Evolution and Domestication of a Novel Biosynthetic Gene Cluster Contributing to the Flavonoid Metabolism and High‐Altitude Adaptability of Plants in the <i>Fagopyrum</i> Genus

The diversity of secondary metabolites is an important means for plants to cope with the complex and ever-changing terrestrial environment. Plant biosynthetic gene clusters (BGCs) are crucial for the biosynthesis of secondary metabolites. The domestication and evolution of BGCs and how they affect plant secondary metabolites biosynthesis and environmental adaptation are still not fully understood. Buckwheat exhibits strong resistance and abundant secondary metabolites, especially flavonoids, allowing it to thrive in harsh environments. A non-canonical BGC named UFGT3 cluster is identified, which comprises a phosphorylase kinase (PAK), two transcription factors (MADS1/2), and a glycosyltransferase (UFGT3), forming a complete molecular regulatory module involved in flavonoid biosynthesis. This cluster is selected during Tartary buckwheat domestication and is widely present in species of the Fagopyrum genus. In wild relatives of cultivated buckwheat, a gene encoding anthocyanin glycosyltransferase (AGT), which glycosylates pelargonidin into pelargonidin-3-O-glucoside, is found inserted into this cluster. The pelargonidin-3-O-glucoside can help plants resist UV stress, endowing wild relatives with stronger high-altitude adaptability. This study provides a new research paradigm for the evolutionary dynamics of plant BGCs, and offers new perspectives for exploring the mechanism of plant ecological adaptability driven by environmental stress through the synthesis of secondary metabolites.

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Publication Details

Journal
Advanced Science
Published
2024-09-23
DOI
https://doi.org/10.1002/advs.202403603
Citations
25
Primary Topic
Seed and Plant Biochemistry
Type
article
Field-Weighted Citation Impact
8.71

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article

Evolution and Domestication of a Novel Biosynthetic Gene Cluster Contributing to the Flavonoid Metabolism and High‐Altitude Adaptability of Plants in the Fagopyrum Genus

Meiliang Zhou, Yaliang Shi, Milen I. Georgiev, Dili Lai et al.
25 citations
Advanced Science
Seed and Plant Biochemistry
8.71
article

Evolution and Domestication of a Novel Biosynthetic Gene Cluster Contributing to the Flavonoid Metabolism and High‐Altitude Adaptability of Plants in the Fagopyrum Genus

Meiliang Zhou, Yaliang Shi, Milen I. Georgiev, Dili Lai, Muriel Quinet, Xu Huang, Hui Zhao, Sun–Hee Woo, Yuqi He, Alisdair Robert Fernie, Xiangru Wang, Hao Lin, Wei Li, Kaixuan Zhang, Zhimin Yang, Xu Liu, Yawen Xiao, Yinan Ouyang
article en
25 citations

Abstract

The diversity of secondary metabolites is an important means for plants to cope with the complex and ever-changing terrestrial environment. Plant biosynthetic gene clusters (BGCs) are crucial for the biosynthesis of secondary metabolites. The domestication and evolution of BGCs and how they affect plant secondary metabolites biosynthesis and environmental adaptation are still not fully understood. Buckwheat exhibits strong resistance and abundant secondary metabolites, especially flavonoids, allowing it to thrive in harsh environments. A non-canonical BGC named UFGT3 cluster is identified, which comprises a phosphorylase kinase (PAK), two transcription factors (MADS1/2), and a glycosyltransferase (UFGT3), forming a complete molecular regulatory module involved in flavonoid biosynthesis. This cluster is selected during Tartary buckwheat domestication and is widely present in species of the Fagopyrum genus. In wild relatives of cultivated buckwheat, a gene encoding anthocyanin glycosyltransferase (AGT), which glycosylates pelargonidin into pelargonidin-3-O-glucoside, is found inserted into this cluster. The pelargonidin-3-O-glucoside can help plants resist UV stress, endowing wild relatives with stronger high-altitude adaptability. This study provides a new research paradigm for the evolutionary dynamics of plant BGCs, and offers new perspectives for exploring the mechanism of plant ecological adaptability driven by environmental stress through the synthesis of secondary metabolites.

Advanced ScienceVol. 11(43)
Chungbuk National University (KR), Bulgarian Academy of Sciences (BG), Center of Plant Systems Biology and Biotechnology (BG), Max Planck Institute of Molecular Plant Physiology (DE), Chinese Academy of Agricultural Sciences (CN), Institute of Crop Sciences (CN), UCLouvain (BE)
European Commission, National Natural Science Foundation of China, Chinese Academy of Agricultural Sciences, European Regional Development Fund
Openalex Percentile: Top 2%
Seed and Plant Biochemistry
8.71
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