Abstract

Acylsugars are a class of plant defense compounds produced across many distantly related families. Members of the horticulturally important morning glory (Convolvulaceae) family produce a diverse subclass of acylsugars called resin glycosides (RGs), which comprise oligosaccharide cores, hydroxyacyl chain(s), and decorating aliphatic and aromatic acyl chains. While many RG structures are characterized, the extent of structural diversity of this class in different genera and species is not known. In this study, we asked whether there has been lineage-specific diversification of RG structures in different Convolvulaceae species that may suggest diversification of the underlying biosynthetic pathways. Liquid chromatography coupled with tandem mass spectrometry (LC–MS/MS) was performed from root and leaf extracts of 26 species sampled in a phylogeny-guided manner. LC–MS/MS revealed thousands of peaks with signature RG fragmentation patterns with one species producing over 300 signals, mirroring the diversity in Solanaceae-type acylsugars. A novel RG from Dichondra argentea was characterized using nuclear magnetic resonance spectroscopy, supporting previous observations of RGs with open hydroxyacyl chains instead of closed macrolactone ring structures. Substantial lineage-specific differentiation in utilization of sugars, hydroxyacyl chains, and decorating acyl chains was discovered, especially among Ipomoea and Convolvulus—the two largest genera in Convolvulaceae. Adopting a computational, knowledge-based strategy, we further developed a high-recall workflow that successfully explained ~72% of the MS/MS fragments, predicted the structural components of 11/13 previously characterized RGs, and partially annotated ~45% of the RGs. Overall, this study improves our understanding of phytochemical diversity and lays a foundation for characterizing the evolutionary mechanisms underlying RG diversification.

中文翻译：

---

利用计算代谢组学阐明牵牛花（旋花科）家族中树脂糖苷酰基糖谱系特异性的多样化

 抽象的

酰糖是一类由许多远亲科产生的植物防御化合物。园艺上重要的牵牛花（旋花科）家族的成员产生多种酰基糖亚类，称为树脂糖苷 (RG)，其中包含寡糖核心、羟基酰基链以及装饰性脂肪族和芳香族酰基链。虽然许多 RG 结构已被表征，但此类在不同属和种中的结构多样性程度尚不清楚。在这项研究中，我们询问不同旋花科物种中 RG 结构是否存在谱系特异性多样化，这可能表明潜在的生物合成途径多样化。以系统发育为指导的方式对 26 个物种的根和叶提取物进行了液相色谱与串联质谱联用 (LC-MS/MS) 分析。 LC-MS/MS 显示了数千个具有标志性 RG 碎片模式的峰，其中一个物种产生了 300 多个信号，反映了茄科型酰基糖的多样性。使用核磁共振波谱对一种来自银蓟的新型 RG 进行了表征，支持了之前对具有开放羟基酰基链而不是闭合大环内酯环结构的 RG 的观察。人们发现，在糖、羟酰基链和装饰酰基链的利用方面存在显着的谱系特异性差异，特别是在旋花科中最大的两个属甘草属和旋花属中。 采用基于知识的计算策略，我们进一步开发了一个高召回率工作流程，成功解释了约 72% 的 MS/MS 片段，预测了 11/13 个先前表征的 RG 的结构成分，并部分注释了约 45% 的片段。 RG。总的来说，这项研究提高了我们对植物化学多样性的理解，并为表征 RG 多样化的进化机制奠定了基础。