Co-option 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. The genomic and regulatory mechanisms underlying these differences are poorly understood. How QDR against a generalist necrotrophic pathogen evolved and whether it is driven by conserved or species-specific regulatory networks remains unclear. We examined the transcriptomic responses of five diverse wild tomato species that span a gradient of QDR. We initially hypothesized that conserved regulatory modules might control QDR. We use differential gene expression analysis and weighted gene co-expression network analysis (WGCNA) to find instead that species-specific regulatory features, encompassing both infection-induced and constitutively expressed genes, predominantly shape QDR levels. To further dissect the evolutionary basis of these regulatory patterns, we performed phylotranscriptomic analyses of 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 signaling pathways of NAC29 provide evidence for its co-option in the resistance mechanisms of S. pennellii. The role of NAC29 in conferring resistance is confirmed by the presence of a premature stop codon in susceptible S. pennellii genotypes. This finding highlights the species-specific rewiring of gene regulatory networks by repurposing a conserved regulatory element to effectively enhance resistance against pathogens. These results offer insights into the evolutionary and regulatory complexity underlying QDR and emphasize the significance of species-specific gene regulation in shaping resistance against a cosmopolitan necrotrophic pathogen.