Sterol glycosyltransferases (SGTs) catalyze the glycosylation of the free hydroxyl group at C-3 position of sterols to produce sterol glycosides. Glycosylated sterols and free sterols are primarily located in cell membranes where in combination with other membrane-bound lipids play a key role in modulating their properties and functioning. In contrast to most plant species, those of the genus Solanum contain very high levels of glycosylated sterols, which in the case of tomato may account for more than 85% of the total sterol content. In this study, we report the identification and functional characterization of the four members of the tomato (Solanum lycopersicum cv. Micro-Tom) SGT gene family. Expression of recombinant SlSGT proteins in E. coli cells and N. benthamiana leaves demonstrated the ability of the four enzymes to glycosylate different sterol species including cholesterol, brassicasterol, campesterol, stigmasterol, and β-sitosterol, which is consistent with the occurrence in their primary structure of the putative steroid-binding domain found in steroid UDP-glucuronosyltransferases and the UDP-sugar binding domain characteristic for a superfamily of nucleoside diphosphosugar glycosyltransferases. Subcellular localization studies based on fluorescence recovery after photobleaching and cell fractionation analyses revealed that the four tomato SGTs, like the Arabidopsis SGTs UGT80A2 and UGT80B1, localize into the cytosol and the PM, although there are clear differences in their relative distribution between these two cell fractions. The SlSGT genes have specialized but still largely overlapping expression patterns in different organs of tomato plants and throughout the different stages of fruit development and ripening. Moreover, they are differentially regulated in response to biotic and abiotic stress conditions. SlSGT4 expression increases markedly in response to osmotic, salt, and cold stress, as well as upon treatment with abscisic acid and methyl jasmonate. Stress-induced SlSGT2 expression largely parallels that of SlSGT4. On the contrary, SlSGT1 and SlSGT3 expression remains almost unaltered under the tested stress conditions. Overall, this study contributes to broaden the current knowledge on plant SGTs and provides support to the view that tomato SGTs play overlapping but not completely redundant biological functions involved in mediating developmental and stress responses.
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.
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