Sclerotinia sclerotiorum Circumvents Flavonoid Defenses by Catabolizing Flavonol Glycosides and Aglycones

Abstract

Flavonols are widely distributed plant metabolites that inhibit microbial growth. Yet many pathogens cause disease in flavonolcontaining plant tissues. We investigated how Sclerotinia sclerotiorum, a necrotrophic fungal pathogen that causes disease in a range of economically important crop species, is able to successfully infect flavonol-rich tissues of Arabidopsis (Arabidopsis thaliana). Infection of rosette stage Arabidopsis with a virulent S. sclerotiorum strain led to the selective hydrolysis of flavonol glycosidic linkages and the inducible degradation of flavonol aglycones to phloroglucinol carboxylic and phenolic acids. By chemical analysis of fungal biotransformation products and a search of the S. sclerotiorum genome sequence, we identified a quercetin dioxygenase gene (QDO) and characterized the encoded protein, which catalyzed cleavage of the flavonol carbon skeleton. QDO deletion lines degraded flavonols with much lower efficiency and were less pathogenic on Arabidopsis leaves than wild-type S. sclerotiorum, indicating the importance of flavonol degradation in fungal virulence. In the absence of QDO, flavonols exhibited toxicity toward S. sclerotiorum, demonstrating the potential roles of these phenolic compounds in protecting plants against pathogens.

Contribution of phenylpropanoid metabolism to plant development and plant–environment interactions

“…Additionally, overexpression of F3H resulted in higher levels of flavonols such as kaempferol, isorhamnetin, and syringetin, reducing the oxidative damage and susceptibility to Colletotrichum sublineola , which is the causal agent of anthracnose in sorghum ( Sorghum bicolor ) (Wang et al, 2020b). Arabidopsis thaliana plants with deletion of the gene encoding quercetin dioxygenase, which catalyzes the cleavage of the flavonol carbon skeleton, exhibit lower efficiency of flavonol degradation, and the resulting high level of flavonol is toxic to Sclerotinia sclerotiorum , a fungal pathogen that causes disease in diverse crops (Chen et al, 2019a). Flavones function as phytoalexins in plant defense (Jiang et al, 2016).…”

Metabolome and Transcriptome Analysis of the Response Mechanisms of Ginseng to Rust Root Symptoms

“…The phenolic content is often considered closely related to the total antioxidant capacity of plant tissues [34]. Studies have shown that avonoids are also one of the main chemical defense substances in plants and can reduce various forms of reactive oxygen species in plant cells, which are usually produced in response to external environmental stresses such as light intensity, temperature, and soil moisture [35]. Besides, it is also an active substance involved in plant-microbe interactions [36].…”

Transcriptional response to host chemical cues underpins expansion of host range in a fungal plant pathogen lineage

“…While there are more than 10,000 flavonoid structures, S. sclerotiorum may use a conserved pathway to tackle these toxins. Indeed, the quercetin dioxygenase SsQDO (Sscle07g059700) catalyzes the cleavage of the flavonol carbon skeleton, thus targeting a range of flavonoids (Chen et al, 2019). This gene was strongly induced on sunflower, common bean and castor bean in our dataset.…”