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Transcriptome-Wide Identification of an Aurone Glycosyltransferase With G C A T T A C G G C A T genes Article Transcriptome-Wide Identification of an Aurone Glycosyltransferase with Glycosidase Activity from Ornithogalum saundersiae Shuai Yuan †, Ming Liu † ID , Yan Yang, Jiu-Ming He, Ya-Nan Wang and Jian-Qiang Kong * ID Institute of Materia Medica, Chinese Academy of Medical Sciences & Peking Union Medical College (State Key Laboratory of Bioactive Substance and Function of Natural Medicines & Ministry of Health Key Laboratory of Biosynthesis of Natural Products), Beijing 100050, China; [email protected] (S.Y.); [email protected] (M.L.); [email protected] (Y.Y.); [email protected] (J.-M.H.); [email protected] (Y.-N.W.) * Correspondence: [email protected] † These authors contributed equally to this work. Received: 29 May 2018; Accepted: 22 June 2018; Published: 28 June 2018 Abstract: Aurone glycosides display a variety of biological activities. However, reports about glycosyltransferases (GTs) responsible for aurones glycosylation are limited. Here, the transcriptome- wide discovery and identification of an aurone glycosyltransferase with glycosidase activity is reported. Specifically, a complementary DNA (cDNA), designated as OsUGT1, was isolated from the plant Ornithogalum saundersiae based on transcriptome mining. Conserved domain (CD)-search speculated OsUGT1 as a flavonoid GT. Phylogenetically, OsUGT1 is clustered as the same phylogenetic group with a putative 5,6-dihydroxyindoline-2-carboxylic acid (cyclo-DOPA) 5-O-glucosyltransferase, suggesting OsUGT1 may be an aurone glycosyltransferase. The purified OsUGT1 was therefore used as a biocatalyst to incubate with the representative aurone sulfuretin. In vitro enzymatic analyses showed that OsUGT1 was able to catalyze sulfuretin to form corresponding monoglycosides, suggesting OsUGT1 was indeed an aurone glycosyltransferase. OsUGT1 was observed to be a flavonoid GT, specific for flavonoid substrates. Moreover, OsUGT1 was demonstrated to display transglucosylation activity, transferring glucosyl group to sulfuretin via o-Nitrophenyl-β-D-glucopyranoside (oNP-β-Glc)-dependent fashion. In addition, OsUGT1-catalyzed hydrolysis was observed. This multifunctionality of OcUGT1 will broaden the application of OcUGT1 in glycosylation of aurones and other flavonoids. Keywords: aurones; sulfuretin; glycosyltransferase; Ornithogalum saundersiae 1. Introduction Aurones, represented by sulfuretin (Figure1, 1) and sulfurein (Figure1, 1c), are minor tricyclic flavonoids that consist of a benzofuranone ring linked through a carbon-carbon double bond to a phenyl moiety (Figure1)[ 1]. Besides lending flowers a bright yellow pigment, aurones function as phytoalexins against infections [2]. Aurones distribute widely among the plant kingdom and two aurone types can be distinguished, 4-hydroxyaurones and 4-deoxyaurones [1]. Aurones show a remarkable spectrum of biological activities, like antioxidant, antitumor, antimicrobial, antiviral and anti-inflammatory activities, making them interesting scaffolds for the design of potential therapeutic agents [1,3]. Thus, many efforts have been made for synthetic modifications of aurone scaffolds, such as glycosylation, hydroxylation and methoxylation [1]. Genes 2018, 9, 327; doi:10.3390/genes9070327 www.mdpi.com/journal/genes Genes 2018, 9, 327 2 of 15 Genes 2018, 9, x FOR PEER REVIEW 2 of 17 FigureFigure 1. OsUGT1-catalyzed 1. OsUGT1-catalyzed biosynthesis biosynthesis of of sulfuretin sulfuretin glucosides glucosides (1a(1a,, 1b1b andand 1c1c)) viavia glucosylationglucosylation or transglucosylationor transglucosylation reaction. reaction UDP:. UDP: uridine uridine diphosphate; diphosphate; OsUGT1:OsUGT1: glycosyltransferaseglycosyltransferase from from OrnithogalumOrnithogalum saundersiae saundersiae. Among these modifications, glycosylation of aurones have attracted much interest because Among these modifications, glycosylation of aurones have attracted much interest because these these resulting glycosylated aurones display enhanced and advantageous properties, like resulting glycosylated aurones display enhanced and advantageous properties, like neuroprotective [4], neuroprotective [4], antioxidant [5–9], anti-inflammatory [10] and leishmanicidal activities [11]. antioxidant [5–9], anti-inflammatory [10] and leishmanicidal activities [11]. Theoretically, Theoretically, glycosylations of aurones may be achieved by chemical or enzymatical syntheses. glycosylationsChemical approaches of aurones maygenerally be achieved require by multiple chemical protection or enzymatical and de-protection syntheses. Chemical steps in approaches order to generallyachieve require regio- and multiple stereo-selectivity. protection Moreover, and de-protection chemical glycosylations steps in order involve to achievethe use of regio- toxic and and stereo-selectivity.hazardous chemicals, Moreover, which chemical may glycosylations pose potential involve environmental the use of and toxic biological and hazardous risks. chemicals,For such whichreasons, may pose glycosyltransferases potential environmental (GTs)-catalyzed and biological glycosylations risks. For suchbecome reasons, increasingly glycosyltransferases important (GTs)-catalyzedenzymatic synthesis glycosylations due to its become high regio-selectiv increasinglyity important without the enzymatic need of any synthesis protecting due groups. to its highThe regio-selectivityenzymatic glucosylation without the of need4-deoxyaurones of any protecting was firstly groups. achieved The by enzymaticHalbwirth et glucosylation al., 1997 [12]. of 4-deoxyauronesSulfuretin 6-glucoside, was firstly namely achieved sulfurein by Halbwirth (1c), was et yielded al., 1997 after [12 ].incubation Sulfuretin of 6-glucoside, sulfuretin (1) namely with sulfureinenzyme (1c), preparation was yielded from after Coreopsis incubation grandiflora of sulfuretin. However, (1) the with biocatalyst enzyme preparation used in this fromglucosylationCoreopsis grandiflorareaction. was However, enzyme the extract biocatalyst of C. grandiflora used in but this not glucosylation a purified glucosyltransferase reaction was enzyme [12]. Sakakibara extract of C. grandifloraet al. providedbut not a agene purified encoding glucosyltransferase an aurone glycosyltr [12]. Sakakibaraansferase with et al. an provided activity of a genetransferring encoding a an auroneglycosyl glycosyltransferase group to an aurone with[13]. However, an activity this of aurone transferring GT required a glycosyl expensive group uridine to an diphosphate aurone [13]. However,(UDP)-sugar this aurone as the GT requiredsugar donor expensive for glycosylations uridine diphosphate of aurones, (UDP)-sugar which aslimited the sugar its extensive donor for glycosylationsapplications of aurones,[13]. Herein, which the limited transcriptome-wi its extensivede applications discovery [ 13and]. Herein, identification the transcriptome-wide of an aurone discoveryglycosyltransferase and identification OsUGT1 of an with aurone glycosidase glycosyltransferase activity was OsUGT1described, with which glycosidase meant OsUGT1 activity was was able to glycosylate aurones using either expensive UDP-sugars or the cheap alternatives as sugar described, which meant OsUGT1 was able to glycosylate aurones using either expensive UDP-sugars donors. Specifically, a complementary DNA (cDNA), designated as OsUGT1, coding for an aurone or the cheap alternatives as sugar donors. Specifically, a complementary DNA (cDNA), designated GT was firstly isolated from Ornithogalum saundersiae based on transcriptome mining. The as OsUGT1, coding for an aurone GT was firstly isolated from Ornithogalum saundersiae based recombinant OsUGT1 was then determined to have the ability to glucosylate sulfuretin (1) to form on transcriptome mining. The recombinant OsUGT1 was then determined to have the ability three monoglucosides using UDP-D-glucose (UDP-Glc) as a sugar donor. In addition, OsUGT1 to glucosylatedisplayed catalytic sulfuretin promiscuity, (1) to form transferring three monoglucosides sugar group usingto diverse UDP- flavonoidsD-glucose from (UDP-Glc) UDP-Glc. as a sugarBesides donor. being In addition, a glycosyltransferase, OsUGT1 displayed OsUGT1 catalytic was demonstrated promiscuity, transferringto display transglycosylase sugar group to diverseactivity, flavonoids forming from sulfuretin UDP-Glc. glucosides Besides being using a glycosyltransferase, cheap aryl glycosides OsUGT1 as wassugar demonstrated donor by to displaytransglycosylation. transglycosylase Moreover, activity, OsUGT1-catalyzed forming sulfuretin hydrolysis glucosides activity using cheapwas arylobservable. glycosides This as sugarmultifunctionality donor by transglycosylation. thus broadened Moreover, the potential OsUGT1-catalyzed applications of OsUGT1 hydrolysis in glycosylation activity was observable.of aurones Thisand multifunctionality other flavonoids. thus broadened the potential applications of OsUGT1 in glycosylation of aurones and other flavonoids. 2. Materials and Methods 2.1. Chemicals Genes 2018, 9, 327 3 of 15 2. Materials and Methods Genes2.1. Chemicals 2018, 9, x FOR PEER REVIEW 3 of 17 A total of 41 compounds, including flavonoids flavonoids ( 1–7), anthraquinones anthraquinones ( (88),), steroids steroids ( (99––2525),), terpenoids ( (26–28),), phenolic acids acids ( (29–33)) and alkaloids ( 34–41), were used as the sugar acceptors for OsUGT1-catalyzed glycosylation glycosylation reactions reactions (Figur (Figuree 22,, TableTable S1).S1). FourFour UDP-activatedUDP-activated nucleotides,nucleotides,
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