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Dissection of the general two-step di-C-glycosylation pathway for the biosynthesis of (iso)schaftosides in higher plants

文献类型: 外文期刊

作者: Wang, Zi-Long 1 ; Gao, Hao-Meng 2 ; Wang, Shuang 1 ; Zhang, Meng 1 ; Chen, Kuan 1 ; Zhang, Ya-Qun 1 ; Wang, Hai-Dong 1 ;

作者机构: 1.Peking Univ, Sch Pharmaceut Sci, State Key Lab Nat & Biomimet Drugs, Beijing 100191, Peoples R China

2.Peking Univ, Sch Basic Med Sci, Dept Biochem & Biophys, Beijing 100191, Peoples R China

3.Peking Univ, Sch Basic Med Sci, Dept Integrat Chinese & Western Med, Beijing 100191, Peoples R China

4.Jiangsu Acad Agr Sci, Inst Plant Protect, Nanjing 210014, Peoples R China

关键词: flavonoid C-glycoside; C-glycosyltransferase; schaftoside; crystal structure; catalytic mechanism

期刊名称:PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA ( 影响因子:11.205; 五年影响因子:12.291 )

ISSN: 0027-8424

年卷期: 2020 年 117 卷 48 期

页码:

收录情况: SCI

摘要: Schaftoside and isoschaftoside are bioactive natural products widely distributed in higher plants including cereal crops and medicinal herbs. Their biosynthesis may be related with plant defense. However, little is known on the glycosylation biosynthetic pathway of these flavonoid di -C-glycosides with different sugar residues. Herein, we report that the biosynthesis of (iso)schaftosides is sequentially catalyzed by two C-glycosyltransferases (CGTs), i.e., CGTa for C-glucosylation of the 2-hydroxyflavanone aglycone and CGTb for C-arabinosylation of the mono-C-glucoside. The two enzymes of the same plant exhibit high homology but remarkably different sugar acceptor and donor selectivities. A total of 14 CGTa and CGTb enzymes were cloned and characterized from seven dicot and monocot plants, including Scutellaria baicalensis, Glycyrrhiza uralensis, Oryza sativa ssp. japonica, and Zea mays, and the in vivo functions for three enzymes were verified by RNA interference and overexpression. Through transcriptome analysis, we found homologous genes in 119 other plants, indicating this pathway is general for the biosynthesis of (iso)schaftosides. Furthermore, we resolved the crystal structures of five CGTs and realized the functional switch of SbCGTb to SbCGTa by structural analysis and mutagenesis of key amino acids. The CGT enzymes discovered in this paper allow efficient synthesis of (iso)schaftosides, and the general glycosylation pathway presents a platform to study the chemical defense mechanisms of higher plants.

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Wyse;Bouskila, Amos;Shacham, Boaz;Gossa, Tegenu;Ballerio, Alberto;Allievi, Alessandro;de Jager, Gerhard;Petroni, Giulio;Peruzzi, Lorenzo;D'Antraccoli, Marco;Serra, Valentina;Bisi, Alessandro;Chiarucci, Alessandro;Hilpold, Andreas;Rosso, Antonietta;Sciuto, Francesco;Mingozzi, Antonio;Giovanni, Boano;Massa, Bruno;Marrone, Federico;Vecchioni, Luca;Guarino, Riccardo;Giusto, Carlo;Lombardi, Chiara;Nepi, Chiara;Scaccini, Davide;Fontaneto, Diego;Banfi, Enrico;Rigato, Fabrizio;Galasso, Gabriele;Chiozzi, Giorgio;Gallo, Enrico;Bertasi, Fabio;Bartolucci, Fabrizio;Fabbriciani, Fabrizio;Andreone, Franco;Polgar, Gianluca;Filibeck, Goffredo;Tessa, Giulia;Gardini, Giulio;Fenu, Giuseppe;Mazzini, Ilaria;Langeneck, Joachim;Bartolozzi, Luca;Bologna, Marco A.;Abeli, Thomas;Dellacasa, Marco;Uliana, Marco;Novarini, Nicola;Faccoli, Massimo;Majorano, Paolo;Zilioli, Michele;Raia, Pasquale;Cerretti, Pierfilippo;Poggi, Roberto;Bertolino, Sandro;Orsenigo, Simone;Martellos, Stefano;Greuter, Werner;Greuter, Werner;Kouakou, Lombart Maurice;Kato, Daichi;Yadav, Harsh;Chiba, Hideyuki;Chiba, Hideyuki;Yoshitomi, Hiroyuki;Kakui, Keiichi;Kwak, Mackenzie L.;Dick, Matthew H.;Ikuno, Kenji;Genka, Masaaki;Yano, Okihito;Kakizoe, Showtaro;Hellemans, Simon;Jashenko, Roman;Dujsebayeva, Tatjana;Kabak, Ilya;Kabak, Ilya;Katumo, Daniel Mutavi;Baasanmunkh, Shukherdorj;Choi, Hyeok Jae;Shin, Jae-Seo;Eun, Lim Ji;Jung, Eui-Kwon;Kim, Young-Dong;Lazkov, Georgii;Strijk, Joeri Sergej;Shavrin, Alexey;Greke, Kristine;Kalnins, Martins;Petrasiunas, Andrius;Uogintas, Domas;Stonis, Jonas R.;Gudzinskas, Zigmantas;Sokolova, Elena;Kharchenko, Viktoria;Andriambololonera, Sylvie;Kumaran, Jayaraj Vijaya;Appalasamy, Suganthi;Prozorov, Alexey M.;Dembele, Jacques;Hanan Alipi, Ana Maria;Solano Gomez, Aniceto Rodolfo;Maruri-Aguilar, Beatriz;Ramirez Diaz, Claudia Janeth;Carnevali Fernandez-Concha, German;Ramirez-Morillo, Ivon M.;Stefano Duno, Rodrigo;Delgadillo-Moya, Claudio;Prieto Torres, David Alexander;Daniel Tejero-Diez, J.;Meave, Jorge A.;Alvarado Cardenas, Leonardo Osvaldo;Terrazas, Teresa;Barradas, Victor L.;Adilson Pinedo-Escatel, J.;Murugan, Gopal;Ruiz Sanchez, Eduardo;Sanchez Martinez, Emiliano;Hernandez Martinez, Maria Magdalena;Gomez-Noguez, Felipe;Montiel Canales, Gustavo;Socorro Gonzalez-Elizondo, M.;Gonzalez Elizondo, Martha;Rolando Bastida-Zavala, J.;del Socorro Garcia-Madrigal, Maria;Alvarado Rodriguez, Jose Fernando;Lopez Mata, Lauro;Gonzalez Ledesma, Manuel;Ramirez-Marcial, Neptali;Cuevas Guzman, Ramon;Martinez-Camilo, Rub'n;Adilson Pinedo-Escatel, J.;Boldgiv, Bazartseren;Mathieu, Chambouleyron;Lermmel, Claude;Leger, Jean-Francois;Farooq, Harith;Irish, John;Shrestha, Krishna;Dop, A. J.;van der Geer, Alexandra;Jaramillo, Angelica Cibrian;Gielis, Cornelis (Cees);Simons, Erik;Sangster, George;Kronenberg, Gijs C.;Henrot, Jacqueline;Arntzen, Jan W.;Monsch, Kenneth A.;Duistermaat, Leni;Schilthuizen, Menno;d'Oliveira, Micha C.;van Eck, Andre P. W.;Egberts, E.;Peeters, Edwin;Sival, Francisca;Kessels, Han;Rutjes, Hendrikus Antonius;van Dam, Herman;Huang, Huasheng;van Eck, Iris;Klinge, Marcel;Graveland, Jaap;van der Vleuten, Jan;van Zuijlen, Jan Willem;Stroom, Jasper;Collombon, Miriam;van Valkenburg, Johan;Melis, John;Bruins, Linda;Knapp, Markus;Soesbergen, Martin;Beuk, Paul L. T.;van Els, Paul;Haveman, Rense;Lansdown, Richard;Suijkerbuijk, Rob;Pot, Roelf;van Manen, Willem;Marshall, Andrew;de Lange, Peter J.;Blanchon, Dan;Early, John W.;Leduc, Daniel;Gordon, Dennis Preston;Kelly, Michelle;Lowe, David J.;Gordon, Dennis;Ford, Kerry;Harper, Margaret;Marinov, Milen;Marinov, Milen;Maes, Jean-Michel;Perez, Rosa Maria Reyes;Valqui, Thomas;Seid, Abel Gizaw;Langangen, Anders;Bjora, Charlotte Sletten;Di Martino, Emanuela;Nakrem, Hans Arne;Lifjeld, Jan T.;Eidesen, Pernille Bronken;Elven, Reidar;Gusarov, Vladimir I.;Tandberg, Anne Helene Solberg;Andersson, Carin;Westergaard, Kristine Bakke;Ekrem, Torbjorn;Malaquias, Manuel Antonio E.;Majid, Abdul;Hanif, Uzma;Aiello, Annette;Carrion, Juan F.;Garcete-Barrett, Bolivar R.;Soria Rey, Nelida;Cano, Asuncion;Rojas-Fox, Jenny;Reynel Rodriguez, Carlos;Heredia Huarino, Din Olger;Fany Palomino, Elva;Gagliardi-Urrutia, Giussepe;Pino, Guillermo;Trevino Zevallos, Italo Francisco;Trevino Zevallos, Italo Francisco;Cabrera Melendez, Jorge Luis;Cabrera Melendez, Jorge Luis;Dupo, Aimee Lynn;Lit, Ireneo L., Jr.;Lucanas, Cristian C.;General, David Emmanuel M.;Tolentino, Haira Jill;Calaramo, Michael Agbayani;Calaramo, Michael Agbayani;Kaczmarek, Adam;Kaim, Andrzej;Hryniewicz, Krzysztof;Taszakowski, Artur;Tokarska-Guzik, Barbara;Wisniowski, Bogdan;Moniuszko, Hanna;Garcia-Cunchillos, Ivan;De Baets, Kenneth;Talanda, Mateusz;Wieclaw, Helena;Koopman, Jacob;Tyszka, Jaroslaw;Lis, Jerzy;Piatek, Marcin;Wanat, Marek;Zakrzewska, Marta;Kuklinski, Piotr;Salamatin, Ruslan;Solarz, Wojciech;Casimiro Justo Carapeto, Andre de Matos;Muriel, Andreu Santin;Sampaio, Iris;Calado, Antonio Jose;Esquete, Patricia;Sa, Artur A.;Serrano, Artur R. M.;Gois-Marques, Carlos A.;Vila-Vicosa, Carlos;Parrinha, Diogo;Grosso-Silva, Jose Manuel;Ceriaco, Luis M. 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Luisa;Sanz Arnal, Maria;Miguez Rios, Monica;Sanchez Villegas, Rogelio;Alvarez, Elena;Fabado Alos, Javier;Baixeras, Joaquin;Gabriel Segarra-Moragues, Jose;Lucas Lledo, Jose Ignacio;Perez Santa-Rita, Jose Vicente;Monros, Juan S.;Monros Gonzalez, Juan S.;Angel Gomez-Serrano, Miguel;Lopez-Lopez, Pascual;Garilleti, Ricardo;Laguna, Emilio;Penalver Molla, Enrique;Jose Carreras, Esther San;Sanchez Frances, Raul;Gomez Valle, Silvia;Javier Jimenez-Lopez, F.;Fernandez-Gonzalez, Federico;Luis Yela, Jose;Torres Gonzalez, Felix;Garcia Martin, Joaquina Maria;Montserrat Martinez-Ortega, M.;Andres Sanchez, Santiago;Ojeda, Fernando;Blanco Pastor, Jose Luis;Rodriguez-Iglesias, Manuel A.;Ochoa-Hueso, Raol;Cabezas, Francisco J.;Galan-Diaz, Javier;Munoz-Rodriguez, Pablo;Canto, Paloma;Medina, Rafael;Gavilan, Rosario G.;Magana Ugarte, Rosina;Romero, Sara;Rico, Victor J.;Vazquez, Francisco M.;Mercadal i Corominas, Gabriel;Martinez-Sagarra, Gloria;Antonio Devesa, Juan;de la Estrella, Manuel;Romera, Graciela Gil;Ibarra, Pablo Tejero;Gonzalez-Samperiz, Pen'lope;Lazagabaster, Ignacio A.;Salcedo, Isabel;Etayo, Javier;Denzer, Wolfgang;Lopez-Pujol, Jordi;Garnatje, Teresa;Carlos Miranda, Jose;Rubiales, Juan M.;Martinez Labarga, Juan M.;Capo, Miquel;Andres Ros, Jose Vicente;Carretero Diaz, Jose-Miguel;Padulles Cubino, Josep;Borras, Joshua;Carlos Gutierrez-Marco, Juan;Mota, Juan F.;Pino Perez, Juan Jose;Saez, Llorenc;Serra Laliga, Lluis;Serra Laliga, Lluis;Lopez Merino, Lourdes;Buide del Real, M. Luisa;Vicens Fornes, Magdalena;Sanchez-Angulo, Manuel;Escudero, Marcial;Alcolea, Marta;Sanchez Gomez, Pedro;Fraga i Arguimbau, Pere;Orihuela-Rivero, Raol;Granjel, Rodrigo R.;Molino, Sonia;Garcia Mendizabal, Yoana;Carlsson, Bengt;Svensson, Brita;Bosagna, Carlos Guerrero;Arnqvist, Goran;Cardenas, Paco;Ahlberg, Per;Alstrom, Per;Liu, Zongzhuang;Alonso, German Hernandez;Wahlsteen, Eric;Bisang, Irene;Jonsson, Knud Andreas;Hedenas, Lars;Wedin, Mats;Noren, Michael;Stohr, Sabine;Kiel, Steffen;Rota, Jadranka;Wahlberg, Niklas;Tyler, Torbjorn;Arup, Ulf;Strid, Arne;Liljeblad, Johan;Lundin, Kennet;Nielsen, Peter;Strid, Arne;Alonso, German Hernandez;Chautems, Alain;Charpin, Andre;Mombrial, Florian;Zamora, Juan Carlos;Fumeaux, Nicolas;Clerc, Philippe;Garcia-Martin, Ana B.;Mueller, Andreas;Freitag, Anne;Landry, Bernard;Cuccodoro, Giulio;Sabatinelli, Guido;Lobl, Ivan;Valtotton, Laurent;Ruedi, Manuel;Schuchert, Peter;Praz, Christophe;Thivaiou, Danae;Klopfstein, Seraina;Cherix, Daniel;Mitchell, Edward;Mariaux, Jean;Haenni, Jean-Paul;Theurillat, Jean-Paul;Theurillat, Jean-Paul;Bernasconi, Marvco V.;Hawlitschek, Oliver;Samathi, Adun;Hyde, Kevin;Radji, Raoufou;Morales, J. Francisco;Charfi, Faouzia;El Mokni, Ridha;Gunay, Filiz;Agayeva, Saida;Giusti, Alessandro;Schuiteman, Andr';Goyder, David;Noltie, Henry J.;Larridon, Isabel;Bateman, Richard M.;Whittington, Andrew E.;Stewart, Nick;Leftwich, Ashley;Williams, Christopher David;Little, Crispin;Sherwood, Danniella;Lees, David C.;John, David Michael;Noltie, Henry J.;McLean, Ian F. G.;Badmin, John;Todd, Jonathan A.;Barclay, Maxwell V. L.;Geiser, Michael F.;Chen, Zhe-Yu;Telnov, Dmitry;Dickinson, Edward;Beccaloni, George W.;Badmin, John;McArthur, John M.;Davranoglou, Leonidas Romanos;Taberer, Tabitha R.;Shaw, Mark R.;Blagoderov, Vladimir;Young, Mark T.;Ebejer, Martin;Kelly, Martyn;Kelly, Martyn;Langton, Peter;Marchant, Rob;Schneider, Simon;Horton, Tammy;Wuster, Wolfgang;Telnov, Dmitry;Novikov, Andriy;Dubyna, Dmytro;Olshanskyi, Ihor;Fedoronchuk, Mykola;Shiyan, Natalia M.;Vinogradova, Oxana;Mikhailyuk, Tatiana;Hayova, Vera;Balashov, Igor;Kharchenko, Vitaliy A.;Khodosovtsev, Oleksandr;Kovalchuk, Oleksandr;Dyadichko, Vasily;Nachychko, Viktor O.;Kolomiichuk, Vitalii;Perkovsky, Evgeny E.;Perkovsky, Evgeny E.;Mailhos, Ary;Marchesi, Eduardo;Mauricio Bonifacino, Jose;Valtierra Sierra, Maria Victoria;Bauer, Aaron M.;Adeyemi, Adeyinka;Arnold, Keith;Franck, Alan;Burkett-Cadena, Nathan;Smith-Vaniz, William F.;Pandolfi, Alessandra;Dal Pos, Davide;Norrbom, Allen L.;Moncrieff, Andre E.;Remsen, J. V., Jr.;Esselstyn, Jacob;Eberhard, Jessica;Harms, Kyle E.;Johnson, Andrew;Capparella, Angelo;Rossi, Anthony;Casamatta, Dale;Namayandeh, Armin;Borkent, Art;Smith, Brian Tilston;Engel, Michael S.;Hellenthal, Barbara;Ratcliffe, Brett C.;O'Shea, Brian J.;Schmitt, C. Jonathan;Boufford, David;Morris, Paul J.;Shakya, Subir;Swift, Camm C.;McLeod, Samuel A.;Cohen, Chris M.;Borkent, Christopher J.;Borkent, Christopher J.;Rogers, D. Christopher;Gonzalez, Victor H.;Koenemann, Daniel;Campbell, David;Krause, David W.;Cushing, Paula;Sikes, Derek;Les, Don;DeKeyser, Edward S.;Cruz-Rivera, Edwin;Carter, Emily;Seeholzer, Glenn Fairbanks;Pratt, H. Douglas;Gerwin, John A.;Kaiser, Hinrich;Machio, Irene Villa;Harber, Julian;Zander, Richard H.;Gereau, Roy E.;Applequist, Wendy;Egger, J. Mark;Sagebiel, James Christopher;Lopez-Ribot, Jose L.;Atkinson, Thomas H.;Liebherr, James;Dombroskie, Jason J.;Hoghe, James N.;Wolfe, Jared;McGuire, Jimmy A.;Will, Kipling;Zuparko, Robert L.;Hansen, Robert W.;Brett, Roberta;Leal, Jose H.;Winston, Judith E.;Wen, Jun;Pinheiro, Paulo Duraes Pereira;Lee, Justin L.;Rabeler, Richard;Pargeter, Justin;Gregg, Katharine;Carpenter, Kenneth;McCracken, Kevin;Williams, Kevin;Korneyev, Severyn;Winker, Kevin;Austin, Kyhl A.;Watling, Les;Watson, Linda;Marin, Manuel;Epstein, Marc Edward;Key, Marcus M., Jr.;Marques, Mariana P.;Pyron, Mark;Dovciak, Martin;Hauser, Martin;Sage, Obediah;Garrison, Rosser W.;Winterton, Shaun L.;Gaimari, Stephen D.;West-Eberhard, Mary Jane;Diazgranados, Mauricio;Warren, Mel;Oliver, Michael K.;Ferro, Michael L.;Williams, Kevin;Evenhuis, Neal L.;Snow, Neil;Mizumoto, Nobuaki;Rakes, Patrick;Rohner, Patrick;Rozo-Lopez, Paula;Kerr, Peter H.;Stevens, Peter;Uetz, Peter;Wheeler, Quentin;DeWalt, R. Edward;McClelland, R. Kevan Schoonover;Hellenthal, Ronald;Meier, Rose;Heads, Sam W.;James, Samuel Wooster;Hilty, Steve;Adams, Susan B.;Letcher, Susan G.;Wood, Timothy S.;Walsh, S. J.;Murphy, William L.;Thomas, William Wayt;Khalimov, F. Z.;Rakhimov, Mukhammadtuychi;Abdullajonovich, Shodmonov Feruz;Tashpulatov, Yigitali;Rojas-Runjaic, Fernando J. M.;Cerda Perez, Hugo Gullermo;Torrecilla, Pedro;Zapata, Thirza Ruiz;Hoa, Hoang Quynh;Nguyen, Ngoc;Sharp, Cathy;Fitzpatrick, Moira

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