Large-scale metabolomic landscape of edible maize reveals convergent changes in metabolite differentiation and facilitates its breeding improvement.

Abstract

Edible maize is an important food crop that provides energy and nutrients to meet human health and nutritional requirements. However, how environmental pressures and human activity have shaped the metabolome of edible maize remains unclear. In this study, we collected 452 diverse edible maize accessions worldwide, including waxy, sweet, and field maize. A total of 3020 non-redundant metabolites, including 802 annotated metabolites, were identified using a two-step optimized approach, which generated the most comprehensive annotated metabolite dataset in plants to date. Although specific metabolite differentiation was detected between field and sweet maize and between field and waxy maize, convergent metabolite differentiation was the dominant pattern. We identified hub genes in all metabolite classes by hotspot analysis in a metabolite genome-wide association study. Seventeen and 15 hub genes were selected as the key differentiation genes for flavonoids and lipids, respectively. Surprisingly, almost all of these genes were under diversifying selection, suggesting that diversifying selection was the main genetic mechanism of convergent metabolic differentiation. Further genetic and molecular studies revealed the roles and genetic diversifying selection mechanisms of ZmGPAT11 in convergent metabolite differentiation in the lipid pathway. On the basis of our research, we established the first edible maize metabolome database, EMMDB (https://www.maizemdb.site/home/). We successfully used EMMDB for precision improvement of nutritional and flavor traits and bred the elite inbred line 6644_2, with greatly increased contents of flavonoids, lysophosphatidylcholines, lysophosphatidylethanolamines, and vitamins. Collectively, our study sheds light on the genetic mechanisms of metabolite differentiation in edible maize and provides a database for breeding improvement of flavor and nutritional traits in edible maize by metabolome precision design.