Harnessing Plant Sugar Metabolism for Glycoengineering
Abstract
:Simple Summary
Abstract
1. Introduction
2. Engineering Nucleotide Sugar Biosynthesis
3. De Novo Nucleotide Sugar Engineering
4. Engineering Nucleotide Sugar Transport and Localization
5. Engineering Plant Glycosyltransferases
6. Glycoconjugate Biosynthetic Pathway Engineering
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Bar-On, Y.M.; Phillips, R.; Milo, R. The biomass distribution on Earth. Proc. Natl. Acad. Sci. USA 2018, 115, 6506–6511. [Google Scholar] [CrossRef]
- Loqué, D.; Scheller, H.V.; Pauly, M. Engineering of plant cell walls for enhanced biofuel production. Curr. Opin. Plant Biol. 2015, 25, 151–161. [Google Scholar] [CrossRef] [PubMed]
- Brandon, A.G.; Scheller, H.V. Engineering of Bioenergy Crops: Dominant Genetic Approaches to Improve Polysaccharide Properties and Composition in Biomass. Front. Plant Sci. 2020, 11, 282. [Google Scholar] [CrossRef] [PubMed]
- Burton, R.A.; Fincher, G.B. Plant cell wall engineering: Applications in biofuel production and improved human health. Curr. Opin. Biotechnol. 2014, 26, 79–84. [Google Scholar] [CrossRef] [PubMed]
- Yoshida, K.; Sakamoto, S.; Mitsuda, N. In Planta Cell Wall Engineering: From Mutants to Artificial Cell Walls. Plant Cell Physiol. 2021, 62, 1813–1827. [Google Scholar] [CrossRef] [PubMed]
- Voiniciuc, C. It’s time to go glyco in cell wall bioengineering. Curr. Opin. Plant Biol. 2023, 71, 102313. [Google Scholar] [CrossRef] [PubMed]
- Bar-Peled, M.; O’Neill, M.A. Plant Nucleotide Sugar Formation, Interconversion, and Salvage by Sugar Recycling. Annu. Rev. Plant Biol. 2011, 62, 127–155. [Google Scholar] [CrossRef]
- Figueroa, C.M.; Lunn, J.E.; Iglesias, A.A. Nucleotide-sugar metabolism in plants: The legacy of Luis F. Leloir. J. Exp. Bot. 2021, 72, 4053–4067. [Google Scholar] [CrossRef]
- Gondolf, V.M.; Stoppel, R.; Ebert, B.; Rautengarten, C.; Liwanag, A.J.; Loqué, D.; Scheller, H.V. A gene stacking approach leads to engineered plants with highly increased galactan levels in Arabidopsis. BMC Plant Biol. 2014, 14, 344. [Google Scholar] [CrossRef]
- Pauly, M.; Keegstra, K. Cell-wall carbohydrates and their modification as a resource for biofuels. Plant J. 2008, 54, 559–568. [Google Scholar] [CrossRef]
- Ndimande, S. Increasing Cellulosic Biomass in Sugarcane; Stellenbosch University: Stellenbosch, South Africa, 2014. [Google Scholar]
- Huang, Y.; Wang, L.; Hu, S.; Luo, X.; Cao, Y. Overexpression of the bamboo sucrose synthase gene (BeSUS5) improves cellulose production, cell wall thicknessand fiber quality in transgenic poplar. Tree Genet. Genomes 2020, 16, 75. [Google Scholar] [CrossRef]
- Daloso, D.M.; dos Anjos, L.; Fernie, A.R. Roles of sucrose in guard cell regulation. New Phytol. 2016, 211, 809–818. [Google Scholar] [CrossRef]
- Nguyen, Q.A.; Luan, S.; Wi, S.G.; Bae, H.; Lee, D.-S.; Bae, H.-J. Pronounced Phenotypic Changes in Transgenic Tobacco Plants Overexpressing Sucrose Synthase May Reveal a Novel Sugar Signaling Pathway. Front. Plant Sci. 2016, 6, 1216. [Google Scholar] [CrossRef] [PubMed]
- McCormick, A.J.; Watt, D.A.; Cramer, M.D. Supply and demand: Sink regulation of sugar accumulation in sugarcane. J. Exp. Bot. 2009, 60, 357–364. [Google Scholar] [CrossRef]
- Zeleny, R.; Kolarich, D.; Strasser, R.; Altmann, F. Sialic acid concentrations in plants are in the range of inadvertent contamination. Planta 2006, 224, 222–227. [Google Scholar] [CrossRef] [PubMed]
- Castilho, A.; Strasser, R.; Stadlmann, J.; Grass, J.; Jez, J.; Gattinger, P.; Kunert, R.; Quendler, H.; Pabst, M.; Leonard, R.; et al. In Planta Protein Sialylation through Overexpression of the Respective Mammalian Pathway*. J. Biol. Chem. 2010, 285, 15923–15930. [Google Scholar] [CrossRef] [PubMed]
- Temple, H.; Saez-Aguayo, S.; Reyes, F.C.; Orellana, A. The inside and outside: Topological issues in plant cell wall biosynthesis and the roles of nucleotide sugar transporters. Glycobiology 2016, 26, 913–925. [Google Scholar] [CrossRef]
- Rautengarten, C.; Ebert, B.; Liu, L.; Stonebloom, S.; Smith-Moritz, A.M.; Pauly, M.; Orellana, A.; Scheller, H.V.; Heazlewood, J.L. The Arabidopsis Golgi-localized GDP-L-fucose transporter is required for plant development. Nat. Commun. 2016, 7, 12119. [Google Scholar] [CrossRef]
- Rautengarten, C.; Birdseye, D.; Pattathil, S.; McFarlane, H.E.; Saez-Aguayo, S.; Orellana, A.; Persson, S.; Hahn, M.G.; Scheller, H.V.; Heazlewood, J.L.; et al. The elaborate route for UDP-arabinose delivery into the Golgi of plants. Proc. Natl. Acad. Sci. USA 2017, 114, 4261–4266. [Google Scholar] [CrossRef]
- Zhao, X.; Liu, N.; Shang, N.; Zeng, W.; Ebert, B.; Rautengarten, C.; Zeng, Q.-Y.; Li, H.; Chen, X.; Beahan, C.; et al. Three UDP-xylose transporters participate in xylan biosynthesis by conveying cytosolic UDP-xylose into the Golgi lumen in Arabidopsis. J. Exp. Bot. 2018, 69, 1125–1134. [Google Scholar] [CrossRef]
- Hsu, T.M.; Welner, D.H.; Russ, Z.N.; Cervantes, B.; Prathuri, R.L.; Adams, P.D.; Dueber, J.E. Employing a biochemical protecting group for a sustainable indigo dyeing strategy. Nat. Chem. Biol. 2018, 14, 256–261. [Google Scholar] [CrossRef]
- Hardman, J.M.; Brooke, R.T.; Zipp, B.J. Cannabinoid glycosides: In vitro production of a new class of cannabinoids with improved physicochemical properties. BioRxiv 2017, 104349. [Google Scholar] [CrossRef]
- Zipp, B.J.; Hardman, J.M.; Brooke, R.T.; Deutscher, T.R. Cannabinoid Glycoside Prodrugs and Methods of Synthesis. U.S. Patent 20230346952, 20 September 2023. [Google Scholar]
- Brandle, J.E.; Telmer, P.G. Steviol glycoside biosynthesis. Phytochemistry 2007, 68, 1855–1863. [Google Scholar] [CrossRef] [PubMed]
- Yang, M.; Fehl, C.; Lees, K.V.; Lim, E.-K.; Offen, W.A.; Davies, G.J.; Bowles, D.J.; Davidson, M.G.; Roberts, S.J.; Davis, B.G. Functional and informatics analysis enables glycosyltransferase activity prediction. Nat. Chem. Biol. 2018, 14, 1109–1117. [Google Scholar] [CrossRef]
- Brazier-Hicks, M.; Offen, W.A.; Gershater, M.C.; Revett, T.J.; Lim, E.-K.; Bowles, D.J.; Davies, G.J.; Edwards, R. Characterization and engineering of the bifunctional N- and O-glucosyltransferase involved in xenobiotic metabolism in plants. Proc. Natl. Acad. Sci. USA 2007, 104, 20238–20243. [Google Scholar] [CrossRef]
- He, J.-B.; Zhao, P.; Hu, Z.-M.; Liu, S.; Kuang, Y.; Zhang, M.; Li, B.; Yun, C.-H.; Qiao, X.; Ye, M. Molecular and Structural Characterization of a Promiscuous C-Glycosyltransferase from Trollius chinensis. Angew. Chem. Int. Ed. 2019, 58, 11513–11520. [Google Scholar] [CrossRef] [PubMed]
- Teze, D.; Coines, J.; Fredslund, F.; Dubey, K.D.; Bidart, G.N.; Adams, P.D.; Dueber, J.E.; Svensson, B.; Rovira, C.; Welner, D.H. O-/N-/S-Specificity in Glycosyltransferase Catalysis: From Mechanistic Understanding to Engineering. ACS Catal. 2021, 11, 1810–1815. [Google Scholar] [CrossRef]
- George Thompson, A.M.; Iancu, C.V.; Neet, K.E.; Dean, J.V.; Choe, J. Differences in salicylic acid glucose conjugations by UGT74F1 and UGT74F2 from Arabidopsis thaliana. Sci. Rep. 2017, 7, 46629. [Google Scholar] [CrossRef]
- Hiromoto, T.; Honjo, E.; Noda, N.; Tamada, T.; Kazuma, K.; Suzuki, M.; Blaber, M.; Kuroki, R. Structural basis for acceptor-substrate recognition of UDP-glucose: Anthocyanidin 3-O-glucosyltransferase from Clitoria ternatea. Protein Sci. 2015, 24, 395–407. [Google Scholar] [CrossRef]
- Yang, T.; Zhang, J.; Ke, D.; Yang, W.; Tang, M.; Jiang, J.; Cheng, G.; Li, J.; Cheng, W.; Wei, Y.; et al. Hydrophobic recognition allows the glycosyltransferase UGT76G1 to catalyze its substrate in two orientations. Nat. Commun. 2019, 10, 3214. [Google Scholar] [CrossRef]
- Crystal Structures of Rhamnosyltransferase UGT89C1 from Arabidopsis Thaliana Reveal the Molecular Basis of Sugar Donor Specificity for UDP-β-l-Rhamnose and Rhamnosylation Mechanism-Zong-2019-The Plant Journal-Wiley Online Library. Available online: https://onlinelibrary.wiley.com/doi/full/10.1111/tpj.14321 (accessed on 9 November 2023).
- Brandt, W.; Schulze, E.; Liberman-Aloni, R.; Bartelt, R.; Pienkny, S.; Carmeli-Weissberg, M.; Frydman, A.; Eyal, Y. Structural modeling of two plant UDP-dependent sugar-sugar glycosyltransferases reveals a conserved glutamic acid residue that is a hallmark for sugar acceptor recognition. J. Struct. Biol. 2021, 213, 107777. [Google Scholar] [CrossRef] [PubMed]
- Zhang, M.; Li, F.-D.; Li, K.; Wang, Z.-L.; Wang, Y.-X.; He, J.-B.; Su, H.-F.; Zhang, Z.-Y.; Chi, C.-B.; Shi, X.-M.; et al. Functional Characterization and Structural Basis of an Efficient Di-C-glycosyltransferase from Glycyrrhiza glabra. J. Am. Chem. Soc. 2020, 142, 3506–3512. [Google Scholar] [CrossRef]
- Wetterhorn, K.M.; Gabardi, K.; Michlmayr, H.; Malachova, A.; Busman, M.; McCormick, S.P.; Berthiller, F.; Adam, G.; Rayment, I. Determinants and Expansion of Specificity in a Trichothecene UDP-Glucosyltransferase from Oryza sativa. Biochemistry 2017, 56, 6585–6596. [Google Scholar] [CrossRef] [PubMed]
- Li, J.; Qu, G.; Shang, N.; Chen, P.; Men, Y.; Liu, W.; Mei, Z.; Sun, Y.; Sun, Z. Near-perfect control of the regioselective glucosylation enabled by rational design of glycosyltransferases. Green Synth. Catal. 2021, 2, 45–53. [Google Scholar] [CrossRef]
- Xie, K.; Zhang, X.; Sui, S.; Ye, F.; Dai, J. Exploring and applying the substrate promiscuity of a C-glycosyltransferase in the chemo-enzymatic synthesis of bioactive C-glycosides. Nat. Commun. 2020, 11, 5162. [Google Scholar] [CrossRef] [PubMed]
- Sun, Y.; Chen, Z.; Yang, J.; Mutanda, I.; Li, S.; Zhang, Q.; Zhang, Y.; Zhang, Y.; Wang, Y. Pathway-specific enzymes from bamboo and crop leaves biosynthesize anti-nociceptive C-glycosylated flavones. Commun. Biol. 2020, 3, 110. [Google Scholar] [CrossRef]
- Wang, Z.-L.; Gao, H.-M.; Wang, S.; Zhang, M.; Chen, K.; Zhang, Y.-Q.; Wang, H.-D.; Han, B.-Y.; Xu, L.-L.; Song, T.-Q.; et al. Dissection of the general two-step di-C-glycosylation pathway for the biosynthesis of (iso)schaftosides in higher plants. Proc. Natl. Acad. Sci. USA 2020, 117, 30816–30823. [Google Scholar] [CrossRef]
- Putkaradze, N.; Teze, D.; Fredslund, F.; Hededam Welner, D. Natural product C -glycosyltransferases–a scarcely characterised enzymatic activity with biotechnological potential. Nat. Prod. Rep. 2021, 38, 432–443. [Google Scholar] [CrossRef]
- Ketudat Cairns, J.R.; Mahong, B.; Baiya, S.; Jeon, J.-S. β-Glucosidases: Multitasking, moonlighting or simply misunderstood? Plant Sci. 2015, 241, 246–259. [Google Scholar] [CrossRef]
- Mészáros, Z.; Nekvasilová, P.; Bojarová, P.; Křen, V.; Slámová, K. Advanced glycosidases as ingenious biosynthetic instruments. Biotechnol. Adv. 2021, 49, 107733. [Google Scholar] [CrossRef]
- Van Herpen, T.W.J.M.; Cankar, K.; Nogueira, M.; Bosch, D.; Bouwmeester, H.J.; Beekwilder, J. Nicotiana benthamiana as a Production Platform for Artemisinin Precursors. PLoS ONE 2010, 5, e14222. [Google Scholar] [CrossRef] [PubMed]
- Andersen-Ranberg, J.; Kongstad, K.T.; Nafisi, M.; Staerk, D.; Okkels, F.T.; Mortensen, U.H.; Lindberg Møller, B.; Frandsen, R.J.N.; Kannangara, R. Synthesis of C-Glucosylated Octaketide Anthraquinones in Nicotiana benthamiana by Using a Multispecies-Based Biosynthetic Pathway. ChemBioChem 2017, 18, 1893–1897. [Google Scholar] [CrossRef] [PubMed]
- Jansing, J.; Sack, M.; Augustine, S.M.; Fischer, R.; Bortesi, L. CRISPR/Cas9-mediated knockout of six glycosyltransferase genes in Nicotiana benthamiana for the production of recombinant proteins lacking β-1,2-xylose and core α-1,3-fucose. Plant Biotechnol. J. 2019, 17, 350–361. [Google Scholar] [CrossRef] [PubMed]
- Parsons, J.; Altmann, F.; Arrenberg, C.K.; Koprivova, A.; Beike, A.K.; Stemmer, C.; Gorr, G.; Reski, R.; Decker, E.L. Moss-based production of asialo-erythropoietin devoid of Lewis A and other plant-typical carbohydrate determinants. Plant Biotechnol. J. 2012, 10, 851–861. [Google Scholar] [CrossRef]
- Margolin, E.; Crispin, M.; Meyers, A.; Chapman, R.; Rybicki, E.P. A Roadmap for the Molecular Farming of Viral Glycoprotein Vaccines: Engineering Glycosylation and Glycosylation-Directed Folding. Front. Plant Sci. 2020, 11, 609207. [Google Scholar] [CrossRef]
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Tang, S.N.; Barnum, C.R.; Szarzanowicz, M.J.; Sirirungruang, S.; Shih, P.M. Harnessing Plant Sugar Metabolism for Glycoengineering. Biology 2023, 12, 1505. https://doi.org/10.3390/biology12121505
Tang SN, Barnum CR, Szarzanowicz MJ, Sirirungruang S, Shih PM. Harnessing Plant Sugar Metabolism for Glycoengineering. Biology. 2023; 12(12):1505. https://doi.org/10.3390/biology12121505
Chicago/Turabian StyleTang, Sophia N., Collin R. Barnum, Matthew J. Szarzanowicz, Sasilada Sirirungruang, and Patrick M. Shih. 2023. "Harnessing Plant Sugar Metabolism for Glycoengineering" Biology 12, no. 12: 1505. https://doi.org/10.3390/biology12121505