Plant secondary metabolite and glycosyltransferases

Authors

DOI:

https://doi.org/10.5564/pib.v39i1.3147

Keywords:

glycosylation, UDP- dependent glycosyltransferase, PSPG box

Abstract

Glycosylation is the last step in the biosynthesis of the secondary metabolite. The glycosylation process is catalyzed by glycosyltransferase (GTs), which are highly divergent and polyphyletic and belong to a multigene family in plant organisms. Among them, the GT family 1 is the largest, often referred to as UDP-glycosyltransferases (UGTs) and catalyzes the transfer of a glycosyl moiety from UDP sugars to a diverse array of substrates, including hormones, secondary metabolites, and xenobiotics such as pesticides and herbicides. UGTs play an essential role in stabilizing, enhancing water solubility, and deactivating/ detoxifying natural products, leading to regulating metabolic homeostasis, detoxifying xenobiotics, and the biosynthesis, storage, and transport properties of secondary metabolites. In this review, we include the classification, nomenclature, and sequence homology of glycosyltransferases and summarize their roles in plant defense mechanisms, detoxification, secondary metabolite biosynthesis, and hormone regulation with examples from some studies conducted in plants. Knowing more about the function and mechanism of this gene in the organism will be essential to discover its industrial and scientific importance in the future. It is a significant topic in the pharmaceutical industry, especially as it plays a critical role in the synthesis of secondary metabolites and the defense system of plants.

Ургамлын хоёрдогч метаболит ба гликозилтрансферазууд

Хураангуй. Гликозиляцийн процесс нь хоёрдогч метаболитын бионийлэгжлийн хамгийн сүүлийн шат юм. Гликозиляцийн процессыг гликозилтрансфераза (GTs) хурдасгадаг бөгөөд тэдгээр нь олон ялгаатай, полифилетик шинж чанартай бөгөөд ургамлын маш том бүлэг ген юм. Тэдгээрийн дотроос GT 1-р бүлэг хамгийн том нь бөгөөд ихэвчлэн UDP-гликозилтрансфераза (UGTs) гэж нэрлэгддэг ба UDP сахараас гликозилийн хэсгийг гормон, хоёрдогч метаболит, ксенобиотик зэрэг олон төрлийн субстрат уруу шилжүүлдэг катализаторын үүрэг гүйцэтгэдэг. UGT нь байгалийн гаралтай бүтээгдэхүүнийг тогтворжуулах, усанд уусах чадварыг сайжруулах, идэвхгүйжүүлэх/ хоргүйжүүлэхэд чухал үүрэг гүйцэтгэдэг бөгөөд энэ нь бодисын солилцооны гомеостазыг зохицуулах, ксенобиотикийг хоргүйжүүлэх, хоёрдогч метаболитуудын бионийлэгжил, хадгалалт, зөөвөрлөлтийг зохицуулахад оролцдог. Энэхүү тоймд бид гликозилтрансферазын ангилал, нэршил, дарааллын гомологи зэргийг багтаахын зэрэгцээ ургамлын хамгааллын механизм, хоргүйжүүлэлт, хоёрдогч метаболитын бионийлэгжил, дааврын зохицуулалт зэрэгт тэдгээрийн гүйцэтгэх үүргийг ургамалд хийсэн зарим судалгааны жишээн дээр нэгтгэн харуулав. Энэхүү бүлэг генийн организмд , ялангуяа хоёрдогч метаболитуудын нийлэгжилт, ургамал хамгааллын системд гүйцэтгэх үүрэг, механизмын талаар илүү ихийг мэдэх нь шинжлэх ухаанд чухал ач холбогдолтойгоос гадна ирээдүйд түүний үйлдвэрлэлд тус дэм болох юм.
Түлхүүр үгс: гликозиляци, UDP-аас хамааралтай гликозилтрансфераза, PSPG мотиф

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References

M. L. Sinnott, “Catalytic mechanism of enzymic glycosyl transfer,” Chem Rev., vol. 90 no. 7, pp. 1171–1202, 1990, https://doi.org/10.1021/cr00105a006

J. A. Campbell, G. J. Davies, V. Bulone and B. Henrissat, “A classification of nucleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities,” Biochem J., vol. 326, no. Pt 3, pp. 929–939, 1997, https://doi.org/10.1042/bj3260929u

P. Jones and T. Vogt. “Glycosyltransferases in secondary plant metabolism: tranquilizers and stimulant controllers,” Planta, vol. 213, no. 2, pp. 164-174, 2001, https://doi.org/10.1007/s004250000492

P. M. Coutinho, E. Deleury, G. J. Davies and B. Henrissat. “An evolving hierarchical family classification for glycosyltransferases,” J. Mol. Biol., vol. 328, no. 2, pp. 307–317, 2003, https://doi.org/10.1016/S0022-2836(03)00307-3

X. Lu, L. Huang, H. V. Scheller and J. D. Keasling, “Medicinal terpenoid UDP-glycosyltransferases in plants: recent advances and research strategies,” Journal of Experimental Botany, vol. 74, no. 5, pp. 1343–1357, 2023, https://doi.org/10.1093/jxb/erac505

Mackenzie, P.I., I. S. Owens, B. Burchell, K. W. Bock, A. Bairoch, A. Belanger, S. Fournel- Gigleux, M. Green, D. W. Hum, T. Iyanagi, D. Lancet, P. Louisot, J. Magdalou, J. R. Chowdhury, J. K. Ritter, H. Schanchter, T. R. Terphly, K. F. Tipton and D. W. Nebert, “The UDP glycosyltransferase gene superfamily: recommended nomenclature update based on evolutionary divergence,” Pharmacogenetics, vol. 7, pp. 255-269, 1997, https://doi.org/10.1097/00008571-199708000-00001

E. K. Lim and D. J. Bowles, “A class of plant glycosyltransferases involved in cellular homeostasis,” The EMBO J., vol. 23, pp. 2915-2922, 2004, https://doi.org/10.1038/sj.emboj.7600295

Y. Li, S. Baldauf, E. K. Lim and D. J. Bowles, “Phylogenetic analysis of the UDP-glycosyltransferase multigene family of Arabidopsis thaliana,” J Biol Chem., vol. 276, pp. 4338–4343, 2001, https://doi.org/10.1074/jbc.M007447200

J. Ross, Y. Li, E. Lim and D. J. Bowles, “Higher plant glycosyltransferases,” Genome Biol., vol. 2, pp. 3004.1–3004.6, 2001, https://doi.org/10.1186/gb-2001-2-2-reviews3004

E. Wilson and L. Tian, “Phylogenomic analysis of UDP-dependent glycosyltransferases provides insights into the evolutionary landscape of glycosylation in plant metabolism,” The Plant Journal, vol. 100, pp. 1273–1288, 201[, https://doi.org/10.1111/tpj.14514

TAIR homepage https://www.arabidopsis.org/

K. Zhou, L. Hu, P. Li, X. Gong and F. Ma, “Genome-wide identification of glycosyltransferases converting phloretin to phloridzin in Malus species,” Plant Science, vol. 265, pp. 131-145, 2017, https://doi.org/10.1016/j.plantsci.2017.10.003

Y. Wei, H. Mu, G. Xu, Y. Wang, Y. Li, S. Li and L. Wang, “Genome-wide analysis and functional characterization of the UDP-glycosyltransferase family in grapes,” Horticulturae, vol. 7, no. 8, pp. 204, 2021, https://doi.org/10.3390/horticulturae7080204

L. Caputi, M. Malnoy, V. Goremykin, S. Nikiforova and S. Martens, “A genome-wide phylogenetic reconstruction of family 1 UDP-glycosyltransferases revealed the expansion of the family during the adaptation of plants to life on land,” Plant J., vol. 69, pp. 1030-1042, 2012. https://doi.org/10.1111/j.1365-313X.2011.04853.x

Q. Yin, G. Shen, S. Di, C. Fan, Z. Chang and Y. Pang, “Genome-wide identification and functional characterization of UDP-glucosyltransferase genes involved in flavonoid biosynthesis in Glycine max,” Plant Cell Physiol., vol. 58, no. 9, pp. 1558-1572, 2017, https://doi.org/10.1093/pcp/pcx081

T. D. Hoffmann, E. Kurze, J. Liao, T. Hoffmann, C. Song and W. Schwab, “Genome-wide identification of UDP-glycosyltransferases in the tea plant (Camellia sinensis) and their biochemical and physiological functions,” Front. Plant Sci., vol. 14, pp. 1191625, 2023, https://doi.org/10.3389/fpls.2023.1191625

S. Huang, R. Li, Z. Zhang, et al., “The genome of the cucumber, Cucumis sativus L.” Nat. Genet., vol. 41, pp. 1275–1281, 2009, https://doi.org/10.1038/ng.475

T. Tanaka, B. A. Antonio, S. Kikuchi, et al., “The rice annotation project database (RAP-DB): 2008 update,” Nucleic Acids Res., vol. 36, pp. D1028–D1033, 2008, https://doi.org/10.1093/nar/gkm978

H. Paterson, J. E. Bowers, R. Bruggmann, et al., “The Sorghum bicolor genome and the diversification of grasses,” Nature, vol. 457, pp. 551–556, 2009, https://doi.org/10.5167/uzh-16962

J. A. Banks, T. Nishiyama, M. Hasebe, et al., “The Selaginella genome identifies genetic changes associated with the evolution of vascular plants,” Science, vol. 332, pp. 960–963, 2011, https://doi.org/10.1126/science.1203810

Y. Li, P. Li, Y. Wang, et al., “Genome-wide identification and phylogenetic analysis of Family-1 UDP glycosyltransferases in maize (Zea mays),” Planta, vol. 239, pp. 1265–1279, 2014, https://doi.org/10.1007/s00425-014-2050-1

T. Vogt and P. Jones, “Glycosyltransferases in plant natural product synthesis: characterization of a supergene family,” Trends Plant Sci., vol. 5, no. 9, pp. 380–386, 2000, https://doi.org/10.1016/S1360-1385(00)01720-9

S. A. Osmani, S. Bak and B. L. Møller, “Substrate specificity of plant UDP-dependent glycosyltransferases predicted from crystal structures and homology modeling,” Phytochemistry, vol. 70, no. 3, pp. 325–347, 2009, https://doi.org/10.1016/j.phytochem.2008.12.009

J. Hughes and M. A. Hughes, “Multiple secondary plant product UDP-glucose glucosyltransferase genes expressed in cassava (Manihot esculenta Crantz) cotyledons,” DNA Sequence, vol. 5, pp. 41-49, 1994, https://doi.org/10.3109/10425179409039703

S. Paquette, B. L. Moller and S. Bak, “On the origin of family 1 plant glycosyltransferases,” Phytochemistry, vol. 62, pp. 399-413, 2003, https://doi.org/10.1016/S0031-9422(02)00558-7

D. Bowles, E. K. Lim, B. Poppenberger and F. E. Vaistij, “Glycosyltransferases of lipophilic small molecules,” Annu Rev Plant Biol., vol. 57, pp. 567–597, 2006, https://doi.org/10.1146/annurev.arplant.57.032905.105429

C. A. Williams and R. J. Grayer, “Anthocyanins and other flavonoids,” Nat. Prod. Rep., vol. 21, pp. 539-573, 2004, https://doi.org/10.1039/B311404J

Y. Mo, C. Nagel and L. P. Taylor, “Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen,” PNAS., vol. 89, no. 15, pp. 7213-7217, 1992, https://doi.org/10.1073/pnas.89.15.7213

W. A. Peer and A. S. Murphy, “Flavonoids and auxin transport: modulators or regulators?’ Trends Plant Sci., vol. 12, no. 12, pp. 556–563, 2007, https://doi.org/10.1016/j.tplants.2007.10.003

J. Mol, E. Grotewold and R. Koes, “How genes paint flowers and seeds,” Trends Plant Sci., vol. 3, no. 6, pp. 212–217, 1998, https://doi.org/10.1016/S1360-1385(98)01242-4

J. W. Fahey, T. Zalcmann and P. Talalay, “The chemical diversity and distribution of glucosinolates and isothiocyanates among plants,” Phytochemistry, vol. 56, no. 1, pp. 5–51, 2001, https://doi.org/10.1016/S0031-9422(00)00316-2

R. C. Prince and D. E. Gunson., ”Just plain vanilla?” Trends Biochem Sci., vol. 20, no. 1, pp. 28, 1994, https://doi.org/10.1016/0968-0004(94)90049-3

J. E. Poulton, “Localization and catabolism of cyanogenic glycosides,” Ciba Found Symp., vol. 140, pp. 67-91, 2007, https://doi.org/10.1002/9780470513712.ch6

E. Osbourn, “Saponins in cereals,” Phytochemistry, vol. 62, no. 1, pp. 1-4, 2003, https://doi.org/10.1016/S0031-9422(02)00393-X

P. Moehs, P. V. Allen, M. Friedman and W. R. Belknap, “Cloning and expression of solanidine UDP-glucose glucosyltransferase from potato,” The Plant J., vol. 11, no. 2, pp. 227-236, 1997, https://doi.org/10.1046/j.1365-313X.1997.11020227.x

H. Warzecha, P. Obitz and J. Stöckigt, ”Purification, partial amino acid sequence and structure of the product of raucaffricine-O-β-d-glucosidase from plant cell cultures of Rauwolfia serpentine,” Phytochemistry, vol. 50, no. 7, pp. 1099-1109, 1999, https://doi.org/10.1016/S0031-9422(98)00689-X

S. Rahimi, J. W. Kim, I. Mijakovic, K. Jung, G. Choi, S. C. Kim, Y. J. Kim, “Triterpenoid-biosynthetic UDP-glycosyltransferases from plants,” Biotechnology Advances, vol. 37, pp. 107394. https://doi.org/10.1016/j.biotechadv.2019.04.016

B. Hou, E. K. Lim, G. S. Higgins and D. J. Bowles, “N-glucosylation of cytokinins by glycosyltransferases of Arabidopsis thaliana,” J. Biol. Chem., vol. 279, pp. 47822-47832, 2004, https://doi.org/10.1074/jbc.M409569200

J. B. Szerszen, K. Szczyglowski and R. S. Bandurski, “iaglu, a gene from Zea mays involved in conjugation of growth hormone indole-3-acetic acid,” Science, vol. 265, no. 5179, pp. 1699-1701, 1994, https://doi.org/10.1126/science.8085154

R. G. Jackson, E. K. Lim, Y. Li, M. Kowalczyk, G. Sandberg, J. Hoggett, D. A. Ashford and D. J. Bowles, “Identification and biochemical characterization of an Arabidopsis indole-3-acetic acid glucosyltransferase,” J. Biol. Chem., vol. 276, pp. 4350-4356, 2001, https://doi.org/10.1074/jbc.M006185200

D. W. S. Mok and M. C. Mok, “Cytokinin metabolism and action,” Annu. Rev. Plant Physiol. Plant Mol. Biol., vol. 52, pp. 89-118, 2001, https://doi.org/10.1146/annurev.arplant.52.1.89

R. C. Martin, M. C. Mok and D. W. S. Mok, ”Isolation of a cytokinin gene, ZOG1, encoding zeatin O-glucosyltransferase from Phaseolus lunatus,” Plant Biology, vol. 96, pp. 284-289, 1999, https://doi.org/10.1073/pnas.96.1.284

D. W. S. Mok, R. C. Martin, X. Shan and M. C. Mok, “Genes encoding zeatin O-glycosyltransferases,” Plant Growth Regulation, vol. 32, no. 2-3, pp. 285-287, 2000, https://doi.org/10.1023/A:1010712102890

R. C. Martin, M. C. Mok, J. E. Habben and D. W. S. Mok, “A maize cytokinin gene encoding an O-glucosyltransferase specific to cis-zeatin,” PNAS, vol., 98, pp. 5922-5926, 2001, https://doi.org/10.1073/pnas.101128798

E. Nambara and A. Marion-Poll, “Abscisic acid biosynthesis and catabolism,“ Annu. Rev. Plant Biol., vol. 56, pp. 165-185, 2005, https://doi.org/10.1146/annurev.arplant.56.032604.144046

E. K. Lim, C. J. Doucet, B. Hou, R. G. Jackson, S. R. Abrams and D. J. Bowles, “Resolution of (+)-abscisic acid using an Arabidopsis glycosyltransferase,” Tetrahedron: Asymmetry, vol. 16, no. 1, pp. 143-147, 2005, https://doi.org/10.1016/j.tetasy.2004.11.062

D. M. Priest, R. G. Jackson, D. A. Ashford, S. R. Abrams and D. J. Bowles, “The use of abscisic acid analogues to analyse the substrate selectivity of UGT71B6, a UDP-glycosyltransferase of Arabidopsis thaliana,” FEBS Lett., vol. 579, no. 20, pp. 4454–4458, 2005, https://doi.org/10.1016/j.febslet.2005.06.084

S. Fujioka and T. Yokota, “Biosynthesis and metabolism of brassinosteroids,” Annu. Rev. Plant Biol., vol. 54, pp. 137-164, 2003, https://doi.org/10.1146/annurev.arplant.54.031902.134921

Bajguz, “Metabolism of brassinosteroids in plants,” Plant Physiol Biochem., vol. 45, no. 2, pp. 95-107, 2007, https://doi.org/10.1016/j.plaphy.2007.01.002

Poppenberger, S. Fujioka, K. Soeno, G. L. George, F. E. Vaistij, S. Hiranuma, H. Seto, S. Takatsuto, G. Adam, S. Yoshida and D. J. Bowles, “The UGT73C5 of Arabidopsis thaliana glucosylates brassinosteroids,” PNAS, vol. 102, no. 42, pp. 15253-15258, 2005, https://doi.org/10.1073/pnas.0504279102

Poppenberger, F. Berthiller, D. Lucyshyn, T. Sieberer, R. Schuhmacher, R. Krska, K. Kuchler, J. Glössl, C. Luschnig and G. Adam, “Detoxification of the Fusarium mycotoxin deoxynivalenol by a UDP-glucosyltransferase from Arabidopsis thaliana,” J. Biol. Chem., vol. 278, pp. 47905-47914, 2003, https://doi.org/10.1074/jbc.M307552200

Khorolragchaa, Y. J. Kim, S. Rahimi, J. Sukweenadhi, M. G. Jang and D. C. Yang, “Grouping and characterization of putative glycosyltransferase genes from Panax ginseng Meyer.,” Gene, vol. 536, no. 2014, pp. 186–192, 2014, https://doi.org/10.1016/j.gene.2013.07.077

Mazel and A. Levine, “Induction of glucosyltransferase transcription and activity during superoxide-dependent cell death in Arabidopsis plants,” Plant Physiol. Biochem., vol. 40, no. 2, pp. 133-140, 2002, https://doi.org/10.1016/S0981-9428(01)01351-1

K. Langlois-Meurinne, C. M. M. Gachon and P. Saindrenan, “Pathogen-responsive expression of glycosyltransferase genes UGT73B3 and UGT73B5 is necessary for resistance to Pseudomonas syringae pv tomato in Arabidopsis,” Plant Physiol., vol. 139, no. 4, pp. 1890-1901, 2005, https://doi.org/10.1104/pp.105.067223

J. Chong, R. Baltz, C. Schmitt, R. Beffa, B. Fritig and P. Saindrenan, “Downregulation of a pathogen-responsive tobacco udp-glc:phenylpropanoid glucosyltransferase reduces scopoletin glucoside accumulation, enhances oxidative stress, and weakens virus resistance,” The Plant Cell, vol. 14, no. 5, pp. 1093-1107, 2002, https://doi.org/10.1105/tpc.010436

Gachon, R. Baltz and P. Saindrenan, “Over-expression of a scopoletin glucosyltransferase in Nicotiana tabacum leads to precocious lesion formation during the hypersensitive response to tobacco mosaic virus but does not affect virus resistance,” Plant Mol. Biol., vol. 54, no. 1, pp. 137-146, 2004, https://doi.org/10.1023/B:PLAN.0000028775.58537.fe

J. T. Song, Y. J. Koo, H. S. Seo, M. C. Kim, Y. D. Choi and J. H. Kim, “Overexpression of AtSGT1, an Arabidopsis salicylic acid glucosyltransferase, leads to increased susceptibility to Pseudomonas syringae,” Phytochemistry, vol. 69, no. 5, pp. 1128–1134, 2008, https://doi.org/10.1016/j.phytochem.2007.12.010

E. K. Lim, C. J. Doucet, Y. Li, L. Elias, D. Worrall, S. P. Spencer, J. Ross and D. J. Bowles, “The activity of Arabidopsis glycosyltransferases toward salicylic acid, 4-hydroxybenzoic acid, and other benzoates,” J. Biol. Chem., vol. 277, pp. 586-592, 2002, https://doi.org/10.1074/jbc.M109287200

J. V. Dean and S. P. Delaney. Metabolism of salicylic acid in wild-type, UGT74F1 and UGT74F2 glucosyltransferase mutants of Arabidopsis thaliana. Physiol Plantarum, vol. 132, no. 4, pp. 417–425, 2008, https://doi.org/10.1111/j.1399-3054.2007.01041.x

Wasternack, “Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development,” Annals of Botany, vol. 100, no. 4, pp. 681-697, 2007, https://doi.org/10.1093/aob/mcm079

M. S. Song, Kim, D. G. and S. H. Lee, ”Isolation and characterization of a jasmonic acid carboxyl methyltransferase gene from hot pepper (Capsicum annuum L.),” J. Plant Biol., vol, 48, no. 3, pp. 292-297, 2005, https://doi.org/10.1007/BF03030525

G. Glauser, J. Boccard, S. Rudaz and J. L. Wolfender, “Mass spectrometry-based metabolomics oriented by correlation analysis for wound-induced molecule discovery: identification of a novel jasmonate glucoside,” Phytochem Anal., vol. 21, no. 1, pp. 95–101, 2010, https://doi.org/10.1002/pca.1155

Abe, M. Rohmer and G. D. Prestwich. “Enzymatic cyclization of squalene and oxidosqualene to sterols and triterpenes,” Chem. Rev., vol. 93, no. 6, pp. 2189–2206, 1993, https://doi.org/10.1021/cr00022a009

Ohyama, M. Suzuki, J. Kikuchi, K. Saito and T. Muranaka, “Dual biosynthetic pathways to phytosterol via cycloartenol and lanosterol in Arabidopsis.” PNAS, vol. 106, no. 3, pp. 725-730, 2009, https://doi.org/10.1073/pnas.0807675106

L. Cantarel, P. M. Coutinho, C. Rancurel, T. Xu, R., G. C. Fazio and S. P. T. Matsuda, “On the origins of triterpenoid skeletal diversity,” Phytochemistry, vol. 65, pp. 261–291, 2004, https://doi.org/10.1016/j.phytochem.2003.11.014

R. Thoma, T. Schulz-Gasch, B. D’Arcy, J. Benz, J. Aebi, H. Dehmlow, M. Hennig, M. Stihle and A. Ruf, “Insight into steroid scaffold formation from the structure of human oxidosqualene cyclase,” Nature, vol. 432, pp. 118-122, 2004, https://doi.org/10.1038/nature02993

R. A. Kahn and F. Durst, “Function and evolution of plant cytochrome P450,” Recent Adv. Phytochemistry, vol. 34, pp. 151–189, 2000.

C. Hansen, D. R. Nelson, B. L. Møller and D. Werck-Reichhart, “Plant cytochrome P450 plasticity and evolution,” Molecular Plant, vol. 14, no. 8, pp. 1244-1265, 2021, https://doi.org/10.1016/j.molp.2021.06.028

S. Sawai and K. Saito, “Triterpenoid biosynthesis and engineering in plants,” Front Plant Sci., vol. 2, pp. 25, 2011, https://doi.org/10.3389/fpls.2011.00025

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2023-12-31

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K. Altanzul, “Plant secondary metabolite and glycosyltransferases”, Proc. Inst. Biol., vol. 39, no. 1, pp. 106–123, Dec. 2023.

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