Genomic basis of the distinct biosynthesis of β-glucogallin, a biochemical marker for hydrolyzable tannin production, in three oak species

Qinsong Yang; Jinjin Li; Yan Wang; Zefu Wang; Ziqi Pei; Nathaniel R Street; Rishikesh P Bhalerao; Zhaowei Yu; Yuhao Gao; Junbei Ni; Yang Jiao; Minghui Sun; Xiong Yang; Yixin Chen; Puyuan Liu; Jiaxi Wang; Yong Liu; Guolei Li

doi:10.1111/nph.19711

Genomic basis of the distinct biosynthesis of β-glucogallin, a biochemical marker for hydrolyzable tannin production, in three oak species

New Phytol. 2024 Mar 21. doi: 10.1111/nph.19711. Online ahead of print.

Authors

Qinsong Yang^#^{1

2}, Jinjin Li^#^{1

2}, Yan Wang^#³, Zefu Wang⁴, Ziqi Pei^{1

2}, Nathaniel R Street^{5

6}, Rishikesh P Bhalerao⁷, Zhaowei Yu^{1

2}, Yuhao Gao⁸, Junbei Ni⁸, Yang Jiao⁸, Minghui Sun^{1

2}, Xiong Yang^{1

2}, Yixin Chen^{1

2}, Puyuan Liu^{1

2}, Jiaxi Wang^{1

2}, Yong Liu^{1

2}, Guolei Li^{1

2}

Affiliations

¹ State Key Laboratory of Efficient Production of Forest Resources, Beijing Forestry University, Beijing, 100083, China.
² Research Center of Deciduous Oaks, Beijing Forestry University, Beijing, 100083, China.
³ College of Horticulture, China Agricultural University, Beijing, 100193, China.
⁴ Co-Innovation Center for Sustainable Forestry in Southern China, College of Ecology and Environment, Nanjing Forestry University, Nanjing, 210037, China.
⁵ Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, Umeå, 90754, Sweden.
⁶ SciLifeLab, Umeå University, Umeå, 90754, Sweden.
⁷ Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 90187, Umeå, Sweden.
⁸ College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, 310058, China.

^# Contributed equally.

PMID: 38515244
DOI: 10.1111/nph.19711

Abstract

Hydrolyzable tannins (HTs), predominant polyphenols in oaks, are widely used in grape wine aging, feed additives, and human healthcare. However, the limited availability of a high-quality reference genome of oaks greatly hampered the recognition of the mechanism of HT biosynthesis. Here, high-quality reference genomes of three Asian oak species (Quercus variabilis, Quercus aliena, and Quercus dentata) that have different HT contents were generated. Multi-omics studies were carried out to identify key genes regulating HT biosynthesis. In vitro enzyme activity assay was also conducted. Dual-luciferase and yeast one-hybrid assays were used to reveal the transcriptional regulation. Our results revealed that β-glucogallin was a biochemical marker for HT production in the cupules of the three Asian oaks. UGT84A13 was confirmed as the key enzyme for β-glucogallin biosynthesis. The differential expression of UGT84A13, rather than enzyme activity, was the main reason for different β-glucogallin and HT accumulation. Notably, sequence variations in UGT84A13 promoters led to different trans-activating activities of WRKY32/59, explaining the different expression patterns of UGT84A13 among the three species. Our findings provide three high-quality new reference genomes for oak trees and give new insights into different transcriptional regulation for understanding β-glucogallin and HT biosynthesis in closely related oak species.

Keywords: UGT84A13; hydrolyzable tannin; oak; whole‐genome sequencing; β‐glucogallin.

Abstract

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