Diverse transcriptome reprogramming trajectories underlie quantitative disease resistance at the species level

Quantitative disease resistance (QDR) is an immune response limiting the damage caused by pathogen infection in plants. It involves the transcriptomic reprogramming of numerous genes each having a weak contribution to the plant immunity phenotype. Despite QDR widespread and broad-spectrum nature, the evolution of the underlying transcriptome reprogramming remains largely uncharacterized. Here, we analyzed global gene expression in response to the necrotrophic fungus Sclerotinia sclerotiorum in 23 Arabidopsis thaliana accessions of diverse origin and contrasted QDR phenotype. Over a half of the species pan-transcriptome displayed local responses to S. sclerotiorum , with global reprogramming patterns incongruent with accessions phylogeny. Due to frequent small-amplitude variations, only ~11% responsive genes were common to all accessions. They formed protein-protein interactions networks densely connecting both old and recent genes. Clustering of accessions based on global regulation patterns identified four subsets unrelated to QDR phenotypes, highlighting at least four distinct paths towards regulatory evolution of QDR at the species level. We identified WRKY and MYB-related DNA binding sites enriched in the 5′-regulatory regions of core and subset-specific responsive genes respectively. Our findings show that the evolution of QDR involves distinct gene reprogramming trajectories at the species level, associated with contrasted patterns of cis-regulatory variation. ### Competing Interest Statement The authors have declared no competing interest.