Co-optation of Transcription Factors Drives Evolution of Quantitative Disease Resistance Against a Necrotrophic Pathogen

Wild relatives of crop species possess diverse levels of quantitative disease resistance (QDR) to biotic stresses, yet the genomic and regulatory mechanisms underlying these differences are poorly understood. In particular, how QDR against a generalist necrotrophic pathogen evolved and whether it is driven by conserved or species-specific regulatory networks remains unclear. Here, we examined the transcriptomic responses of five diverse wild tomato species that span a gradient of QDR. We initially hypothesised that conserved regulatory modules might control QDR. Instead, we use differential gene expression analysis and weighted gene co-expression network analysis (WGCNA) to find that species-specific regulatory features, encompassing both infection-induced and constitutively expressed genes, predominantly shape QDR levels. Although we identified an ethylene response factor among candidate genes for QDR-regulation, it did not fully account for the phenotypic variation. To further dissect the evolutionary basis of these regulatory patterns, we performed phylotranscriptomic analyses on gene regulatory networks. Notably, our findings reveal that the conserved NAC transcription factor 29 is pivotal in developing disease resistance only in S. pennellii . The differential regulation and altered downstream signalling pathways of NAC29 provide evidence for its co-option in the resistance mechanisms of S. pennellii . This finding highlights the species-specific rewiring of gene regulatory networks by repurposing a conserved regulatory element to enhance resistance against pathogens effectively. These results offer new insights into the evolutionary and regulatory complexity underlying QDR and emphasise the significance of species-specific gene regulation in shaping resistance against a cosmopolitan necrotrophic pathogen.