Defense Thesis

Director: Marc Bardin
Co-Director: Bernard Caromel
Examiners: Laurent Legendre, Julie Ferreira-De-Carvalho
Rapporteurs: Elsa Ballini, Laurence Godiard

Abstract: Plants are continuously exposed to biotic stresses caused by viruses, bacteria, fungi, and oomycetes. Although they have evolved efficient defense mechanisms, the effectiveness of these responses varies among cultivars and is increasingly challenged by climate change. Plant resistance inducers (PRIs) represent a promising strategy to sustainably enhance crop resistance. However, their efficacy strongly depends on the plant genotype, and the genetic basis underlying this variability remains poorly understood. The objective of this thesis was to identify the genetic determinants controlling tomato accession responses to PRIs. To achieve this, a core collection of 148 tomato accessions was evaluated using two commercial PRIs: Belvine®, applied against Phytophthora infestans (late blight agent) and phenotyped under tunnel conditions in 2024 and 2025, and Planticare®, applied against Oidium neolycopersici (powdery mildew agent) and evaluated under greenhouse conditions using the same experimental design.

Genome-wide association studies (GWAS) identified twelve quantitative trait loci (QTLs) associated with tomato responses to PRIs, distributed across chromosomes 2, 3, 4, 5, 7, 8, and 12, depending on the PRI, the target pathogen, and the experimental environment. Gene expression analyses further showed that both PRIs induced the upregulation of several defense-related genes, including pathogenesis-related (PR) genes (PR-1, PR-2, PR-4, PR-5, and PR-8), oxidative stress related genes (Peroxidase and Glutathione S-transferase), and a key gene involved in ethylene biosynthesis (ACCO). Among the candidate genes identified within the confidence intervals of the Belvine®-associated QTLs, three belonged to these induced defense gene families (PR2, Peroxidase, and Glutathione S-transferase), supporting their potential role in PRI responsiveness.

Beyond PRI responses, this work also investigated the genetic architecture of tomato resistance to Oidium neolycopersici. The evaluation of 31 accessions representing six species of the genus Solanum revealed Solanum cheesmaniae LA0421 as a new source of resistance to powdery mildew. An F₂ population derived from a cross between LA0421, and the susceptible accession Rose de Berne (S. lycopersicum) was subsequently developed. Combining QTL-seq and linkage mapping enabled the identification of a novel QTL on chromosome 9. The SNP is located at the QTL peak maps within the ETO1 gene (Regulator of ethylene biosynthetic process), making it a strong candidate for the observed resistance. Owing to the close genetic relationship between S. cheesmaniae and cultivated tomato, together with the availability of KASP markers, this QTL represents a valuable resource for marker-assisted breeding. Furthermore, the GWAS conducted on the panel of 148 accessions identified seven additional resistance QTLs distributed across chromosomes 1, 4, 5, 8, 9, and 12.

This work is the first to identify genomic regions associated with tomato responsiveness to plant resistance inducers. It provides new QTLs controlling PRI responses, identifies candidate genes involved in induced defense mechanisms, and uncovers a novel source of powdery mildew resistance readily transferable to cultivated tomato. Together, these findings provide new opportunities for developing tomato cultivars combining genetic resistance with enhanced responsiveness to PRIs, thereby contributing to more sustainable disease management and reduced reliance on chemical plant protection products.