The fate of a Solanum steroidal alkaloid toxin in the cabbage looper (Trichoplusia ni)

Abstract

Plants produce complex chemical defenses against herbivores, resulting in the emergence of detoxification strategies in phytophagous insects. While enzymatic detoxification and target site mutagenesis are well-documented, the quantitative contribution of excretion remains less studied. We focus on the cabbage looper (Trichoplusia ni), a generalist herbivore, to elucidate the detoxification of a steroidal alkaloid, solanidine, produced in potato (Solanum tuberosum). Through larval feeding experiments and chemical analysis of metabolites using high-resolution mass spectrometry, we identify solanidine 3-O-β-glucopyranoside and solanidine 3-phosphate as major metabolization products of solanidine. Glycosylation and phosphorylation reactions have not previously been observed in cabbage looper. Modified solanidine derivatives exhibit reduced lipophilicity, preventing passive transport as predicted by physicochemical analyses, and only solanidine was detected in body tissue. In addition, the metabolism of solanidine in a T. ni mutant strain with midgut cadherin protein knocked out was also investigated to examine the potential role of the cadherin, an important receptor for Bt toxins, in steroidal alkaloid detoxification. T. ni cadherin-knockout strain showed lower solanidine conversion (33.9% ± 2.2) and uptake (27.41 ± 0.49 nmol/g) compared to the wild-type strain (51.3% ± 4.1, 33.66 ± 2.48 nmol/g) but similar excretion kinetics. Although solanidine negatively impacted the feeding performance of both strains the cadherin-knockout does not affect the feeding performance. Our study expands the metabolization enzyme repertoire in cabbage loopers, emphasizing the complexity of detoxification mechanisms in generalist herbivores.