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

• Published in: Molecular plant Vol. 18; no. 4; pp. 619 - 638
• Main Authors: Li, Chunhui, Li, Zhiyong, Lu, Baishan, Shi, Yaxing, Xiao, Senlin, Dong, Hui, Zhang, Ruyang, Liu, Hui, Jiao, Yanyan, Xu, Li, Su, Aiguo, Wang, Xiaqing, Zhao, Yanxin, Wang, Shuai, Fan, Yanli, Luo, Meijie, Xi, Shengli, Yu, Ainian, Wang, Fengge, Ge, Jianrong, Tian, Hongli, Yi, Hongmei, Lv, Yuanda, Li, Huihui, Wang, Ronghuan, Song, Wei, Zhao, Jiuran
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 07.04.2025
• Subjects: data collection; diversifying selection; energy; flavonoids; flavor; food crops; Genome-Wide Association Study; human health; humans; landscapes; lysophosphatidylcholine; metabolite differentiation; metabolites; metabolome; Metabolome - genetics; metabolome database; Metabolomics; Plant Breeding; sweet maize; waxy corn; waxy maize; Zea mays - genetics; Zea mays - metabolism; metabolome database; metabolite differentiation; waxy maize; sweet maize; diversifying selection
• ISSN: 1674-2052; 1752-9867; 1752-9867
• DOI: 10.1016/j.molp.2025.02.007

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. A total of 3020 non-redundant metabolites (including 802 annotated metabolites) are identified from 452 diverse edible maize accessions worldwide. Seventeen and 15 hub genes are identified as key differentiation genes for flavonoids and lipids, respectively. Additional analyses reveal that ZmGPAT11 underwent diversifying selection during convergent metabolite differentiation in the lipid pathway. An edible maize metabolome database, EMMDB, is established for guiding improvement of maize nutritional and flavor traits.