Resistance in the Plant, Barbarea vulgaris, and Counter-Adaptations in Flea Beetles Mediated by Saponins

Abstract

Three saponins and two sapogenins had differential effects on food consumption in five near-isogenic flea beetle lines, which differ in their ability to utilize a novel host plant, Barbarea vulgaris (Brassicaceae). The ability to live on this plant is controlled by major, dominant R-genes in the flea beetle, Phyllotreta nemorum (Coleoptera: Chrysomelidae: Alticinae). A susceptible genotype (rr) is unable to live on the plant, whereas resistant genotypes (RR and Rr) can utilize the novel host plant. Among compounds isolated from B. vulgaris, hederagenin cellobioside (hederagenin-3-O-(4-O-beta-D-glucopyranosyl)-beta-D-glucopyranoside) inhibited feeding, whereas the effect of oleanolic acid cellobioside was much weaker. The aglycones (sapogenins) were inactive. Although hederagenin cellobioside was active against all flea beetle lines, its effect on food consumption was much stronger on the susceptible genotype (rr) compared to the resistant genotype (Rr). Susceptible and resistant flea beetle genotypes were equally sensitive to a non-host saponin, alpha-hederin (hederagenin-3-O-(2-O-alpha-L-rhamnopyranosyl)-alpha-L-arabinopyranoside). These results suggest that R-alleles in flea beetles might be specific adaptations to defensive saponins in B. vulgaris. A possible mechanism of action of the R-alleles might be to encode for an enzyme (e.g. a glucosidase), which is able to cleave glycosidic bonds in hederagenin cellobioside, but not in alpha-hederin. The potential role of saponins as defensive compounds in B. vulgaris and as targets for counter-adaptations in flea beetles and other insects is discussed.

UDP-Glycosyltransferases from the UGT73C Subfamily in Barbarea vulgaris Catalyze Sapogenin 3-O-Glucosylation in Saponin-Mediated Insect Resistance

“…Alternatively, glucosylated saponins may have a more adverse taste for insects than the corresponding sapogenins (Glendinning, 2002); however, P. nemorum larvae die from exposure to G-type leaves (Nielsen, 1997a). Nielsen et al (2010) suggested that cleavage of the b-1,4-glycosidic bond in the cellobiosides by bglucosidases allows resistant P. nemorum lines to feed on G-type B. vulgaris. This mechanism would be similar to what has been found for fungal adaptation to saponins (Osbourn et al, 1991;Wubben et al, 1996;Pareja-Jaime et al, 2008).…”

“…The resistance of G-type B. vulgaris against herbivorous insects, such as P. xylostella and susceptible P. nemorum, has previously been shown to depend on the presence of saponins, and especially hederagenin and oleanolic acid cellobioside, which are absent in the susceptible P-type (Shinoda et al, 2002;Agerbirk et al, 2003a;Kuzina et al, 2009;Nielsen et al, 2010). Therefore, the synthesis of saponins was initially thought to be unique to the G-type.…”

“…Nonchoice feeding assays were performed as described previously by Nielsen et al (2010). Briefly, purified 3-O-b-D-Glc hederagenin and 3-O-b-DGlc oleanolic acid were in final concentrations of 2, 0.5, and 0.125 mM dissolved in 75% ethanol.…”

Phytochemical and TLC Profiling of Oroxylum indicum and Milletia pachycarpa

“…The presence of cardiac glycosides reaffirms their use a traditional medicine.Saponins are produced by plants to protect them against pathogens and herbivory. They have been found to kill fungus, insects and molluscs that attack plants and also act as allelopathic [62][63][64]. Saponins also act as anticancerous, and antiangiogenic agents and have been reported to inhibit the progression of the cell cycle and induce apoptosis [65].…”

“…Saponins also act as anticancerous, and antiangiogenic agents and have been reported to inhibit the progression of the cell cycle and induce apoptosis [65]. The other activities attributed to saponins include antioxidant, anticarcinogenic, immunostimulatory, antibacterial, antifungal, antiviral, antiprotozoal, hypoglycemic, hemolytic, immune adjuvant and membrane permeabilizing [62,63,64]. The saponins were present in all the extracts of O. indicum, and M. pachycarpa, except the chloroform extract of the former.…”