A noncanonical vacuolar sugar transferase required for biosynthesis of antimicrobial defense compounds in oat

Plants produce an array of natural products with important ecological functions. These compounds are often decorated with oligosaccharide groups that influence bioactivity, but the biosynthesis of such sugar chains is not well understood. Triterpene glycosides (saponins) are a large family of plant natural products that determine important agronomic traits, as exemplified by avenacins, antimicrobial defense compounds produced by oats. Avenacins have a branched trisaccharide moiety consisting of l-arabinose linked to 2 d-glucose molecules that is critical for antifungal activity. Plant natural product glycosylation is usually performed by uridine diphosphate-dependent glycosyltransferases (UGTs). We previously characterized the arabinosyltransferase that initiates the avenacin sugar chain; however, the enzymes that add the 2 remaining d-glucose molecules have remained elusive. Here we characterize the enzymes that catalyze these last 2 glucosylation steps. AsUGT91G16 is a classical cytosolic UGT that adds a 1,2-linked d-glucose molecule to l-arabinose. Unexpectedly, the enzyme that adds the final 1,4-linked d-glucose (AsTG1) is not a UGT, but rather a sugar transferase belonging to Glycosyl Hydrolase family 1 (GH1). Unlike classical UGTs, AsTG1 is vacuolar. Analysis of oat mutants reveals that AsTG1 corresponds to Sad3, a previously uncharacterized locus shown by mutation to be required for avenacin biosynthesis. AsTG1 and AsUGT91G16 form part of the avenacin biosynthetic gene cluster. Our demonstration that a vacuolar transglucosidase family member plays a critical role in triterpene biosynthesis highlights the importance of considering other classes of carbohydrate-active enzymes in addition to UGTs as candidates when elucidating pathways for the biosynthesis of glycosylated natural products in plants.

Medienart:

E-Artikel

Erscheinungsjahr:

2019

Erschienen:

2019

Enthalten in:

Zur Gesamtaufnahme - volume:116

Enthalten in:

Proceedings of the National Academy of Sciences of the United States of America - 116(2019), 52 vom: 26. Dez., Seite 27105-27114

Sprache:

Englisch

Beteiligte Personen:

Orme, Anastasia [VerfasserIn]
Louveau, Thomas [VerfasserIn]
Stephenson, Michael J [VerfasserIn]
Appelhagen, Ingo [VerfasserIn]
Melton, Rachel [VerfasserIn]
Cheema, Jitender [VerfasserIn]
Li, Yan [VerfasserIn]
Zhao, Qiang [VerfasserIn]
Zhang, Lei [VerfasserIn]
Fan, Danlin [VerfasserIn]
Tian, Qilin [VerfasserIn]
Vickerstaff, Robert J [VerfasserIn]
Langdon, Tim [VerfasserIn]
Han, Bin [VerfasserIn]
Osbourn, Anne [VerfasserIn]

Links:

Volltext

Themen:

Biosynthetic gene clusters
Glycosylation
Journal Article
Natural products
Plant defense
Saponins

Anmerkungen:

Date Revised 05.12.2022

published: Print-Electronic

Citation Status PubMed-not-MEDLINE

doi:

10.1073/pnas.1914652116

funding:

Förderinstitution / Projekttitel:

PPN (Katalog-ID):

NLM304084166