Host-Specific Transcriptional Responses of Phytophthora capsici During Early Crown Infection in Cucurbitaceous and Solanaceous Plants

Phytophthora capsici is a broad-host-range oomycete phytopathogen responsible for economic losses in crops worldwide. Previous transcriptomic analyses have focused mainly on plant responses to infection. However, the transcriptional adaptations of the phytopathogen to different host species remain poorly understood. In this study, we investigated the transcriptomic response of P. capsici during early infection in Cucumis sativus, Cucumis melo, Capsicum annuum CM334, and Solanum lycopersicum by RNA-seq and multiphoton microscopy. Focusing on crown infections since it is the natural entry point for the pathogen.

Our results reveal striking host-specific infection strategies. In tomato, rapid necrosis at 12-27 hours post-inoculation was associated with early metabolic reprogramming and effector repression. In contrast, cucurbits exhibited delayed necrosis (36-102 hpi), supporting extensive host intracellular colonization and upregulation of carbohydrate metabolism pathways. Partially resistant CM334 chili pepper restricted pathogen proliferation, with P. capsici displaying transcriptional signatures indicative of metabolic stress. In addition, effector expression is tightly regulated, with the differential deployment of RxLR, NLP, and CRN families across hosts.

Comparative transcriptomics highlights metabolic reprogramming as a key determinant of infection success, with P. capsici fine-tuning its gene expression to exploit host-specific vulnerabilities. These findings provide novel insights into P. capsici adaptive strategies in soil-borne infections and underscore the importance of targeting crown infection sites for disease management. Future research should integrate host transcriptomics and functional studies to elucidate the molecular determinants of host specificity.