Comparative transcriptome profiling reveals the role of phytohormones and phenylpropanoid pathway in early-stage resistance against powdery mildew in watermelon (Citrullus lanatus L.)

Abstract

Yield and fruit quality loss by powdery mildew (PM) fungus is a major concern in cucurbits, but early-stage resistance mechanisms remain elusive in the majority of cucurbits. Here, we explored the comparative transcriptomic dynamics profiling of resistant line ZXG1755 (R) and susceptible line ZXG1996 (S) 48 h post-inoculation in watermelon seedlings to check precise expression changes induced by Podosphaera. xanthii race ‘2F’. Phenotypic responses were confirmed by microscopy and endogenous levels of defense and signaling related phytochromes were detected higher in resistant lines. In total, 7642 differently expressed genes (DEGs) were detected, and 57.27% of genes were upregulated in four combinations. DEGs were predominantly abundant in the KEGG pathway linked with phenylpropanoid biosynthesis, plant hormone and transduction, and phenylalanine metabolism, whereas GO terms of defense response, response to fungus, and chitin response were predominant in resistant lines, evidencing significant defense mechanisms and differences in the basal gene expression levels between these contrasting lines. The expression of selected DEGs from major pathways (hormonal, lignin, peroxidase, sugar) were validated via qRT-PCR. Detailed analysis of DEGs evidenced that along with other DEGs, genes including PR1 (Cla97C02G034020) and PRX (Cla97C11G207220/30, Cla97C02G045100 and Cla97C02G049950) should be studied for their potential role. In short, our study portrayed strong evidence indicating the important role of a complex network associated with lignin biosynthesis and phytohormone related downstream mechanisms that are responsible for incompatible interaction between PM and watermelon resistance line.

Transcriptomic Analysis of the Response of Susceptible and Resistant Bitter Melon (Momordica charantia L.) to Powdery Mildew Infection Revealing Complex Resistance via Multiple Signaling Pathways

“…A precedent set by a wheat study elucidates the accumulation of transcripts from monolignol genes in the resistant strains upon PM infection [ 18 , 50 , 51 ]. This pattern echoes in instances such as watermelon powdery mildew interactions, where there is a conspicuous upregulation of genes related to defense mechanisms [ 36 ]. Our research findings shed light on the amplified expression of PAL genes in the R_all vs. R_0 comparison.…”

“…It is noteworthy that this finding resonates with previous transcriptomic explorations conducted with cucumber, watermelon, and tobacco. These antecedent investigations similarly unveiled that resistant strains tend to manifest an enhanced DEG expression profile when juxtaposed with their susceptible counterparts during the ordeal of biotic stress [ 33 , 34 , 36 ].…”

“…Likewise, there is a documented surge in peroxidase activities in Pichia galeiformis -infected citrus plants [ 63 ]. Recent research in watermelon and melon underscores the induction of a plethora of peroxidase-encoding genes in resistant lines, while their counterparts in susceptible lines maintain a neutral stance following PM infection [ 36 , 64 ]. Interestingly, this investigation reveals the identification of a total of 22 DEGs that differentiate between resistant and susceptible lines, in which there is a remarkable upregulation of the majority of PRX genes in the resilient category.…”

“…This investigative avenue has extended to encompass the defensive responses of mango against Colletotrichum gloeosporioides [ 31 ], tomato against Phytophthora parasitica [ 32 ], and tobacco against Phytophthora nicotianae [ 33 ]. Contemporary focus has converged on transcriptomic inquiries targeting cucurbit species such as cucumber, watermelon, and melon—deciphering their inherent resilience to PM [ 34 , 35 , 36 ].…”

Transcriptome Analyses Revealed the Wax and Phenylpropanoid Biosynthesis Pathways Related to Disease Resistance in Rootstock-Grafted Cucumber

“…They found that low-temperature stress regulated the transcript levels of genes related to phenylalanine metabolism, the phytohormone ethylene, photosynthesis, flavonoid accumulation, lignin synthesis, cells, cycleactive gibberellin, and salicylic acid (SA) signaling in cucumber seedlings. Yadav [ 46 ] employed transcriptome sequencing to identify genes related to phytohormones and found that the phenylpropanoid pathway was involved in resistance to powdery mildew disease in watermelon. Genes related to the phenylpropanoid pathway were transcriptionally up-regulated in resistant cucumber lines.…”