Two UGT84A Family Glycosyltransferases Regulate Phenol, Flavonoid, and Tannin Metabolism in Juglans regia (English Walnut)
We showed previously that gallic acid is produced in walnut from 3-dehydroshikimate by a shikimate dehydrogenase (JrSkDH). This study focuses on the next step in the hydrolysable tannin pathway, the formation of 1-O-galloyl-β-D-glucose from the phenolic gallic acid and UDP glucose by a glycosyltrans...
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Frontiers Media S.A.
2021-02-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2021.626483/full |
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| author | Houston J. Saxe Takanori Horibe Bipin Balan Timothy S. Butterfield Noah G. Feinberg Christopher M. Zabaneh Aaron E. Jacobson Abhaya M. Dandekar |
| author_facet | Houston J. Saxe Takanori Horibe Bipin Balan Timothy S. Butterfield Noah G. Feinberg Christopher M. Zabaneh Aaron E. Jacobson Abhaya M. Dandekar |
| author_sort | Houston J. Saxe |
| collection | DOAJ |
| description | We showed previously that gallic acid is produced in walnut from 3-dehydroshikimate by a shikimate dehydrogenase (JrSkDH). This study focuses on the next step in the hydrolysable tannin pathway, the formation of 1-O-galloyl-β-D-glucose from the phenolic gallic acid and UDP glucose by a glycosyltransferase. JrGGT1 (UGT84A73) and JrGGT2 (UGT84A74) are predicted to be two such glycosyltransferases, which we expressed in tobacco plants. GC-MS analysis of the transgenic tobacco revealed moderate, yet significant alterations in plant secondary metabolism, such as depleted phenolic acids, including gallic acid. We postulate that these effects are due to JrGGT1 and JrGGT2 activity, as JrGGT orthologs glycosylate these phenolic compounds in vitro. Moreover, JrGGT expression in tobacco caused upregulation of shikimic acid pathway metabolites and differing responses in phenylpropanoids, such as phenolic acids and flavonoids. In transcriptome analysis of walnut pellicle tissues, both JrGGTs showed substantial and significant expression correlations with the gallic acid-producing JrSkDHs and were highly coexpressed with the genetic circuits constituting the shikimic acid and phenylpropanoid biosynthetic pathways. Verification of JrGGT gene expression by transcriptome analysis of 20 walnut tissues revealed striking similarities with that of the pellicle data, with the greatest expression in roots, wood, buds, and leaves of Juglans regia cv. Chandler: tissues that typically accumulate hydrolysable tannins. Like the transgenic tobacco, pellicle metabolomic analyses revealed that many phenylpropanoids correlated negatively with JrGGT expression, while shikimic acid pathway metabolites correlated positively with JrGGT expression. This research supports the hypothesis that JrGGT1 and JrGGT2 play non-trivial roles in metabolism of phenolic acids, flavonoids, and ostensibly, tannins. |
| first_indexed | 2024-12-14T11:46:41Z |
| format | Article |
| id | doaj.art-0092b98f8913485eb3e3999e32187f45 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-14T11:46:41Z |
| publishDate | 2021-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-0092b98f8913485eb3e3999e32187f452022-12-21T23:02:32ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-02-011210.3389/fpls.2021.626483626483Two UGT84A Family Glycosyltransferases Regulate Phenol, Flavonoid, and Tannin Metabolism in Juglans regia (English Walnut)Houston J. Saxe0Takanori Horibe1Bipin Balan2Timothy S. Butterfield3Noah G. Feinberg4Christopher M. Zabaneh5Aaron E. Jacobson6Abhaya M. Dandekar7Department of Plant Sciences, University of California, Davis, Davis, CA, United StatesCollege of Bioscience and Biotechnology, Chubu University, Kasugai, JapanDepartment of Plant Sciences, University of California, Davis, Davis, CA, United StatesARS Crops Pathology and Genetics Unit, United States Department of Agriculture, Davis, CA, United StatesDepartment of Plant Sciences, University of California, Davis, Davis, CA, United StatesDepartment of Plant Sciences, University of California, Davis, Davis, CA, United StatesDepartment of Plant Sciences, University of California, Davis, Davis, CA, United StatesDepartment of Plant Sciences, University of California, Davis, Davis, CA, United StatesWe showed previously that gallic acid is produced in walnut from 3-dehydroshikimate by a shikimate dehydrogenase (JrSkDH). This study focuses on the next step in the hydrolysable tannin pathway, the formation of 1-O-galloyl-β-D-glucose from the phenolic gallic acid and UDP glucose by a glycosyltransferase. JrGGT1 (UGT84A73) and JrGGT2 (UGT84A74) are predicted to be two such glycosyltransferases, which we expressed in tobacco plants. GC-MS analysis of the transgenic tobacco revealed moderate, yet significant alterations in plant secondary metabolism, such as depleted phenolic acids, including gallic acid. We postulate that these effects are due to JrGGT1 and JrGGT2 activity, as JrGGT orthologs glycosylate these phenolic compounds in vitro. Moreover, JrGGT expression in tobacco caused upregulation of shikimic acid pathway metabolites and differing responses in phenylpropanoids, such as phenolic acids and flavonoids. In transcriptome analysis of walnut pellicle tissues, both JrGGTs showed substantial and significant expression correlations with the gallic acid-producing JrSkDHs and were highly coexpressed with the genetic circuits constituting the shikimic acid and phenylpropanoid biosynthetic pathways. Verification of JrGGT gene expression by transcriptome analysis of 20 walnut tissues revealed striking similarities with that of the pellicle data, with the greatest expression in roots, wood, buds, and leaves of Juglans regia cv. Chandler: tissues that typically accumulate hydrolysable tannins. Like the transgenic tobacco, pellicle metabolomic analyses revealed that many phenylpropanoids correlated negatively with JrGGT expression, while shikimic acid pathway metabolites correlated positively with JrGGT expression. This research supports the hypothesis that JrGGT1 and JrGGT2 play non-trivial roles in metabolism of phenolic acids, flavonoids, and ostensibly, tannins.https://www.frontiersin.org/articles/10.3389/fpls.2021.626483/fullglucosyltransferasehydrolysable tanninUGT84Agallic acidwalnutphenol metabolism |
| spellingShingle | Houston J. Saxe Takanori Horibe Bipin Balan Timothy S. Butterfield Noah G. Feinberg Christopher M. Zabaneh Aaron E. Jacobson Abhaya M. Dandekar Two UGT84A Family Glycosyltransferases Regulate Phenol, Flavonoid, and Tannin Metabolism in Juglans regia (English Walnut) Frontiers in Plant Science glucosyltransferase hydrolysable tannin UGT84A gallic acid walnut phenol metabolism |
| title | Two UGT84A Family Glycosyltransferases Regulate Phenol, Flavonoid, and Tannin Metabolism in Juglans regia (English Walnut) |
| title_full | Two UGT84A Family Glycosyltransferases Regulate Phenol, Flavonoid, and Tannin Metabolism in Juglans regia (English Walnut) |
| title_fullStr | Two UGT84A Family Glycosyltransferases Regulate Phenol, Flavonoid, and Tannin Metabolism in Juglans regia (English Walnut) |
| title_full_unstemmed | Two UGT84A Family Glycosyltransferases Regulate Phenol, Flavonoid, and Tannin Metabolism in Juglans regia (English Walnut) |
| title_short | Two UGT84A Family Glycosyltransferases Regulate Phenol, Flavonoid, and Tannin Metabolism in Juglans regia (English Walnut) |
| title_sort | two ugt84a family glycosyltransferases regulate phenol flavonoid and tannin metabolism in juglans regia english walnut |
| topic | glucosyltransferase hydrolysable tannin UGT84A gallic acid walnut phenol metabolism |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2021.626483/full |
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