Genome resequencing reveals the genetic basis of population evolution, local adaptation, and rewiring of the rhizome metabolome in <i>Atractylodes lancea</i>

Abstract

The formation of high-quality Chinese medicinal materials is a micro-evolutionary process of multiple genes involving quantitative inheritance under environmental stress. <i>Atractylodes lancea</i> is a traditionally used medicinal plant in China that is broadly distributed and possesses a considerable amount of essential oils. However, to date, limited research has been conducted to characterize the genetics and metabolites of <i>A. lancea</i> shaped by natural variation. Hence, we assembled a high-quality genome of <i>A. lancea</i>, featuring a contig N50 of 1.18 Mb. We further integrated population resequencing of <i>A. lancea</i> and conducted analyses to characterize its genetic diversity, population evolution, and rewiring of volatile metabolites. The natural variation effect exerted significant pressure on <i>A. lancea</i> from different geographic locations, resulting in genetic differentiation among three groups. Correlation analysis of metabolites in <i>A. lancea</i> revealed significant natural variations of terpenoids, heterocyclic compounds, ketones, and esters. We also found that 427 metabolites displayed noteworthy divergence due to directional selection. Additionally, our genome-wide association studies on the metabolome for medicinal quality traits identified several candidate genes, such as <i>AlZFP706</i> and <i>AlAAHY1</i>, exhibiting significant correlations with atractylodin and hinesol levels, respectively. Overall, this study provides an intricate genomic resource for <i>A. lancea</i>, thereby expanding our understanding of the effect of natural variation on metabolites and facilitating the genetic improvement of its medicinal properties.