Glutathione transferases catalyze recycling of auto‐toxic cyanogenic glucosides in sorghum. (19th May 2018)

• Record Type: Journal Article
• Authors: Bjarnholt, Nanna; Neilson, Elizabeth H. J.; Crocoll, Christoph; Jørgensen, Kirsten; Motawia, Mohammed Saddik; Olsen, Carl Erik; Dixon, David P.; Edwards, Robert; Møller, Birger Lindberg
• Is Part Of: Plant journal. Volume 94:Number 6(2018)
• Page Start: 1109
• Page End: 1125
• Publication Date: 2018-05-19
• Subjects: nitrilases -- cyanogenic glucosides -- dhurrin -- glutathione transferases -- resource allocation -- Sorghum bicolor; Plant molecular biology -- Periodicals; Plant cells and tissues -- Periodicals; Botany -- Periodicals; 580
• DOI: 10.1111/tpj.13923
• Languages: English
• ISSNs: 0960-7412

Abstract

Summary: Cyanogenic glucosides are nitrogen‐containing specialized metabolites that provide chemical defense against herbivores and pathogens via the release of toxic hydrogen cyanide. It has been suggested that cyanogenic glucosides are also a store of nitrogen that can be remobilized for general metabolism via a previously unknown pathway. Here we reveal a recycling pathway for the cyanogenic glucoside dhurrin in sorghum ( Sorghum bicolor ) that avoids hydrogen cyanide formation. As demonstrated in vitro, the pathway proceeds via spontaneous formation of a dhurrin‐derived glutathione conjugate, which undergoes reductive cleavage by glutathione transferases of the plant‐specific lambda class (GSTLs) to produce p ‐hydroxyphenyl acetonitrile. This is further metabolized to p ‐hydroxyphenylacetic acid and free ammonia by nitrilases, and then glucosylated to form p ‐glucosyloxyphenylacetic acid. Two of the four GSTLs in sorghum exhibited high stereospecific catalytic activity towards the glutathione conjugate, and form a subclade in a phylogenetic tree of GSTLs in higher plants. The expression of the corresponding two GSTLs co‐localized with expression of the genes encoding the p ‐hydroxyphenyl acetonitrile‐metabolizing nitrilases at the cellular level. The elucidation of this pathway places GSTs as key players in a remarkable scheme for metabolic plasticity allowing plants to reverse the resource flow between general and specialized metabolism in actively growing tissue. Significance Statement : Glutathione transferase enzymes (GSTs) are highly abundant in plants, but only very few have been assigned a physiological function. Here we demonstrate that GSTs are key players in a pathway for endogenous recycling of a cyanogenic glucoside defense compound in sorghum, revealing that plants continuously optimize, and can even reverse, their allocation of resources between general and specialized metabolism.