Breaking the trade-off: Trichoderma effector Tahfb1 dual-targets growth and defense pathways via Hsp70L

Beneficial microbes like Trichoderma can help plants balance growth and defense, but the key signaling molecules and mechanisms underlying this balance remain unclear. In the present study, we demonstrated that Trichoderma asperellum promotes tomato growth and enhances resistance to Botrytis cinerea. Interaction transcriptomics revealed a 156-fold upregulation of Tahfb1, a gene encoding a class II hydrophobin. Application of exogenous Tahfb1 protein increased lateral root growth and reduced lesion area on tomato leaves. A CRISPR/Cas9-mediated knockout of Tahfb1 resulted in a 32% reduction in lateral roots and a 39% increase in lesion size. Conversely, overexpression strains significantly enhanced lateral root growth by 97% and decreased lesion area by 40%. Pot experiments further confirmed that Tahfb1 increased the number of lateral roots by 42% and reduced lesion area by 58%. Furthermore, yeast two-hybrid (Y2H), co-immunoprecipitation (Co-IP), and bimolecular fluorescence complementation (BiFC) confirmed that Tahfb1 directly interacts with the tomato heat shock protein Hsp70L. RNAi silencing of Hsp70L significantly compromised Tahfb1-induced lateral root development by 53% and increased lesion size by 62%. Quantitative analysis indicated that Tahfb1 modulates auxin signaling pathway (ARF19/PIN1/CYCB1;2), and the jasmonic acid/ethylene pathway (LOX/ETR1) to synergistically promote growth and immunity. Our results identify the Tahfb1-Hsp70L module as a key mediator of the synergistic enhancement of growth and defense in Trichoderma-plant interactions.