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Molecular cloning and biochemical characterization of three Concord grape (Vitis labrusca) flavonol 7-O-glucosyltransferases

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Abstract

Grapes berries produce and accumulate many reactive secondary metabolites, and encounter a wide range of pathogen- and human-derived xenobiotic compounds. The enzymatic glucosylation of these metabolites changes their reactivity, stability and subcellular location. Two ESTs with more than 90% nucleotide sequence identity to three full-length glucosyltransferases are expressed in several grape tissues. The full-length clones have more than 60% amino acid sequence similarity to previously characterized flavonoid 7-O-glucosyltransferases, catechin O-glucosyltransferases and anthocyanin 5-O-glucosyltransferases. In vitro, these enzymes glucosylate flavonols and the xenobiotic 2,4,5-trichlorophenol (TCP). Kinetic analysis indicates that TCP is the preferred substrate for these enzymes, while expression analysis reveals variable transcription of these genes in grape leaves, flowers and berry tissues. The in vivo role of these Vitis labrusca glucosyltransferases is discussed.

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Abbreviations

AF:

After flowering

DFCI:

Dana Farber Cancer Institute

GTs:

Glucosyltransferases

PMSF:

Phenylmethyl sulfonyl fluoride

PSPG:

Plant secondary product glucosyltransferases

PVP-10 or PVPP:

Polyvinylpyrrolidone

Q3G:

Quercetin 3-O-glucoside

TCP:

Trichlorophenol

UDPG:

Uridine 5′-diphosphoglucose

VLOGT:

Vitis labrusca O-glucosyltransferase

VLRSGT:

Vitis labrusca resveratrol glucosyltransferase

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Acknowledgments

This research was funded by a Natural Sciences and Engineering Research Council of Canada Discovery grant to V.D.L. and a Tier 1 Canada Research Chair in Plant Biotechnology to V.D.L., as well as an NSERC post-graduate fellowship to D.H. We thank G&H Wiley Ltd (St, Catharine’s, Ontario, Canada) for allowing us to collect Concord grapes during the growing season. We thank Tim Jones for performing HPLC-mass spectrometry on selected flavonoid reaction products.

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  1. Dawn Hall

    Present address: Michael Smith Laboratories, The University of British Columbia, #301, 2185 East Mall, Vancouver, BC, V6T 1Z4, Canada

Authors and Affiliations

  1. Department of Biological Sciences, Brock University, 500 Glenridge Ave, St. Catharines, ON, L2S 3A1, Canada

    Dawn Hall, Kyung Hee Kim & Vincenzo De Luca

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Corresponding author

Correspondence to Vincenzo De Luca.

Electronic supplementary material

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425_2011_1474_MOESM1_ESM.tif

Figure S1 UPLC chromatogram of grape anthocyanins (1, 2, 3, 4, 9) and flavonoids (5, 6, 7, 8) analyzed at 590 and 360 nm, respectively. The Table insert describes the composition of anthocyanins & flavonoids in mature Vitis labrusca grape mesocarp & exocarp. Mean values from 3 biological replicates ± SD are shown (TIFF 11721 kb)

425_2011_1474_MOESM2_ESM.tif

Figure S2 Amino acid sequence alignment of the Vitis labrusca 7-O-glucosyltransferases VLOGT1 (ABQ02256), VLOGT2 (ABQ02257) and VLOGT3 (ABQ02258) with other enzymes which glucosylate the 7-O-position of flavonols. Abbreviations: NtGT2—Nicotiana tabacum coumarin GT (BAB88935), the Lb_catGT- Lycium barbarium catechin GT (BAG80544), Ep_TpGT—Eucalyptus perriniana monoterpene OGT (BAD90934); Ph_5GT—Petunia x hybrida anthocyanin 5-O-glucosyltransferase (BAA89009); Mp_7GT—Maclura pomifera flavonoid 7-O-glucosyltransferase (ABL85474); Pc_7GT—Pyrus communis flavonoid 7-O-glucosyltransferase (AAY27090). The Plant Secondary Product Glucosyltransferase (PSPG) box is underlined. Different colours represent unique amino acids (TIFF 15113 kb)

425_2011_1474_MOESM3_ESM.tif

Figure S3 Neighbor-joining phylogenetic tree of the Vitis labrusca flavonol 7-O-glucosyltransferase gene family and other previously characterized glycosyltransferases. Lb_catGT—Lycium barbarum catechin 4′OGT (BAG80544); Solanum_5gt—Solanum sogarandinum anthocyanin 5OGT (AAK54465); NtGt2—Nicotiana tabacum coumarin GT (BAB88935); Pet_5gt—Petunia x hybrida anthocyanin 5OGT (BAA89009); Pc_7GT—Pyrus communis flavonoid 7OGT (AAY27090); Mp_7gt—Maclura pomifera flavonoid 7OGT (ABL85474); VLOGT3—Vitis labrusca flavonol 7OGT3 (ABQ02258); Vv_TC108954—Vitis vinifera DFCI EST TC108954; Vv_NP9528154—Vitis vinifera genome sequence NP9528154; Vv_LOC100246377—Vitis vinifera genome sequence Locus 100246377; Ep_TpGT1—Eucalyptus perriniana monoterpene GT 1 (BAD90934); Vvx_5GT—Vitis vinifera cv Regent non-functional anthocyanin 5OGT; VV_5GT—Vitis vinifera cv Regent anthocyanin 5OGT; Per_5GT—Perilla frutescens anthocyanin 5OGT (BAA36421); Verb_5GT—Verbena x hybrida anthocyanin 5OGT (BAA36423); Torenia hybrida anthocyanin 5OGT (BAC54093); At_UGT75D1—Arabidopsis thaliana UGT75D1 xenobiotic and flavonol GT; At_UGT75B1—Arabidopsis thaliana UGT75B1 hydroxybenzoic acid OGT; At_UGT75B2—Arabidopsis thaliana UGT75B2 hydroxybenzoic acid OGT; At_UGT75C1_5GT—Arabidopsis thaliana UGT75C1 anthocyanin 5OGT; Vv_TC125631—Vitis vinifera DFCI EST TC125631; Vv_LOC100242998—Vitis vinifera genome sequence Locus 100242998; VLOGT2—Vitis labrusca flavonol 7OGT2 (ABQ02257); Vv_LOC100248120—Vitis vinifera genome sequence Locus 100248120; Vv_ NP9526770- Vitis vinifera genome sequence NP9526770; VLOGT1—Vitis labrusca flavonol 7OGT 1 (ABQ02256); Gent_5GT—Gentiana triflora anthocyanin 5OGT (BAG32255); Iris_5gt—Iris hollandica anthocyanin 5OGT (BAD06874); At_UGT74F2—Arabidopsis thaliana SAGT1 and 4-aminobenzoate OGT; At_UGT74F1—Arabidopsis thaliana UGT74F1 anthranilate OGT; Nt_SAgt—Nicotiana tabacum salicylic acid OGT (AAF61647); Stev_UGT74G1—Stevia rebaudiana UGT74G1 steviol OGT (AAR06920); At_UGT74B1—Arabidopsis thaliana UGT74B1 thiohydroximate SGT; Bn_thiogt—Brassica napus thiohydroximate SGT (AAL09350); At_JAgt—Arabidopsis thaliana UGT74D1 jasmonic acid OGT (NP_180734); Crocus_safgt—Crocus sativus OGT2 (AAP94878); Zea_IAAgt—Zea mays indole-3-acetate OGT (AAA59054); At_UGT84A3—Arabidopsis thaliana UGT84A3 sinapate 1 OGT (NP_193284); At_UGT84A4—Arabidopsis thaliana UGT84A4 sinapate 1 OGT (NP_193285); At_UGT84A2- Arabidopsis thaliana UGT84A2 sinapate 1 OGT (NP_188793); Bn_Sgt1—Brassica napus sinapate glucosyltransferase (AF287143_1); At_UGT84A1—Arabidopsis thaliana sinapate 1 glucosyltransferase (NP_193283); VLRSGT—Vitis labrusca resveratrol/hydroxycinnamic acid OGT (ABH03018); Fra_SAgt2—Fragaria x ananassa cinnamate OGT (AAU09443); Citrus_Limgt—Citrus unshiu liminoid OGT (BAA93039); Mt_UGT84F1—Medicago truncatula isoflavonoid OGT (ABI94023); At_UGT84B1—Arabidopsis thaliana abscisic acid/indole-3-acetic acid OGT/quercetin 7OGT (NP_179907); At_UGT84B2—Arabidopsis thaliana abscisic acid OGT (NP_179906); Dian_chalconegt—Dianthus caryophyllus chalcone 2’OGT (BAD52007); Stev_ugt76G1—Stevia rebaudiana UGT76G1 (AAR06912); At_UGT76E11—Arabidopsis thaliana UGT76E11 quercetin 3OGT and 7OGT (NP_190251); Mt_UGT85H2—Medicago truncatula isoflavonoid OGT (ABI94024); At_UGT85A1_ZeaGT—Arabidopsis thaliana UGT85A1 zeatin OGT (NP_173656); Stev_ugt85C2—Stevia rebaudiana UGT85C2 (AAR06916); Sorghum_UGT85B1—Sorghum bicolor p-hydroxymandelonitrile OGT (Q9SBL1); OryzaIsoFL7GT—Oryza sativa isoflavonoid 7OGT (NP_001059671); Phas_HRA25—Phaseolus vulgaris OGT HRA25 (AF303396_1); Vv_3gt—Vitis vinifera flavonoid 3OGT (AAB81683); VL_3gt—Vitis labrusca flavonoid 3OGT (ABR24135); FraGT1_3GT—Fragaria x ananassa flavonoid 3OGT (AAU09442); At_UGT78D2—Arabidopsis thaliana UGT 78D2 flavonoid 3OGT (NP_197207); At_UGT78D3—Arabidopsis thaliana UGT78D3 flavonol 3-O-arabinosyltransferase (NP_197205); At_UGT78D1—Arabidopsis thaliana UGT 78D1 UDP-rhamnose flavonol 3-O-rhamnosyltransferase (NP_564357); Per_3gt—Perilla frutescens flavonoid 3OGT (BAA19659); Gent _3gt—Gentiana triflora anthocyanidin 3OGT (Q96493); Pet_3gt—Petunia x hybrida anthocyanidin 3OGT (BAA89008); Ipomoea—Ipomoea purpurea flavonoid 3OGT (AAB86473); Mt_UGT78G1—Medicago truncatula isoflavonoid OGT (ABI94025); Dian_3gt—Dianthus caryophyllus flavonol 3OGT (BAD52005); Iris_3gt—Iris hollandica anthocyanidin 3OGT (BAD83701); Hv_3gt—Hordeum vulgare anthocyanidin 3OGT (P14726); Zea_3gt—Zea mays anthocyanidin 3OGT (P16165); Cr_curcgt2—Catharanthus roseus curcumin OGT2 (BAD29722); Gent_3′gt—Gentiana triflora anthocyanin 3’OGT (Q8H0F2); Scut_7gt—Scutellaria baicalensis flavonoid 7OGT (BAA83484); Doro_bet5gt—Dorotheanthus bellidiformis betanidin 5OGT (CAB56231); Rhodiola_salidrosideGT—Rhodiola sachalinensis salidroside OGT (AAS55083); At_UGT73B1—Arabidopsis thaliana UGT73B1 flavonoid 7OGT (NP_567955); Gly_isoflv_gt—Glycyrrhiza echinata isoflavonoid OGT (BAC78438); Vigna_ABAgt—Vigna angularis abscisic acid OGT (BAB83692); Mt_UGT73P1—Medicago truncatula isoflavonoid OGT (ABI94026); Sol_saponin_gt—Solanum aculeatissimum saponin OGT (BAD89042); Sol_sgat1—Solanum tuberosum solanidine galactosyltransferase (AAB48444); At_UGT73C5—Arabidopsis thaliana UGT73C5 zeatin OGT, flavonol 4′ and 7OGT (NP_181218); AtUGT73C6—Arabidopsis thaliana UGT73C6 flavonol 3 and 7OGT (NP_181217); At_UGT73C1—Arabidopsis thaliana UGT73C1 zeatin OGT (NP_181213); Nt_gt4—Nicotiana tabacum flavonoid OGT (BAD93688); Mt_UGT73C8—Medicago truncatula isoflavonoid OGT (ABI94020); At_UGT89B1—Arabidopsis thaliana UGT89B1 flavonol 3,4′ and 7OGT (NP_177529); At_89C1—Arabidopsis thaliana UGT89C1 7-O-rhamnosyltransferase to 7-O-glucose (NP_563756); Mira_DOPAgt—Mirabilis jalapa DOPA 5OGT (BAD91803); Ipo2′′gt—Ipomoea purpurea anthocyanin 2′′OGT (BAD95882); Nt_gt1—Nicotiana tabacum OGT1 (BAB60720); Nt_gt1b—Nicotiana tabacum OGT1b (BAB60721); Nt_gt3—Nicotiana tabacum OGT3 (BAB88934); Cr_curcgt1—Catharanthus roseus curcumin OGT1 (BAD29721); Ipomoea_IAAgt—Ipomoea purpurea indole-3-acetate OGT (BAF75917); Doro_bet6gt—Dorotheanthus bellidiformis betanidin 6OGT (AAL57240); Mt_UGT71G1—Medicago truncatula triterpenoid/flavonoid OGT (2ACW_A); At_UGT71C1—Arabidopsis thaliana UGT71C1 flavonol 3′ and 7OGT (NP_180536); OryzaFl3GT—Oryza sativa flavonol 3OGT (BAC83989); Mt_UGT88E1—Medicago truncatula isoflavonoid OGT (ABI94021); Mt_UGT88E2—Medicago truncatula isoflavonoid OGT (ABI94022); GM_Isoflv7GT—Glycine max isoflavonoid 7OGT (BAF64416); Rose_5gt—Rosa x hybrida anthocyanidin 5,3OGT (Q4R1I9); Antirr_chalcGT—Antirrhinum majus chalcone OGT (BAE48239); Sc_5OGT—Sinningia cardinalis 3-deoxy anthocyanin 5OGT (BAJ11653); Oryza7GT—Oryza sativa flavonoid 7OGT (NP_001044173); Os_RF5—Oryza sativa flavonoid OGT5 (NP_001044170); Bn_UGT2—Brassica napus xenobiotic GT (CAM31954); Mt_epicat_GT—Medicago truncatula epicatechin OGT (ACC38470); Os_RUGT10—Oryza sativa OGT (NP_001174726); Gly_Zeatingt—Glycine max zeatin OGT (AAM09514); Phas_ZOG1—Phaseolus lunatus zeatin OGT (Q9ZSK5); Zea_cisZOGT—Zea mays cis-zeatin OGT (NP_001105017) (TIFF 9949 kb)

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Hall, D., Kim, K.H. & De Luca, V. Molecular cloning and biochemical characterization of three Concord grape (Vitis labrusca) flavonol 7-O-glucosyltransferases. Planta 234, 1201–1214 (2011). https://doi.org/10.1007/s00425-011-1474-0

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