Deciphering the Mechanisms Regulating Variability in Induced Systemic Resistance Among Tomato Genotypes

Tomato responds to induced systemic resistance by the beneficial fungus Trichoderma harzianum against foliar pathogens in a genotype-specific manner. This study investigated the mechanisms underlying these differences using the foliar pathogen Botrytis cinerea and RNA sequencing. Solanum pimpinellifolium LA 1589 (responsive) and S. lycopersicum 'Wisconsin 55' (unresponsive) were treated with T. harzianum before inoculation with B. cinerea to characterize differences in priming capabilities. The LA 1589 T. harzianum-treated samples exhibited reduced disease lesion area, increased plant height, and higher root biomass compared with the nontreated control. Conversely, the Wisconsin 55 T. harzianum-treated samples did not show the same response. To understand the molecular basis of this differential response, temporal gene expression patterns were compared between genotypes. Genes and Gene Ontology terms associated with responses to autophagy, hypersensitive response, and auxin, brassinosteroid, ethylene, flavonoid, jasmonic acid, phenylalanine, salicylic acid, and sterol metabolic processes were uniquely enriched in at least one genotype × T. harzianum × B. cinerea treatment combination. Upregulation of genes associated with the brassinosteroid, phenylpropanoid, and jasmonic acid/ethylene signaling pathways, along with downregulation of genes related to the salicylic acid signaling pathway, was identified as a key factor to prime the induced systemic resistance-responsive genotype against B. cinerea. These findings provide valuable insights into how to improve the efficacy of Trichoderma-based biocontrol strategies and provide a foundation for the development of more effective approaches to select genotypes that can better respond to beneficial microbes to obtain improved growth traits and heightened resistance against tomato pathogens.