Dual activity of anthocyanidin reductase supports the dominant plant proanthocyanidin extension unit pathway
Abstract
Proanthocyanidins (PAs) are plant natural products important for agriculture and human health. They are polymers of flavan-3-ol subunits, commonly (-)-epicatechin and/or (+)-catechin, but the source of the in planta extension unit that comprises the bulk of the polymer remains unclear, as does how PA composition is determined in different plant species. Anthocyanidin reductase (ANR) can generate 2,3-cis-epicatechin as a PA starter unit from cyanidin, which itself arises from 2,3-trans-leucocyanidin, but ANR proteins from different species produce mixtures of flavan-3-ols with different stereochemistries in vitro. Genetic and biochemical analyses here show that ANR has dual activity and is involved not only in the production of (-)-epicatechin starter units but also in the formation of 2,3-cis-leucocyanidin to serve as (-)-epicatechin extension units. Differences in the product specificities of ANRs account for the presence/absence of PA polymerization and the compositions of PAs across plant species.
- Authors:
-
[1];
[1];
[1];
[1];
[1]
- Univ. of North Texas, Denton, TX (United States). Dept. of Biological Sciences. BioDiscovery Inst.
- Publication Date:
- Research Org.:
- Univ. of Georgia, Athens, GA (United States); Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; USDOE
- OSTI Identifier:
- 1816719
- Alternate Identifier(s):
- OSTI ID: 1963708
- Grant/Contract Number:
- SC0015662
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Science Advances
- Additional Journal Information:
- Journal Volume: 7; Journal Issue: 20; Journal ID: ISSN 2375-2548
- Publisher:
- AAAS
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Jun, Ji Hyung, Lu, Nan, Docampo-Palacios, Maite, Wang, Xiaoqiang, and Dixon, Richard A. Dual activity of anthocyanidin reductase supports the dominant plant proanthocyanidin extension unit pathway. United States: N. p., 2021.
Web. doi:10.1126/sciadv.abg4682.
Jun, Ji Hyung, Lu, Nan, Docampo-Palacios, Maite, Wang, Xiaoqiang, & Dixon, Richard A. Dual activity of anthocyanidin reductase supports the dominant plant proanthocyanidin extension unit pathway. United States. https://doi.org/10.1126/sciadv.abg4682
Jun, Ji Hyung, Lu, Nan, Docampo-Palacios, Maite, Wang, Xiaoqiang, and Dixon, Richard A. Sat .
"Dual activity of anthocyanidin reductase supports the dominant plant proanthocyanidin extension unit pathway". United States. https://doi.org/10.1126/sciadv.abg4682. https://www.osti.gov/servlets/purl/1816719.
@article{osti_1816719,
title = {Dual activity of anthocyanidin reductase supports the dominant plant proanthocyanidin extension unit pathway},
author = {Jun, Ji Hyung and Lu, Nan and Docampo-Palacios, Maite and Wang, Xiaoqiang and Dixon, Richard A.},
abstractNote = {Proanthocyanidins (PAs) are plant natural products important for agriculture and human health. They are polymers of flavan-3-ol subunits, commonly (-)-epicatechin and/or (+)-catechin, but the source of the in planta extension unit that comprises the bulk of the polymer remains unclear, as does how PA composition is determined in different plant species. Anthocyanidin reductase (ANR) can generate 2,3-cis-epicatechin as a PA starter unit from cyanidin, which itself arises from 2,3-trans-leucocyanidin, but ANR proteins from different species produce mixtures of flavan-3-ols with different stereochemistries in vitro. Genetic and biochemical analyses here show that ANR has dual activity and is involved not only in the production of (-)-epicatechin starter units but also in the formation of 2,3-cis-leucocyanidin to serve as (-)-epicatechin extension units. Differences in the product specificities of ANRs account for the presence/absence of PA polymerization and the compositions of PAs across plant species.},
doi = {10.1126/sciadv.abg4682},
journal = {Science Advances},
number = 20,
volume = 7,
place = {United States},
year = {Sat May 01 00:00:00 EDT 2021},
month = {Sat May 01 00:00:00 EDT 2021}
}
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Works referenced in this record:
Genetics and Biochemistry of seed Flavonoids
journal, June 2006
- Lepiniec, Loïc; Debeaujon, Isabelle; Routaboul, Jean-Marc
- Annual Review of Plant Biology, Vol. 57, Issue 1
Analysis of Proanthocyanidin Cleavage Products Following Acid-Catalysis in the Presence of Excess Phloroglucinol
journal, March 2001
- Kennedy, James A.; Jones, Graham P.
- Journal of Agricultural and Food Chemistry, Vol. 49, Issue 4
Structural evidence for the inhibition of grape dihydroflavonol 4-reductase by flavonols
journal, July 2008
- Trabelsi, Nadia; Petit, Pierre; Manigand, Claude
- Acta Crystallographica Section D Biological Crystallography, Vol. 64, Issue 8
The C-4 stereochemistry of leucocyanidin substrates for anthocyanidin synthase affects product selectivity
journal, November 2003
- Turnbull, Jonathan J.; Nagle, Michael J.; Seibel, Jürgen F.
- Bioorganic & Medicinal Chemistry Letters, Vol. 13, Issue 21
Proanthocyanidins - a final frontier in flavonoid research?: Tansley Review
journal, November 2004
- Dixon, Richard A.; Xie, De-Yu; Sharma, Shashi B.
- New Phytologist, Vol. 165, Issue 1
Enzymic and Nonenzymic Reduction of (+)-Dihydroquercetin to Its 3,4,-Diol
journal, September 1982
- Stafford, Helen A.; Lester, Hope H.
- Plant Physiology, Vol. 70, Issue 3
AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility
journal, December 2009
- Morris, Garrett M.; Huey, Ruth; Lindstrom, William
- Journal of Computational Chemistry, Vol. 30, Issue 16
A review on astringency and bitterness perception of tannins in wine
journal, November 2014
- Ma, Wen; Guo, Anque; Zhang, Yulin
- Trends in Food Science & Technology, Vol. 40, Issue 1
Procyanidin metabolism—A hypothesis
journal, January 1977
- Haslam, Edwin; Opie, Clive T.; Porter, Lawrence J.
- Phytochemistry, Vol. 16, Issue 1
Reciprocal regulation ofArabidopsis UGT78D2 and BANYULS is critical for regulation of the metabolic flux of anthocyanidins to condensed tannins in developing seed coats
journal, December 2005
- Lee, Yeon; Yoon, Hye Ryon; Paik, Yong Sook
- Journal of Plant Biology, Vol. 48, Issue 4
Effect of feed additives on in vitro and in vivo rumen characteristics and frothy bloat dynamics in steers grazing wheat pasture
journal, December 2005
- Min, Byeng R.; Pinchak, William E.; Fulford, Jerry D.
- Animal Feed Science and Technology, Vol. 123-124
Coot model-building tools for molecular graphics
journal, November 2004
- Emsley, Paul; Cowtan, Kevin
- Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
Dissecting genetic architecture of grape proanthocyanidin composition through quantitative trait locus mapping
journal, February 2012
- Huang, Yung-Fen; Doligez, Agnès; Fournier-Level, Alexandre
- BMC Plant Biology, Vol. 12, Issue 1
Structure and epimerase activity of anthocyanidin reductase from Vitis vinifera
journal, August 2009
- Gargouri, Mahmoud; Manigand, Claude; Maugé, Chloé
- Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 9
Biosynthesis of flavan 3-ols by leucoanthocyanidin 4-reductases and anthocyanidin reductases in leaves of grape (Vitis vinifera L.), apple (Malus x domestica Borkh.) and other crops
journal, May 2006
- Pfeiffer, Judith; Kühnel, Christiane; Brandt, Jeannette
- Plant Physiology and Biochemistry, Vol. 44, Issue 5-6
Functional Characterization of Proanthocyanidin Pathway Enzymes from Tea and Their Application for Metabolic Engineering
journal, January 2013
- Pang, Yongzhen; Abeysinghe, I. Sarath B.; He, Ji
- Plant Physiology, Vol. 161, Issue 3
Biosynthesis of plant proanthocyanidins
journal, January 1974
- Jacques, David; Haslam, Edwin
- Journal of the Chemical Society, Chemical Communications, Issue 6
Biogenetically patterned synthesis of procyanidins
journal, January 1974
- Haslam, Edwin
- Journal of the Chemical Society, Chemical Communications, Issue 15
Accumulation of Catechin and Proanthocyanidins in Black Poplar Stems After Infection by Plectosphaerella populi: Hormonal Regulation, Biosynthesis and Antifungal Activity
journal, November 2019
- Ullah, Chhana; Unsicker, Sybille B.; Reichelt, Michael
- Frontiers in Plant Science, Vol. 10
Proanthocyanidin Biosynthesis—a Matter of Protection
journal, August 2020
- Dixon, Richard A.; Sarnala, Sai
- Plant Physiology, Vol. 184, Issue 2
Synthesis of 3,4-cis-[3H]Leucocyanidin and Enzymatic Reduction to Catechin
journal, March 1993
- Tanner, G. J.; Kristiansen, K. N.
- Analytical Biochemistry, Vol. 209, Issue 2
A transcript profiling approach reveals an epicatechin-specific glucosyltransferase expressed in the seed coat of Medicago truncatula
journal, September 2008
- Pang, Y.; Peel, G. J.; Sharma, S. B.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 37
Proanthocyanidins in Health Care: Current and New Trends
journal, May 2004
- Cos, P.; Bruyne, T.; Hermans, N.
- Current Medicinal Chemistry, Vol. 11, Issue 10
Free radicals and grape seed proanthocyanidin extract: importance in human health and disease prevention
journal, August 2000
- Bagchi, Debasis; Bagchi, Manashi; Stohs, Sidney J.
- Toxicology, Vol. 148, Issue 2-3
Anthocyanidin reductases from Medicago truncatula and Arabidopsis thaliana
journal, February 2004
- Xie, De-Yu; Sharma, Shashi B.; Dixon, Richard A.
- Archives of Biochemistry and Biophysics, Vol. 422, Issue 1
Functional demonstration of plant flavonoid carbocations proposed to be involved in the biosynthesis of proanthocyanidins
journal, October 2019
- Wang, Peiqiang; Liu, Yajun; Zhang, Lingjie
- The Plant Journal, Vol. 101, Issue 1
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998
- Clough, Steven J.; Bent, Andrew F.
- The Plant Journal, Vol. 16, Issue 6, p. 735-743
Occurrence and biological significance of proanthocyanidins in the American diet
journal, September 2005
- Prior, Ronald L.; Gu, Liwei
- Phytochemistry, Vol. 66, Issue 18
The chemistry of tea flavonoids
journal, December 1997
- Balentine, Douglas A.; Wiseman, Sheila A.; Bouwens, Liesbeth C. M.
- Critical Reviews in Food Science and Nutrition, Vol. 37, Issue 8
Heterologous expression of dihydroflavonol 4-reductases from various plants
journal, October 2002
- Martens, Stefan; Teeri, Teemu; Forkmann, Gert
- FEBS Letters, Vol. 531, Issue 3
Age-Related Shifts in Leaf Chemistry of Clonal Aspen (Populus tremuloides)
journal, May 2006
- Donaldson, Jack R.; Stevens, Michael T.; Barnhill, Heidi R.
- Journal of Chemical Ecology, Vol. 32, Issue 7
Evidence for oxidation at C-3 of the flavonoid C-ring during anthocyanin biosynthesis
journal, January 2001
- Welford, Richard W. D.; Turnbull, Jonathan J.; Claridge, Timothy D. W.
- Chemical Communications, Issue 18
Structure of Condensed Tannins
journal, October 1965
- Creasy, L. L.; Swain, T.
- Nature, Vol. 208, Issue 5006
Mechanisms of Carbon Sequestration in Highly Organic Ecosystems – Importance of Chemical Ecology
journal, April 2020
- Adamczyk, Bartosz; Heinonsalo, Jussi; Simon, Judy
- ChemistryOpen, Vol. 9, Issue 4
BANYULS, a novel negative regulator of flavonoid biosynthesis in the Arabidopsis seed coat
journal, February 1997
- Albert, Sylvie; Delseny, Michel; Devic, Martine
- The Plant Journal, Vol. 11, Issue 2
Proanthocyanidin Biosynthesis in Plants
journal, August 2003
- Tanner, Gregory J.; Francki, Kathy T.; Abrahams, Sharon
- Journal of Biological Chemistry, Vol. 278, Issue 34
The first near-complete assembly of the hexaploid bread wheat genome, Triticum aestivum
journal, October 2017
- Zimin, Aleksey V.; Puiu, Daniela; Hall, Richard
- GigaScience, Vol. 6, Issue 11
The B73 Maize Genome: Complexity, Diversity, and Dynamics
journal, November 2009
- Schnable, P. S.; Ware, D.; Fulton, R. S.
- Science, Vol. 326, Issue 5956, p. 1112-1115
Production of 3,4- cis - and 3,4- trans -Leucocyanidin and Their Distinct MS/MS Fragmentation Patterns
journal, December 2017
- Zhang, Jia-Rong; Tolchard, James; Bathany, Katell
- Journal of Agricultural and Food Chemistry, Vol. 66, Issue 1
Metabolic Characterization of the Anthocyanidin Reductase Pathway Involved in the Biosynthesis of Flavan-3-ols in Elite Shuchazao Tea (Camellia sinensis) Cultivar in the Field
journal, December 2017
- Zhao, Lei; Jiang, Xiao-Lan; Qian, Yu-Mei
- Molecules, Vol. 22, Issue 12
A role for leucoanthocyanidin reductase in the extension of proanthocyanidins
journal, November 2016
- Liu, Chenggang; Wang, Xiaoqiang; Shulaev, Vladimir
- Nature Plants, Vol. 2, Issue 12
Role of Anthocyanidin Reductase, Encoded by BANYULS in Plant Flavonoid Biosynthesis
journal, January 2003
- Xie, D. -Y.
- Science, Vol. 299, Issue 5605
Enzymic regulation of procyanidin biosynthesis; lack of a flav-3-en-3-ol intermediate
journal, January 1983
- Stafford, Helen A.
- Phytochemistry, Vol. 22, Issue 12
Proanthocyanidin subunit composition determined by functionally diverged dioxygenases
journal, November 2018
- Jun, Ji Hyung; Xiao, Xirong; Rao, Xiaolan
- Nature Plants, Vol. 4, Issue 12
Analysis of the Oxidative Degradation of Proanthocyanidins under Basic Conditions
journal, March 2004
- Jorgensen, Emily M.; Marin, Anna B.; Kennedy, James A.
- Journal of Agricultural and Food Chemistry, Vol. 52, Issue 8
Condensed tannins: quinone methide intermediates in procyanidin synthesis
journal, January 1983
- Hemingway, Richard W.; Foo, L. Yeap
- Journal of the Chemical Society, Chemical Communications, Issue 18