Key genes in a “Galloylation-Degalloylation cycle” controlling the synthesis of hydrolyzable tannins in strawberry plants

Abstract

Strawberry fruits, known for their excellent taste and potential health benefits, are particularly valued for their rich content of hydrolyzable tannins (HTs). These compounds play key roles in regulating growth and development. However, the molecular mechanisms underlying HT synthesis in plants remains poorly elucidated. In this study, based on a correlation analysis between the transcriptome and metabolome of HTs, galloyl glucosyltransferase (UGT84A22), serine carboxypeptidase-like acyltransferases (SCPL-ATs), and carboxylesterases (CXEs) were screened. Furthermore, in vitro enzymatic assays confirmed that FaSCPL3-1 acted as a hydrolyzable tannins synthase (HTS), catalyzing the continuous galloylation of glucose to form simple gallotannins (GTs). Additionally, FaCXE1/FaCXE3/FaCXE7 catalyzed the degalloylation of simple GTs and ellagitannins (ETs), and FaUGT84A22 catalyzed the glycosylation of gallic acid (GA) to produce 1-O-β-glucogallin (βG), a galloyl donor. Moreover, in FvSCPL3-1-RNAi transgenic strawberry plants, the contents of simple GT and some ET compounds were reduced, whereas, in FaCXE7 overexpressing strawberry plants, these compounds were increased. These enzymes constituted a biosynthetic pathway of galloyl derivatives, termed the “galloylation-degalloylation cycle” (G-DG cycle). Notably, the overexpression of FaCXE7 in strawberry plants not only promoted HT synthesis but also interfered with plant growth and development by reducing lignin biosynthesis. These findings offer new insights into the mechanisms of HT accumulation in plants, contributing to improving the quality of berry fruits quality and enhancing plant resistance.

Acknowledgements

This work was funded by the National Natural Science Foundation of China (32072621), the Joint Funds of the National Natural Science Foundation of China (U21A20232), the National Key Research and Development Program of China (2022YFF1003103) and the National Natural Science Foundation of China (32000366).

Author contributions

L.G. and T.X. conceived and designed the study. L.G. and L.Z. drafted the manuscript. L.Z., R.L. and M.W. performed the experiments. Q.Z and N.W. contributed materials/analysis tools. Y.C. and Y.H. analyzed the data. Y.L. and X.J. modified the language of the manuscript. All authors read and approved the final version of the manuscript.

Data availability

The raw sequencing data from this study have been deposited in the Genome Sequence Archive in BIG Data Center (https://bigd.big.ac.cn/), Beijing Institute of Genomics (BIG), Chinese Academy of Sciences, under the accession number CRA017076.

Conflict of interest statement

The authors declare no conflicts of interest.

Supplementary Data

Supplementary data is available at Horticulture Research online.

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