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

Phytophthora capsici is a destructive, broad-host oomycete that causes major agricultural losses. Yet how this generalist pathogen tailors its infection program to different plant species, especially at its natural entry site remains poorly understood. We profiled P. capsici during early crown infection of four hosts representing distinct compatibility outcomes (cucumber, melon, chili pepper CM334, and tomato) using pathogen-centered RNA-seq and microscopy. Disease progression and necrosis diverged sharply: tomato collapsed by 27 hpi, followed by melon (54 hpi), cucumber (102 hpi), and chili pepper (120 hpi). Pathogen transcriptomes were strongly host-dependent, with 4470 differentially expressed genes but only a small conserved core shared across hosts (436 induced; 415 repressed). In rapidly collapsing tomato infections, the pathogen upregulated glycolysis and fatty-acid metabolism and repressed HR-associated elicitin INF2B. In cucurbit infections, expression patterns were consistent with prolonged biotrophy, including increased carbohydrate metabolism, transport processes, and nutrient acquisition. In partially resistant CM334, pathogen profiles indicated constrained early colonization, with metabolic stress, cell wall remodeling, and broad effector repression. Co-expression analysis identified modules linked to colonization, nutrient exploitation, and pathogenesis/defense-related functions. dsRNA-mediated silencing supported these patterns: silencing Pc18476 and Pc9358 reduced pathogen growth on cucumber leaves (∼78% and ∼65%), and in stem assays reduced growth and/or prevented necrosis in CM334 and tomato. Together, these findings show that P. capsici achieves broad host range by dynamically tuning effector deployment and metabolism to host-specific constraints, resulting in divergent infection outcomes during early crown invasion.