of T. afroharzianum T22 in enriching Penicillium and Streptomyces while reducing disease-causing Fusarium in the roots. The microbial consortium, consisting of enriched microbiomes from bacterial and fungal communities, showed disrupted morphological features in plants inoculated with T. afroharzianum T22 in the absence of Streptomyces griseus. However, this disruption was not observed in the absence of Penicillium chrysogenum. These results indicate that S. griseus acts as a helper microbe in close association with T. afroharzianum T22 in the sorghum endosphere. This study provides the first comprehensive explanation of how T. afroharzianum T22 modulates host molecular determinants and endophytic helper microbes, thereby collectively promoting sorghum growth. These findings may facilitate the formulation of synthetic microbial inoculants dominated by T. afroharzianum T22 to enhance growth and stress resilience in sorghum and similar crops.