The saponin bomb: a nucleolar‐localized β‐glucosidase hydrolyzes triterpene saponins in Medicago truncatula

Abstract

 Plants often protect themselves from their own bioactive defense metabolites by storing them in less active forms. Consequently, plants also need systems allowing correct spatiotemporal reactivation of such metabolites, for instance under pathogen or herbivore attack.  Via co-expression analysis with public transcriptomes, we determined that the model legume Medicago truncatula has evolved a two-component system composed of a βglucosidase, denominated G1, and triterpene saponins, which are physically separated from each other in intact cells. G1 expression is root-specific, stress-inducible, and coregulated with that of the genes encoding the triterpene saponin biosynthetic enzymes. However, the G1 protein is stored in the nucleolus and is released and united with its typically vacuolar-stored substrates only upon tissue damage, partly mediated by the surfactant action of the saponins themselves. Subsequently, enzymatic removal of carbohydrate groups from the saponins creates a pool of metabolites with an increased broad-spectrum antimicrobial activity. The evolution of this defense system benefited from both the intrinsic condensation abilities of the enzyme and the bioactivity properties of its substrates. We dub this twocomponent system the saponin bomb, in analogy with the mustard oil and cyanide bombs, commonly used to describe the renowned β-glucosidase-dependent defense systems for glucosinolates and cyanogenic glucosides.

Multiple horizontal gene transfer events have shaped plant glycosyl hydrolase diversity and function

“…GH1 hydrolases are often involved in the processing of glycosylated aromatics such as saponins (Lacchini et al ., 2023), plant hormones stored in inactive glycosylated forms (Kato‐Noguchi & Tanaka, 2008), and monolignol glucosides in the process of lignification (Escamilla‐Treviño et al ., 2006). GH1 enzymes are also part of plant antifeedant system that releases toxic aglycons, like the Sinapis alba myrosinase (Burmeister et al ., 1997) and Trifolium repens beta‐glucosidase (Boersma et al ., 1983).…”

Trichoplusia ni Transcriptomic Responses to the Phytosaponin Aglycone Hederagenin: Sex-Related Differences

“…However, detoxification enzymes not only metabolize plant specialized metabolites but also other xenobiotics such as insecticides. Indeed, sex-linked resistance has been identified in a number of insect species (examples: Heckel et al 1998 ; Kanga et al 2001 ; Reyes and Sauphanor 2008 ; Banazeer et al 2022 ). Thus, identifying sex-specific detoxification genes and understanding their links to resistance strategies has important implications for pesticide management and sustainable agricultural practices.…”

Comparative transcriptome analysis reveals key pathways and regulatory networks in early resistance of Glycine max to soybean mosaic virus

“…They can also interact with other signaling molecules, including hormones, to control plant growth and development ( Rolland et al, 2006 ; Smeekens et al, 2010 ). Among the DEGs enriched in starch and sucrose metabolism, BGLU genes encoding β-glucosidase are involved in several physiological processes as follows: cell wall catabolism ( Patro et al, 2014 ), cell wall lignification ( Dos Santos et al, 2019 ), defense compound activation ( Lacchini et al, 2023 ), plant hormone activation ( Han et al, 2020 ), and release of aromatic volatiles ( Sun Y. et al, 2023 ). As a PR protein belonging to the PR-2 family, one member of GmBGLU (Glyma.15G142400) interacts with a Phakopsora pachyrhizi effector, suppressing PTI and promoting virulence ( Bueno et al, 2022 ).…”