Adaptive transcriptional strategies underpin the host-specific virulence of the generalist oomycete Phytophthora capsici during early crown infection

Abstract

Phytophthora capsici is a destructive, broad-host-range oomycete responsible for substantial losses in global agriculture. While most transcriptomic studies have focused on host responses, the mechanisms by which generalist pathogens dynamically adapt their infection programs to diverse plant species remain poorly understood. Here, we present a comparative transcriptomic analysis of P. capsici during early-stage crown infection in four taxonomically and immunologically distinct hosts, Cucumis sativus, Cucumis melo, Capsicum annuum (CM334), and Solanum lycopersicum, via RNA-seq and multiphoton microscopy. Focusing on crown infections, the natural entry point for the pathogen, we reveal host-specific transcriptional programs that underpin differential infection strategies and outcomes. Our data show that P. capsici exhibits tightly regulated, host-dependent deployment of key virulence factors, including RxLR, NLP, and CRN, and elicitin effectors and reprograms its metabolism to exploit host-specific nutritional environments. In rapidly necrotizing hosts such as tomato, the pathogen induces glycolytic and fatty acid pathways while repressing immunogenic effectors. In contrast, cucurbits support prolonged biotrophic colonization, accompanied by the upregulation of carbohydrate metabolism and membrane transport genes. In the partially resistant chili pepper CM334, P. capsici shows signs of metabolic stress, cell wall remodeling, and effector repression, which is consistent with failed invasion. Functional validation via RNAi-mediated silencing of selected effectors revealed distinct roles in modulating virulence and host necrosis, confirming the functional relevance of the transcriptomic profiles. Co-expression network analysis uncovered discrete transcriptional modules associated with tissue-specific colonization, nutrient acquisition, and immune evasion. These results reveal how a generalist soil-borne pathogen finely tunes its gene expression in response to host-specific constraints, revealing conserved and host-specific transcriptional strategies that drive infection success or failure. This work provides mechanistic insight into adaptive virulence and expands our understanding of host-pathogen compatibility in eukaryotic microbes.