The Oomycete plant pathogen, Phytophthora capsici, causes root, crown, and fruit rot of winter squash (Cucurbita moschata) and limits production. Some C. moschata cultivars develop age-related resistance (ARR), whereby fruit develop resistance to P. capsici 14 to 21 days postpollination (DPP) because of thickened exocarp; however, wounding negates ARR. We uncovered the genetic mechanisms of ARR of two C. moschata cultivars, Chieftain and Dickenson Field, that exhibit ARR at 14 and 21 DPP, respectively, using RNA sequencing. The sequencing was conducted using RNA samples from ‘Chieftain’ and ‘Dickenson Field’ fruit at 7, 10, 14, and 21 DPP. A differential expression and subsequent gene set enrichment analysis revealed an overrepresentation of upregulated genes in functional categories relevant to cell wall structure biosynthesis, cell wall modification/organization, transcription regulation, and metabolic processes. A pathway enrichment analysis detected upregulated genes in cutin, suberin monomer, and phenylpropanoid biosynthetic pathways. A further analysis of the expression profile of genes in those pathways revealed upregulation of genes in monolignol biosynthesis and lignin polymerization in the resistant fruit peel. Our findings suggest a shift in gene expression toward the physical strengthening of the cell wall associated with ARR to P. capsici. These findings provide candidate genes for developing Cucurbita cultivars with resistance to P. capsici and improve fruit rot management in Cucurbita species.
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