Apocarotenoids are allosteric effectors of a dimeric plant glycosyltransferase involved in plant defense and lignin formation

Glycosyltransferases are Nature’s versatile tools to tailor the functionalities of proteins, carbohydrates, lipids, and small molecules by transferring sugars, while C13-apocarotenoids are oxidative degradation products of carotenoids/xanthophylls that fulfil multiple physiological functions. Here, we show that C13-apocarotenoids also interact with the plant glycosyltransferase NbUGT72AY1, ultimately reducing its inherent UDP-α-D-glucose glucohydrolase activity and increasing its catalytic activity for productive substrates such as hydroxycoumarins, which are natural plant protective agents. In contrast, C13-apocarotenoids show no effect on the catalytic activity of the enzyme toward monolignol lignin precursors. Hydrogen deuterium exchange mass spectrometry revealed opposite conformational changes near the catalytic site in the presence of substrates and modulators and studies in tobacco plants confirmed increased glycosylation activity from apocarotenoid supplementation. The interaction of two plant protection mechanisms and the function of apocarotenoids as allosteric enhancers of catalytic proteins has significant implications for potential applications of these multifunctional natural products in agriculture as well as in the pharmaceutical industry.