TY - JOUR

T1 - The saponin bomb

T2 - a nucleolar-localized β-glucosidase hydrolyzes triterpene saponins in Medicago truncatula

AU - Lacchini, Elia

AU - Erffelinck, Marie-Laure

AU - Mertens, Jan

AU - Marcou, Shirley

AU - Molina-Hidalgo, Francisco Javier

AU - Tzfadia, Oren

AU - Venegas-Molina, Jhon

AU - Cárdenas, Pablo D

AU - Pollier, Jacob

AU - Tava, Aldo

AU - Bak, Søren

AU - Höfte, Monica

AU - Goossens, Alain

N1 - © 2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.

PY - 2023

Y1 - 2023

N2 - 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 β-glucosidase, 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 two-component 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.

AB - 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 β-glucosidase, 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 two-component 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.

U2 - 10.1111/nph.18763

DO - 10.1111/nph.18763

M3 - Journal article

C2 - 36683446

VL - 239

JO - New Phytologist

JF - New Phytologist

SN - 0028-646X

IS - 2

ER -