Fruit rot of winter squash and pumpkin (Cucurbita moschata) caused by the oomycete plant pathogen Phytophthora capsici is a limiting factor in the production of these crops. Genetic resistance to fruit rot is not available in commercial cultivars, but age-related resistance (ARR) develops in certain cultivars of C. moschata which may benefit management strategies. Earlier ARR studies indicate that the peel provides fruit resistance. The goal of this research was to elucidate the structural, biochemical and genetic basis of ARR of the winter squash fruit peel to P. capsici. Five C. moschata cultivars were evaluated for P. capsici resistance 10, 14, 16, 18, and 21 days post pollination (dpp). The onset of resistance was variable among cultivars. A cultivar with ARR at 14 dpp was selected and the fruit exocarp cell wall examined 7 dpp (susceptible) and 14 dpp, 21 dpp (resistant) using scanning electron microscopy (SEM). An increase in cuticle and epidermal walls thickness as the fruit age increased was observed. According to SEM observations, P. capsici caused cell wall degradation/tissue collapse to the 7 dpp fruit within 48- hour post inoculation (hpi) while 14 and 21 dpp fruit remained unaffected suggesting a structural barrier to P. capsici in resistant fruit. The contribution of fruit exocarp preformed or induced chemical defense against the pathogen was examined in C. moschata cultivars across developmental stages using phytochemical analysis. Results showed a decrease in antifungal activity in non-inoculated fruit peel as the fruit age increased. A significant change in antifungal activity was not observed under induced conditions with inoculation of the fruit peel with P. capsici, suggesting that there is not a correlation between preformed or induced chemical defense and winter squash fruit ARR to P. capsici. Transcriptome profiling of fruit peel of two C. moschata cultivars at susceptible and resistant developmental stages was performed to uncover the molecular mechanism of ARR. Differential gene expression analysis detected upregulation of multiple genes in the resistant compared to the susceptible stages then functional enrichment analysis detected overrepresentation of these genes in cell wall structures biosynthesis. Pathway enrichment analysis of winter squash orthologous genes detected enrichment in cutin, suberin monomers and phenylpropanoids biosynthetic pathways. Further analysis of genes expression profile in those pathways suggests enrichment in monolignol biosynthesis in the resistant fruit peel.
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