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.

中文翻译：

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控制草莓植株中可水解单宁合成的“合金化-脱合金化循环”中的关键基因


草莓果实以其出色的味道和潜在的健康益处而闻名，因其丰富的可水解单宁 （HT） 含量而受到特别重视。这些化合物在调节生长和发育中起关键作用。然而，植物中 HT 合成的分子机制仍然难以阐明。本研究基于HTs转录组与代谢组的相关性分析，筛选出了葡糖基转移酶（UGT84A22）、丝氨酸羧肽酶样酰基转移酶（SCPL-ATs）和羧酸酯酶（CXEs）。此外，体外酶测定证实 FaSCPL3-1 作为可水解单宁合酶 （HTS） 发挥作用，催化葡萄糖连续酰化形成简单的没食子单宁 （GT）。此外，FaCXE1/FaCXE3/FaCXE7 催化简单 GTs 和鞣花单宁 （ETs） 的脱合金化，FaUGT84A22 催化没食子酸 （GA） 的糖基化产生没食子醇供体 1-O-β-葡萄糖苷 （βG）。此外，在 FvSCPL3–1-RNAi 转基因草莓植株中，简单 GT 和一些 ET 化合物的含量降低，而在 FaCXE7 过表达草莓植株中，这些化合物含量增加。这些酶构成了没食子醇衍生物的生物合成途径，称为“合金化-脱合金化循环”（G-DG 循环）。值得注意的是，FaCXE7 在草莓植株中的过表达不仅促进了 HT 合成，而且还通过减少木质素的生物合成来干扰植物的生长发育。这些发现为植物中 HT 积累的机制提供了新的见解，有助于提高浆果品质和增强植物抗性。