Large-scale metabolomic landscape of edible maize reveals convergent changes in metabolite differentiation and facilitates its breeding improvement
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 access...
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| Published in | Molecular plant Vol. 18; no. 4; pp. 619 - 638 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
Elsevier Inc
07.04.2025
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| Online Access | Get full text |
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| 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.
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. |
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| AbstractList | 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. Edible maize is an important food crop, providing energy and nutrients to meet human health and nutritional requirements. However, how environmental pressures and human activity have shaped the edible maize metabolome remains unclear. In this study, we collected 452 diverse edible maize accessions worldwide, comprising waxy, sweet, and field maize. A total of 3,020 non-redundant metabolites, including 802 annotated metabolites, were identified by a two-step optimized approach, which generated the most comprehensive annotated metabolites dataset in plants to date. Although specific metabolite differentiation was detected in Field-Sweet and Field-Waxy differentiations, convergent metabolite differentiation was the dominant differentiation pattern. We identified hub genes in all metabolite classes by mGWAS hotspot analysis. A total of 17 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, which indicated diversifying selection was the main genetic mechanism of convergent metabolic differentiation. Furthermore, the genetic and molecular studies reveal the roles and diversifying selection genetic mechanisms of ZmGPAT11 in convergent metabolite differentiation in lipid pathway. Based on our research, we established the first edible maize metabolome database, EMMDB (www.maizemdb.site/home/). We successfully applied EMMDB for precision improvement of nutritional and flavor traits, and an elite inbred line 6644_2 was bred with greatly improved in contents of flavonoids, lysophosphatidylcholines, lysophosphatidylethanolamines, and vitamins. These findings provide insights into the underlying genetic mechanisms of edible maize metabolite differentiation and provide a database for the breeding improvement of edible maize flavor and nutritional traits by metabolome precision design.Edible maize is an important food crop, providing energy and nutrients to meet human health and nutritional requirements. However, how environmental pressures and human activity have shaped the edible maize metabolome remains unclear. In this study, we collected 452 diverse edible maize accessions worldwide, comprising waxy, sweet, and field maize. A total of 3,020 non-redundant metabolites, including 802 annotated metabolites, were identified by a two-step optimized approach, which generated the most comprehensive annotated metabolites dataset in plants to date. Although specific metabolite differentiation was detected in Field-Sweet and Field-Waxy differentiations, convergent metabolite differentiation was the dominant differentiation pattern. We identified hub genes in all metabolite classes by mGWAS hotspot analysis. A total of 17 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, which indicated diversifying selection was the main genetic mechanism of convergent metabolic differentiation. Furthermore, the genetic and molecular studies reveal the roles and diversifying selection genetic mechanisms of ZmGPAT11 in convergent metabolite differentiation in lipid pathway. Based on our research, we established the first edible maize metabolome database, EMMDB (www.maizemdb.site/home/). We successfully applied EMMDB for precision improvement of nutritional and flavor traits, and an elite inbred line 6644_2 was bred with greatly improved in contents of flavonoids, lysophosphatidylcholines, lysophosphatidylethanolamines, and vitamins. These findings provide insights into the underlying genetic mechanisms of edible maize metabolite differentiation and provide a database for the breeding improvement of edible maize flavor and nutritional traits by metabolome precision design. 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. 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. |
| Author | Xu, Li Wang, Fengge Zhao, Jiuran Zhao, Yanxin Song, Wei Luo, Meijie Su, Aiguo Ge, Jianrong Yu, Ainian Lu, Baishan Lv, Yuanda Liu, Hui Xi, Shengli Li, Chunhui Wang, Xiaqing Zhang, Ruyang Li, Huihui Tian, Hongli Shi, Yaxing Wang, Shuai Jiao, Yanyan Li, Zhiyong Xiao, Senlin Wang, Ronghuan Dong, Hui Fan, Yanli Yi, Hongmei |
| Author_xml | – sequence: 1 givenname: Chunhui surname: Li fullname: Li, Chunhui organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 2 givenname: Zhiyong surname: Li fullname: Li, Zhiyong organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 3 givenname: Baishan surname: Lu fullname: Lu, Baishan organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 4 givenname: Yaxing surname: Shi fullname: Shi, Yaxing organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 5 givenname: Senlin surname: Xiao fullname: Xiao, Senlin organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 6 givenname: Hui surname: Dong fullname: Dong, Hui organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 7 givenname: Ruyang surname: Zhang fullname: Zhang, Ruyang organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 8 givenname: Hui surname: Liu fullname: Liu, Hui organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 9 givenname: Yanyan surname: Jiao fullname: Jiao, Yanyan organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 10 givenname: Li surname: Xu fullname: Xu, Li organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 11 givenname: Aiguo surname: Su fullname: Su, Aiguo organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 12 givenname: Xiaqing surname: Wang fullname: Wang, Xiaqing organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 13 givenname: Yanxin surname: Zhao fullname: Zhao, Yanxin organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 14 givenname: Shuai surname: Wang fullname: Wang, Shuai organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 15 givenname: Yanli surname: Fan fullname: Fan, Yanli organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 16 givenname: Meijie surname: Luo fullname: Luo, Meijie organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 17 givenname: Shengli surname: Xi fullname: Xi, Shengli organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 18 givenname: Ainian surname: Yu fullname: Yu, Ainian organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 19 givenname: Fengge surname: Wang fullname: Wang, Fengge organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 20 givenname: Jianrong surname: Ge fullname: Ge, Jianrong organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 21 givenname: Hongli surname: Tian fullname: Tian, Hongli organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 22 givenname: Hongmei surname: Yi fullname: Yi, Hongmei organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 23 givenname: Yuanda surname: Lv fullname: Lv, Yuanda organization: Excellence and Innovation Center, Jiangsu Academy of Agricultural Sciences, Nanjing, China – sequence: 24 givenname: Huihui surname: Li fullname: Li, Huihui organization: State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing, China – sequence: 25 givenname: Ronghuan surname: Wang fullname: Wang, Ronghuan email: ronghuanwang@126.com organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 26 givenname: Wei surname: Song fullname: Song, Wei email: songwei1007@126.com organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China – sequence: 27 givenname: Jiuran surname: Zhao fullname: Zhao, Jiuran email: maizezhao@126.com organization: Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Institute, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China |
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| Keywords | metabolome database metabolite differentiation waxy maize sweet maize diversifying selection |
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| Snippet | Edible maize is an important food crop that provides energy and nutrients to meet human health and nutritional requirements. However, how environmental... Edible maize is an important food crop, providing energy and nutrients to meet human health and nutritional requirements. However, how environmental pressures... Edible maize is an important food crop that provides energy and nutrients to meet human health and nutritional requirements. However, how environmental... |
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| SubjectTerms | 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 |
| Title | Large-scale metabolomic landscape of edible maize reveals convergent changes in metabolite differentiation and facilitates its breeding improvement |
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