Inactivation of UDP-Glucose Sterol Glucosyltransferases Enhances Arabidopsis Resistance to Botrytis cinerea

Abstract

Free and glycosylated sterols are both structural components of the plasma membrane that regulate their biophysical properties and consequently different plasma membrane-associated processes such as plant adaptation to stress or signaling. Several reports relate changes in glycosylated sterols levels with the plant response to abiotic stress, but the information about the role of these compounds in the response to biotic stress is scarce. In this work, we have studied the response to the necrotrophic fungus Botrytis cinerea in an Arabidopsis mutant that is severely impaired in steryl glycosides biosynthesis due to the inactivation of the two sterol glucosyltransferases (UGT80A2 and UGT80B1) reported in this plant. This mutant exhibits enhanced resistance against B. cinerea when compared to wild-type plants, which correlates with increased levels of jasmonic acid (JA) and up-regulation of two marker genes (PDF1.2 and PR4) of the ERF branch of the JA signaling pathway. Upon B. cinerea infection, the ugt80A2;B1 double mutant also accumulates higher levels of camalexin, the major Arabidopsis phytoalexin, than wild-type plants. Camalexin accumulation correlates with enhanced transcript levels of several cytochrome P450 camalexin biosynthetic genes, as well as of their transcriptional regulators WRKY33, ANAC042, and MYB51, suggesting that the Botrytis-induced accumulation of camalexin is coordinately regulated at the transcriptional level. After fungus infection, the expression of genes involved in the indole glucosinolate biosynthesis is also up-regulated at a higher degree in the ugt80A2;B1 mutant than in wild-type plants. Altogether, the results of this study show that glycosylated sterols play an important role in the regulation of Arabidopsis response to B. cinerea infection and suggest that this occurs through signaling pathways involving the canonical stress-hormone JA and the tryptophan-derived secondary metabolites camalexin and possibly also indole glucosinolates.

Cryptococcus neoformans Δsgl1 Vaccination Requires Either CD4+ or CD8+ T Cells for Complete Host Protection

“…Collectively, these studies suggest that SGs induce T cell proliferation, direct Th1 cell differentiation, and induce earlier host recognition leading to rapid recruitment of innate immunity. However, the majority of the vaccination studies utilizing SGs have been performed using plants ( Thuan et al., 2013 ; Singh et al., 2016 ; Castillo et al., 2019 ) or purified SGs as a standalone compound prior to infection to induce a protective immune response, not as a simultaneous immunoadjuvant present during the active infection stage ( Lee and Han, 2006 ; Lee et al., 2007 ).…”

Molecular mechanism of modulating miR482b level in tomato with botrytis cinerea infection

“…6). On the contrary, PDF1.2 would be induced by B. cinerea to activate JA pathway for increasing the resistance in Arabidopsis [28]. In addition, a similar expression pattern was observed for PR4, which is another JAresponsive gene of the ERF branch and its expression levels could be induced by necrotrophic pathogen [52], but was also decreased in pri-miR482b OE plants compared to WT.…”

“…The jasmonic acid-mediated defense pathway has an important role in plant resistance against necrotrophic pathogens [48]. There are two distinct branches in Arabidopsis JA pathway including ethylene response factor (ERF) branch and the MYC branch [28]. The ERF branch of the JA pathway is typically activated upon infection by necrotrophic pathogens [49].…”

“…Moreover, the necrotic spots of pri-miR482b-x1 OE plants were ~2 fold larger than those of pri-miR482b-x2 OE plants. In addition, two marker genes, plant defensing 1.2 (PDF1.2) and pathogen related protein 4 (PR4) [28], of the ERF branch of the jasmonic acid signaling pathway were quantitative detected in WT and transgenic plants. The results showed that the expression of both genes was downregulated in transgenic pri-miR482b OE plants compared with wide type plants.…”

Steryl Glycosides in Fungal Pathogenesis: An Understudied Immunomodulatory Adjuvant

“…The authors concluded that silencing SGTs resulted in a positive feedback regulation of withanolide biosynthesis, leading to reduced biotic stress tolerance. In conflict with these results, a 2019 study by Castillo and colleagues [81] reported that inactivation of the SGT enzymes in Arabidopsis plants enhanced the resistance to the necrotrophic fungus Botrytis cinerea. The authors showed that the mutant strain of Arabidopsis that cannot produce SGs was more resistant to infection with B. cinerea due to an increase in plant stress response factors to combat the infection.…”