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

Author:

Yang Qinsong12ORCID,Li Jinjin12,Wang Yan3ORCID,Wang Zefu4ORCID,Pei Ziqi12,Street Nathaniel R.56ORCID,Bhalerao Rishikesh P.7ORCID,Yu Zhaowei12,Gao Yuhao8,Ni Junbei8,Jiao Yang8,Sun Minghui12,Yang Xiong12,Chen Yixin12,Liu Puyuan12,Wang Jiaxi12,Liu Yong12,Li Guolei12ORCID

Affiliation:

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

Abstract

Summary 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.

Funder

China Postdoctoral Science Foundation

National Key Research and Development Program of China

National Natural Science Foundation of China

Publisher

Wiley

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