Exocarp Properties and Transcriptomic Analysis of Cucumber (Cucumis sativus) Fruit Expressing Age-Related Resistance to Phytophthora capsici

Abstract

Very young cucumber (Cucumis sativus) fruit are highly susceptible to infection by the oomycete pathogen, Phytophthora capsici. As the fruit complete exponential growth, at approximately 10–12 days post pollination (dpp), they transition to resistance. The development of age-related resistance (ARR) is increasingly recognized as an important defense against pathogens, however, underlying mechanisms are largely unknown. Peel sections from cucumber fruit harvested at 8 dpp (susceptible) and 16 dpp (resistant) showed equivalent responses to inoculation as did whole fruit, indicating that the fruit surface plays an important role in defense against P. capsici. Exocarp from 16 dpp fruit had thicker cuticles, and methanolic extracts of peel tissue inhibited growth of P. capsici in vitro, suggesting physical or chemical components to the ARR. Transcripts specifically expressed in the peel vs. pericarp showed functional differentiation. Transcripts predominantly expressed in the peel were consistent with fruit surface associated functions including photosynthesis, cuticle production, response to the environment, and defense. Peel-specific transcripts that exhibited increased expression in 16 dpp fruit relative to 8 dpp fruit, were highly enriched (P<0.0001) for response to stress, signal transduction, and extracellular and transport functions. Specific transcripts included genes associated with potential physical barriers (i.e., cuticle), chemical defenses (flavonoid biosynthesis), oxidative stress, penetration defense, and molecular pattern (MAMP)-triggered or effector-triggered (R-gene mediated) pathways. The developmentally regulated changes in gene expression between peels from susceptible- and resistant- age fruits suggest programming for increased defense as the organ reaches full size.

Developmentally regulated activation of defense allows for rapid inhibition of infection in age-related resistance to Phytophthora capsici in cucumber fruit

“…Our previous ARR studies [6,[13][14][15] examined 'Vlaspik', an F 1 hybrid commonly grown for processing cucumber production in the midwestern USA. To facilitate future analyses, we sought to identify a homozygous inbred cultivar expressing ARR.…”

“…One model system for organ specific ARR is cucumber fruit rot by the oomycete Phytophthora capsici [13][14][15]. This soilborne hemibiotroph is a pathogen of many agriculturally important crops including numerous solanaceous and cucurbit species [16].…”

“…Further studies showed that the cucumber fruit peel is important for ARR [14]. Excised peels exhibit equivalent responses (susceptible or resistant) as do intact whole fruit, and if the peel is wounded or removed from resistant-aged fruit the underlying tissue is highly susceptible [14].…”

“…Excised peels exhibit equivalent responses (susceptible or resistant) as do intact whole fruit, and if the peel is wounded or removed from resistant-aged fruit the underlying tissue is highly susceptible [14]. Furthermore, methanolic extracts from resistant-aged peels had inhibitory effects on pathogen growth and cucumber peels of resistant-aged fruit vs. susceptible age are enriched for genes associated with defense against biotic and abiotic stresses [14]. ARR to P. capsici also has been observed in whole pepper plants [4], chile pepper fruit [23], and several cucurbit fruits [6,10].…”

Cucumber (Cucumis sativus) Breeding Line with Young Fruit Resistance to Infection by Phytophthora capsici

“…in the eastern and midwestern United States is subject to severe losses due to fruit rot caused by the soilborne oomycete pathogen, Phytophthora capsici (Granke et al, 2012;Sonogo and Ji, 2012). P. capsici preferentially infects cucumber fruits, especially young fruit, while leaves and vines remain healthy (Ando et al, 2009(Ando et al, , 2015Gevens et al, 2006). Disease is manifested by extensive mycelial growth, sporulation, fruit rot, and tissue collapse.…”