On the Evolution of Quantitative Disease Resistance to Necrotrophic Fungal Pathogens in Solanum species.

Generalist necrotrophic pathogens like Sclerotinia sclerotiorum threaten many crops worldwide. The absence of complete resistance has driven breeders to rely on quantitative disease resistance (QDR), an incomplete yet broad-range plant defence. However, challenges in linking QDR loci to phenotypes highlight how poorly host regulatory factors are understood. In this thesis, I characterised the QDR diversity of wild tomato populations against S. sclerotiorum. I observed an astonishing diversity of the QDR mechanisms, including infection frequency, lag phase duration, and lesion doubling time (LDT), among and within different species. Using high-throughput phenotyping, I found no correlation between either of the three mechanisms, suggesting the existence of independent biological processes determining QDR.

I investigated the shifts in gene expression of genotypes spanning an LDT gradient. Using differential gene expression analysis and different types of network analysis, I observed that basal and highly species-specific gene regulatory networks (GRN) determine LDT-driven QDR. I showed that the conserved NAC29 transcription factor co-opted a role in QDR in Solanum pennellii. Although NAC29 is conserved across all five species, it is only induced upon infection in S. pennellii and is linked to defence-related downstream genes, indicating GRN rewiring.

This study demonstrates that complex regulatory rewiring underlies QDR, with lag-phase duration and lesion doubling time (LDT) controlled independently by the host. Evolutionary analysis highlights the role of paralog diversification, followed by lineage-specific co-option into QDR-related gene regulatory networks. These insights improve our understanding of how QDR mechanisms are regulated and evolve, thereby supporting the development of pre-breeding strategies for more effective QDR-focused breeding programs.

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