Comparative analysis of powdery mildew resistant and susceptible cultivated cucumber (Cucumis sativus L.) varieties to reveal the metabolic responses to Sphaerotheca fuliginea infection

Abstract

Background Cucumber (Cucumis sativus L.) is a widely planted vegetable crop that suffers from various pathogen infections. Powdery mildew (PM) is typical disease caused by Sphaerotheca fuliginea infection and destroys the production of cucumber. However, the metabolic responses to S. fuliginea infection are largely unknown. Results In our study, a PM resistant variety ‘BK2’ and a susceptible variety ‘H136’ were used to screen differentially accumulated metabolites (DAMs) and differentially expressed genes (DEGs) under S. fuliginea infection. Most of DEGs and DAMs were enriched in several primary and secondary metabolic pathways, including flavonoid, hormone, fatty acid and diterpenoid metabolisms. Our data showed that many flavonoid-related metabolites were significantly accumulated in BK2 rather than H136, suggesting an essential role of flavonoids in formation of resistant quality. Changes in expression of CYP73A, CYP81E1, CHS, F3H, HCT and F3’M genes provided a probable explanation for the differential accumulation of flavonoid-related metabolites. Interestingly, more hormone-related DEGs were detected in BK2 compared to H136, suggesting a violent response of hormone signaling pathways in the PM-resistant variety. The number of fatty acid metabolism-related DAMs in H136 was larger than that in BK2, indicating an active fatty acid metabolism in the PM-susceptible variety. Conclusions Many differentially expressed transcription factor genes were identified under S. fuliginea infection, providing some potential regulators for the improvement of PM resistance. PM resistance of cucumber was controlled by a complex network consisting of various hormonal and metabolic pathways.

Research Advances in Genetic Mechanisms of Major Cucumber Diseases Resistance

“…In the recent years, candidate genes or proteins associated with PM resistance have been identified using transcriptomic and proteomic analyses and genetic mapping. Differentially expressed genes (DEGs) have been identified between PM-resistant species and susceptible species, such as SSL508-28 and D8, XY09-118 and Q10, BK2 and H136, and NILs of S1003 and Near Iso-genic Lines (NIL) ( pm5.1 ), using transcriptomes ( Xu et al, 2017 ; Nie et al, 2021 ; Zhang P. et al, 2021 ; Zheng et al, 2021 ). These DEGs function in plant hormone signal transduction, phenylpropanoid biosynthesis, phenylalanine metabolism, ubiquinone and other terpenoid-quinone biosynthesis, endocytosis, plant–pathogen interaction, and Mitogen-activated Protein Kinases (MAPKS).…”

“…These DEGs function in plant hormone signal transduction, phenylpropanoid biosynthesis, phenylalanine metabolism, ubiquinone and other terpenoid-quinone biosynthesis, endocytosis, plant–pathogen interaction, and Mitogen-activated Protein Kinases (MAPKS). In particular, genes encoding the transcriptome factors (WRKY, NAC, and TCP), peroxidase, nucleotide-binding site (NBS), glucanase, and chitinase have been analyzed ( Zhang P. et al, 2021 ; Zheng et al, 2021 ). The miRNAs Csa-miR172c-3p and Csa-miR395a-3p are upregulated in PM-resistant D8 and Csa-miR395d-3p and Csa-miR398b-3p are downregulated in PM-susceptible SSSL508-28, suggesting that their target genes AP2 , bHLH , Dof , UGT , and LASPO may play important roles in PM-inoculated cucumber leaves ( Xu et al, 2020 ).…”

“… Nie et al (2021) showed that 49 differentially expressed lncRNAs may function as target mimics for 106 miRNAs during cucumber_PM interaction, including miR156 , miR159 , miR164 , miR166 , miR169 , miR171 , miR172 , miR6173, miR319 , miR390, miR393 , miR396 , and miR5658 . Moreover, differentially regulated processes, proteins, and accumulated metabolites between different PM-resistant materials have also been detected, including flavonoid, hormones, fatty acid, diterpenoid metabolism, tetrapyrrole biosynthetic process, sulfur metabolic process, and cell redox homeostasis ( Xu et al, 2019 ; Zhang P. et al, 2021 ).…”

Increasing the activities of protective enzymes is an important strategy to improve resistance in cucumber to powdery mildew disease and melon aphid under different infection/infestation patterns

“…In the cucumber-powdery mildew system, early studies showed that cucumber plants were able to resist infection by the powdery mildew pathogen by regulating the metabolism and synthesis of chlorophyll and osmoregulatory substance ( Wang H. Z. et al, 2006 ; Jiang and Si, 2010 ). Several recent studies have described the epidemiology, host specificity, and genome of cucumber powdery mildew pathogens ( Berg et al, 2015 ; Zhang P. et al, 2021 ). In the cucumber-melon aphid system, cucumber plants resist damage from melon aphids by regulating the activities of peroxidase (POD), polyphenol oxidase (PPO), and phenylalanine ammonia lyase (PAL) ( Gao et al, 2017 ).…”

Antifungal activity of l‐azetidine‐2‐carboxylic acid isolated from Disporopsis aspera rhizomes against Podosphaera xanthii

“…Fungicides could impact non‐target or beneficial microorganisms, altering ecological balance required for sustainable agricultural development. Breeding cucumber cultivars resistant to Podosphaera xanthii is time‐consuming 11,12 . Even though cucumber cultivars with resistance to Podosphaera xanthii are available, the resistance can be broken down over time if the pathogen develops a new race.…”