[en] Monolignols are the building blocks for lignin polymerization in the apoplastic domain. Monolignol biosynthesis, transport, storage, glycosylation, and deglycosylation are the main biological processes partaking in their homeostasis. In Arabidopsis thaliana, members of the uridine diphosphate-dependent glucosyltransferases UGT72E and UGT72B subfamilies have been demonstrated to glycosylate monolignols. Here, the poplar UGT72 family, which is clustered into four groups, was characterized: Group 1 UGT72AZ1 and UGT72AZ2, homologs of Arabidopsis UGT72E1-3, as well as group 4 UGT72B37 and UGT72B39, homologs of Arabidopsis UGT72B1-3, glycosylate monolignols. In addition, promoter-GUS analyses indicated that poplar UGT72 members are expressed within vascular tissues. At the subcellular level, poplar UGT72s belonging to group 1 and group 4 were found to be associated with the nucleus and the endoplasmic reticulum. However, UGT72A2, belonging to group 2, was localized in bodies associated with chloroplasts, as well as possibly in chloroplasts. These results show a partial conservation of substrate recognition between Arabidopsis and poplar homologs, as well as divergent functions between different groups of the UGT72 family, for which the substrates remain unknown.
Le Roy, J.; Huss, B.; Creach, A.; Hawkins, S.; Neutelings, G. Glycosylation is a major regulator of phenylpropanoid availability and biological activity in plants. Front. Plant Sci. 2016, 7, 735. [CrossRef]
Kumar, V.; Hainaut, M.; Delhomme, N.; Mannapperuma, C.; Immerzeel, P.; Street, N.R.; Henrissat, B.; Mellerowicz, E.J. Poplar carbohydrate-active enzymes: Whole-genome annotation and functional analyses based on RNA expression data. Plant J. 2019, 99, 589–609. [CrossRef] [PubMed]
Yonekura-Sakakibara, K.; Hanada, K. An evolutionary view of functional diversity in family 1 glycosyltransferases. Plant J. 2011, 66, 182–193. [CrossRef]
Hughes, J.; Hughes, M.A. Multiple secondary plant product UDP-glucose glucosyltransferase genes expressed in cassava (Manihot esculenta Crantz) cotyledons. DNA Seq. 1994, 5, 41–49. [CrossRef] [PubMed]
Osmani, S.A.; Bak, S.; Møller, B.L. Substrate specificity of plant UDP-dependent glycosyltransferases predicted from crystal structures and homology modeling. Phytochemistry 2009, 70, 325–347. [CrossRef] [PubMed]
Tiwari, P.; Sangwan, R.S.; Sangwan, N.S. Plant secondary metabolism linked glycosyltransferases: An update on expanding knowledge and scopes. Biotechnol. Adv. 2016, 34, 714–739. [CrossRef] [PubMed]
Tsuyama, T.; Takabe, K. Distribution of lignin and lignin precursors in differentiating xylem of Japanese cypress and poplar. J. Wood Sci. 2014, 60, 353–361. [CrossRef]
Freudenberg, K.; Harkin, J.M. The glucosides of cambial sap of spruce. Phytochemistry 1963, 2, 189–193. [CrossRef]
Rolando, C.; Daubresse, N.; Pollet, B.; Jouanin, L.; Lapierre, C. Lignification in poplar plantlets fed with deuterium-labelled lignin precursors. C. R. Biol. 2004, 327, 799–807. [CrossRef] [PubMed]
Terazawa, M.; Okuyama, H.; Miyake, M. Isolation of coniferin and syringin from the cambial tissue and inner-bark of some angiospermous woods. J. Jpn. Wood Res. Soc. 1984, 30, 409–412.
Fukushima, K.; Taguchi, S.; Matsui, N.; Yasuda, S. Heterogeneous distribution of monolignol glucosides in the stems of Magnolia kobus. Mokuzai Gakkaishi 1996, 42, 1029–1031.
Aoki, D.; Okumura, W.; Akita, T.; Matsushita, Y.; Yoshida, M.; Sano, Y.; Fukushima, K. Microscopic distribution of syringin in freeze-fixed Syringa vulgaris stems. Plant Direct 2019, 3, e00155. [CrossRef]
Aoki, D.; Nomura, K.; Hashiura, M.; Imamura, Y.; Miyata, S.; Terashima, N.; Matsushita, Y.; Nishimura, H.; Watanabe, T.; Katahira, M.; et al. Evaluation of ring-5 structures of guaiacyl lignin in Ginkgo biloba L. using solid-and liquid-state 13C NMR difference spectroscopy. Holzforschung 2019, 73, 1083–1092. [CrossRef]
Aoki, D.; Matsushita, Y.; Fukushima, K. Cryo-TOF-SIMS visualization of water-soluble compounds in plants. In ACS Symposium Series; American Chemical Society: Washington, DC, USA, 2018; Volume 1286, pp. 137–150. ISBN 9780841232969.
Aoki, D.; Hanaya, Y.; Akita, T.; Matsushita, Y.; Yoshida, M.; Kuroda, K.; Yagami, S.; Takama, R.; Fukushima, K. Distribution of coniferin in freeze-fixed stem of Ginkgo biloba L. by cryo-TOF-SIMS/SEM. Sci. Rep. 2016, 6, 31525. [CrossRef] [PubMed]
Terashima, N. Non-destructive approaches to identify the ultrastructure of lignified ginkgo cell walls. Int. J. Dev. Biol. 2007, 1, 170–177.
Tsuji, Y.; Fukushima, K. Behavior of monolignol glucosides in angiosperms. J. Agric. Food Chem. 2004, 52, 7651–7659. [CrossRef] [PubMed]
Väisänen, E.E.; Smeds, A.I.; Fagerstedt, K.V.; Teeri, T.H.; Willför, S.M.; Kärkönen, A. Coniferyl alcohol hinders the growth of tobacco BY-2 cells and Nicotiana benthamiana seedlings. Planta 2015, 242, 747–760. [CrossRef]
Liu, C.J. Deciphering the enigma of lignification: Precursor transport, oxidation, and the topochemistry of lignin assembly. Mol. Plant 2012, 5, 304–317. [CrossRef] [PubMed]
Wang, Y.; Chantreau, M.; Sibout, R.; Hawkins, S. Plant cell wall lignification and monolignol metabolism. Front. Plant Sci. 2013, 4, 220. [CrossRef] [PubMed]
Dima, O.; Morreel, K.; Vanholme, B.; Kim, H.; Ralph, J.; Boerjan, W. Small glycosylated lignin oligomers are stored in Arabidopsis leaf vacuoles. Plant Cell 2015, 27, 695–710. [CrossRef] [PubMed]
Miao, Y.C.; Liu, C.J. ATP-binding cassette-like transporters are involved in the transport of lignin precursors across plasma and vacuolar membranes. Proc. Natl. Acad. Sci. USA 2010, 107, 22728–22733. [CrossRef]
Alejandro, S.; Lee, Y.; Tohge, T.; Sudre, D.; Osorio, S.; Park, J.; Bovet, L.; Lee, Y.; Geldner, N.; Fernie, A.R.; et al. AtABCG29 is a monolignol transporter involved in lignin biosynthesis. Curr. Biol. 2012, 22, 1207–1212. [CrossRef]
Vermaas, J.V.; Dixon, R.A.; Chen, F.; Mansfield, S.D.; Boerjan, W.; Ralph, J.; Crowley, M.F.; Beckham, G.T. Passive membrane transport of lignin-related compounds. Proc. Natl. Acad. Sci. USA 2019, 116, 23117–23123. [CrossRef]
Lim, E.K.; Li, Y.; Parr, A.; Jackson, R.; Ashford, D.A.; Bowles, D.J. Identification of glucosyltransferase genes involved in sinapate metabolism and lignin synthesis in Arabidopsis. J. Biol. Chem. 2001, 276, 4344–4349. [CrossRef]
Lim, E.-K.; Jackson, R.G.; Bowles, D.J. Identification and characterisation of Arabidopsis glycosyltransferases capable of glucosylating coniferyl aldehyde and sinapyl aldehyde. FEBS Lett. 2005, 579, 2802–2806. [CrossRef]
Lin, J.S.; Huang, X.X.; Li, Q.; Cao, Y.; Bao, Y.; Meng, X.F.; Li, Y.J.; Fu, C.; Hou, B.K. UDP-glycosyltransferase 72B1 catalyzes the glucose conjugation of monolignols and is essential for the normal cell wall lignification in Arabidopsis thaliana. Plant J. 2016, 88, 26–42. [CrossRef] [PubMed]
Lanot, A.; Hodge, D.; Lim, E.K.; Vaistij, F.E.; Bowles, D.J. Redirection of flux through the phenylpropanoid pathway by increased glucosylation of soluble intermediates. Planta 2008, 228, 609–616. [CrossRef]
Huang, Y.; Li, C.Y.; Qi, Y.; Park, S.; Gibson, S.I. SIS8, a putative mitogen-activated protein kinase kinase kinase, regulates sugar-resistant seedling development in Arabidopsis. Plant J. 2014, 77, 577–588. [CrossRef] [PubMed]
Lefevere, H.; Bauters, L.; Gheysen, G. Salicylic acid biosynthesis in plants. Front. Plant Sci. 2020, 11, 338. [CrossRef]
Shi, R.; Wang, J.P.; Lin, Y.-C.; Li, Q.; Sun, Y.-H.; Chen, H.; Sederoff, R.R.; Chiang, V.L. Tissue and cell-type co-expression networks of transcription factors and wood component genes in Populus trichocarpa. Planta 2017, 245, 927–938. [CrossRef] [PubMed]
Sundell, D.; Street, N.R.; Kumar, M.; Mellerowicz, E.J.; Kucukoglu, M.; Johnsson, C.; Kumar, V.; Mannapperuma, C.; Delhomme, N.; Nilsson, O.; et al. Aspwood: High-spatial-resolution transcriptome profiles reveal uncharacterized modularity of wood formation in Populus tremula. Plant Cell 2017, 29, 1585–1604. [CrossRef]
Zhong, R.; Ye, Z.H. Secondary cell walls: Biosynthesis, patterned deposition and transcriptional regulation. Plant Cell Physiol. 2015, 56, 195–214. [CrossRef]
Pyo, H.; Demura, T.; Fukuda, H. TERE; a novel cis-element responsible for a coordinated expression of genes related to programmed cell death and secondary wall formation during differentiation of tracheary elements. Plant J. 2007, 51, 955–965. [CrossRef]
Yamaguchi, M.; Mitsuda, N.; Ohtani, M.; Ohme-Takagi, M.; Kato, K.; Demura, T. VASCULAR-RELATED NAC-DOMAIN 7 directly regulates the expression of a broad range of genes for xylem vessel formation. Plant J. 2011, 66, 579–590. [CrossRef]
Lim, E.-K.; Baldauf, S.; Li, Y.; Elias, L.; Worrall, D.; Spencer, S.P.; Jackson, R.G.; Taguchi, G.; Ross, J.; Bowles, D.J. Evolution of substrate recognition across a multigene family of glycosyltransferases in Arabidopsis. Glycobiology 2003, 13, 139–145. [CrossRef]
Han, D.Y.; Lee, H.R.; Kim, B.G.; Ahn, J.H. Biosynthesis of ferulic acid 4-O-glucoside and feruloyl glucoside using Escherichia coli harboring regioselective glucosyltransferases. Appl. Biol. Chem. 2016, 59, 481–484. [CrossRef]
Lanot, A.; Hodge, D.; Jackson, R.G.; George, G.L.; Elias, L.; Lim, E.-K.; Vaistij, F.E.; Bowles, D.J. The glucosyltransferase UGT72E2 is responsible for monolignol 4-O-glucoside production in Arabidopsis thaliana. Plant J. 2006, 48, 286–295. [CrossRef]
Achnine, L.; Huhman, D.V.; Farag, M.A.; Sumner, L.W.; Blount, J.W.; Dixon, R.A. Genomics-based selection and functional characterization of triterpene glycosyltransferases from the model legume Medicago truncatula. Plant J. 2005, 41, 875–887. [CrossRef]
Chapelle, A. Caractérisation de gènes de β-glucosidase et d’UDP-glycosyltransférase potentiellement impliqués dans la lignification chez Arabidopsis thaliana. Ph.D. Thesis, Université Paris-Sud, Orsay, France, 2009.
McCarthy, R.L.; Zhong, R.; Ye, Z.H. Secondary wall NAC binding element (SNBE), a key Cis-acting element required for target gene activation by secondary wall NAC master switches. Plant Signal. Behav. 2011, 6, 1282–1285. [CrossRef]
Ohashi-Ito, K.; Oda, Y.; Fukuda, H. Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 directly regulates the genes that govern programmed cell death and secondary wall formation during xylem differentiation. Plant Cell 2010, 22, 3461–3473. [CrossRef]
Kim, W.C.; Ko, J.H.; Han, K.H. Identification of a cis-acting regulatory motif recognized by MYB46, a master transcriptional regulator of secondary wall biosynthesis. Plant Mol. Biol. 2012, 78, 489–501. [CrossRef]
Zhong, R.; McCarthy, R.L.; Haghighat, M.; Ye, Z.-H. The poplar MYB master switches bind to the SMRE site and activate the secondary wall biosynthetic program during wood formation. PLoS ONE 2013, 8, e69219. [CrossRef] [PubMed]
McCarthy, R.L.; Zhong, R.; Fowler, S.; Lyskowski, D.; Piyasena, H.; Carleton, K.; Spicer, C.; Ye, Z.H. The poplar MYB transcription factors, PtrMYB3 and PtrMYB20, are involved in the regulation of secondary wall biosynthesis. Plant Cell Physiol. 2010, 51, 1084–1090. [CrossRef]
Zhong, R.; Ye, Z.H. MYB46 and MYB83 bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes. Plant Cell Physiol. 2012, 53, 368–380. [CrossRef]
Nakano, Y.; Yamaguchi, M.; Endo, H.; Rejab, N.A.; Ohtani, M. NAC-MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants. Front. Plant Sci. 2015, 6, 288. [CrossRef]
Ko, J.H.; Jeon, H.W.; Kim, W.C.; Kim, J.Y.; Han, K.H. The MYB46/MYB83-mediated transcriptional regulatory programme is a gatekeeper of secondary wall biosynthesis. Ann. Bot. 2014, 114, 1099–1107. [CrossRef]
Zhong, R.; Lee, C.; Ye, Z.H. Global analysis of direct targets of secondary wall NAC master switches in Arabidopsis. Mol. Plant 2010, 3, 1087–1103. [CrossRef] [PubMed]
Bollhöner, B.; Jokipii-Lukkari, S.; Bygdell, J.; Stael, S.; Adriasola, M.; Muñiz, L.; Van Breusegem, F.; Ezcurra, I.; Wingsle, G.; Tuominen, H. The function of two type II metacaspases in woody tissues of Populus trees. New Phytol. 2018, 217, 1551–1565. [CrossRef] [PubMed]
Endo, H.; Yamaguchi, M.; Tamura, T.; Nakano, Y.; Nishikubo, N.; Yoneda, A.; Kato, K.; Kubo, M.; Kajita, S.; Katayama, Y.; et al. Multiple classes of transcription factors regulate the expression of VASCULAR-RELATED NAC-DOMAIN7, a master switch of xylem vessel differentiation. Plant Cell Physiol. 2015, 56, 242–254. [CrossRef]
Wang, Y.W.; Wang, W.C.; Jin, S.H.; Wang, J.; Wang, B.; Hou, B.K. Over-expression of a putative poplar glycosyltransferase gene, PtGT1, in tobacco increases lignin content and causes early flowering. J. Exp. Bot. 2012, 63, 2799–2808. [CrossRef]
König, S.; Feussner, K.; Kaever, A.; Landesfeind, M.; Thurow, C.; Karlovsky, P.; Gatz, C.; Polle, A.; Feussner, I. Soluble phenylpropanoids are involved in the defense response of Arabidopsis against Verticillium longisporum. New Phytol. 2014, 202, 823–837. [CrossRef]
Rehman, H.M.; Nawaz, M.A.; Shah, Z.H.; Ludwig-Müller, J.; Chung, G.; Ahmad, M.Q.; Yang, S.H.; Lee, S.I. Comparative genomic and transcriptomic analyses of Family-1 UDP glycosyltransferase in three Brassica species and Arabidopsis indicates stress-responsive regulation. Sci. Rep. 2018, 8, 1875. [CrossRef]
Kosugi, S.; Hasebe, M.; Tomita, M.; Yanagawa, H. Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc. Natl. Acad. Sci. USA 2009, 106, 10171–10176. [CrossRef]
Bassard, J.E.; Richert, L.; Geerinck, J.; Renault, H.; Duval, F.; Ullmann, P.; Schmitt, M.; Meyer, E.; Mutterer, J.; Boerjan, W.; et al. Protein-protein and protein-membrane associations in the lignin pathway. Plant Cell 2012, 24, 4465–4482. [CrossRef]
Ono, N.N.; Qin, X.; Wilson, A.E.; Li, G.; Tian, L. Two UGT84 family glycosyltransferases catalyze a critical reaction of hydrolyzable tannin biosynthesis in pomegranate (Punica granatum). PLoS ONE 2016, 11, e0156319. [CrossRef]
Gallage, N.J.; Jørgensen, K.; Janfelt, C.; Nielsen, A.J.Z.; Naake, T.; Duński, E.; Dalsten, L.; Grisoni, M.; Møller, B.L. The intracellular localization of the vanillin biosynthetic machinery in pods of Vanilla planifolia. Plant Cell Physiol. 2018, 59, 304–318. [CrossRef]
Knudsen, C.; Gallage, N.J.; Hansen, C.C.; Møller, B.L.; Laursen, T. Dynamic metabolic solutions to the sessile life style of plants. Nat. Prod. Rep. 2018, 35, 1140–1155. [CrossRef]
Machettira, A.B.; Groß, L.E.; Tillmann, B.; Weis, B.L.; Englich, G.; Sommer, M.S.; Königer, M.; Schleiff, E. Protein-induced modulation of chloroplast membrane morphology. Front. Plant. Sci. 2012, 2. [CrossRef]
Perello, C.; Llamas, E.; Burlat, V.; Ortiz-Alcaide, M.; Phillips, M.A.; Pulido, P.; Rodriguez-Concepcion, M. Differential subplastidial localization and turnover of enzymes involved in isoprenoid biosynthesis in chloroplasts. PLoS ONE 2016, 11, e0150539. [CrossRef]
Armenteros, J.J.A.; Salvatore, M.; Emanuelsson, O.; Winther, O.; Von Heijne, G.; Elofsson, A.; Nielsen, H. Detecting sequence signals in targeting peptides using deep learning. Life Sci. Alliance 2019, 2. [CrossRef]
Baldacci-Cresp, F.; Moussawi, J.; Leplé, J.-C.; Van Acker, R.; Kohler, A.; Candiracci, J.; Twyffels, L.; Spokevicius, A.V.; Bossinger, G.; Laurans, F.; et al. PtaRHE1, a Populus tremula × Populus alba RING-H2 protein of the ATL family, has a regulatory role in secondary phloem fibre development. Plant. J. 2015, 82, 978–990. [CrossRef]
Liu, W.; Xie, Y.; Ma, J.; Luo, X.; Nie, P.; Zuo, Z.; Lahrmann, U.; Zhao, Q.; Zheng, Y.; Zhao, Y.; et al. IBS: An illustrator for the presentation and visualization of biological sequences. Bioinformatics 2015, 31, 3359–3361. [CrossRef]
Dereeper, A.; Guignon, V.; Blanc, G.; Audic, S.; Buffet, S.; Chevenet, F.; Dufayard, J.-F.; Guindon, S.; Lefort, V.; Lescot, M.; et al. Phylogeny.fr: Robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008, 36, W465–W469. [CrossRef]
Anisimova, M.; Gascuel, O. Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst. Biol. 2006, 55, 539–552. [CrossRef]
Baldacci-Cresp, F.; Sacré, P.-Y.; Twyffels, L.; Mol, A.; Vermeersch, M.; Ziemons, E.; Hubert, P.; Pérez-Morga, D.; El Jaziri, M.; de Almeida Engler, J.; et al. Poplar–root knot nematode interaction: A model for perennial woody species. Mol. Plant.-Microbe Interact. 2016, 29, 560–572. [CrossRef]
Hemerly, A.S.; Ferreira, P.; de Almeida Engler, J.; Van Montagu, M.; Engler, G.; Inze, D. cdc2a expression in Arabidopsis is linked with competence for cell division. Plant. Cell 1993, 5, 1711–1723. [PubMed]
Karimi, M.; Inzé, D.; Depicker, A. GATEWAY™ vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 2002, 7, 193–195. [CrossRef]
Nelson, B.K.; Cai, X.; Nebenführ, A. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 2007, 51, 1126–1136. [CrossRef] [PubMed]
Huang, F.C.; Giri, A.; Daniilidis, M.; Sun, G.; Härtl, K.; Hoffmann, T.; Schwab, W. Structural and functional analysis of UGT92G6 suggests an evolutionary link between mono-and disaccharide glycoside-forming transferases. Plant Cell Physiol. 2018, 59, 857–870. [CrossRef]
Leple, J.C.; Brasileiro, A.C.M.; Michel, M.F.; Delmotte, F.; Jouanin, L. Transgenic poplars: Expression of chimeric genes using four different constructs. Plant Cell Rep. 1992, 11, 137–141. [CrossRef] [PubMed]
Van Acker, R.; Vanholme, R.; Storme, V.; Mortimer, J.; Dupree, P.; Boerjan, W. Lignin biosynthesis perturbations affect secondary cell wall composition and saccharification yield in Arabidopsis thaliana. Biotechnol. Biofuels 2013, 6, 46. [CrossRef]
Foster, C.E.; Martin, T.M.; Pauly, M. Comprehensive compositional analysis of plant cell walls (lignocellulosic biomass) Part I: Lignin. J. Vis. Exp. 2010, 37, e1745. [CrossRef] [PubMed]