Proteomics and Co-expression Network Analysis Reveal the Importance of Hub Proteins and Metabolic Pathways in Nicotine Synthesis and Accumulation in Tobacco (Nicotiana tabacum L.)
Nicotine is a unique alkaloid present in tobacco that is widely used in cigarettes and in the agricultural, chemical, and pharmaceutical industries. However, the research on nicotine is mostly limited to its synthesis pathways, and only a few studies have explored the effects of other metabolic path...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-04-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2022.860455/full |
| _version_ | 1811288867203973120 |
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| author | Zejun Mo Zejun Mo Lili Duan Lili Duan Yuanyuan Pu Yuanyuan Pu Zonglin Tian Zonglin Tian Yuzhou Ke Yuzhou Ke Wen Luo Wen Luo Kai Pi Kai Pi Ying Huang Ying Huang Qiong Nie Qiong Nie Renxiang Liu Renxiang Liu |
| author_facet | Zejun Mo Zejun Mo Lili Duan Lili Duan Yuanyuan Pu Yuanyuan Pu Zonglin Tian Zonglin Tian Yuzhou Ke Yuzhou Ke Wen Luo Wen Luo Kai Pi Kai Pi Ying Huang Ying Huang Qiong Nie Qiong Nie Renxiang Liu Renxiang Liu |
| author_sort | Zejun Mo |
| collection | DOAJ |
| description | Nicotine is a unique alkaloid present in tobacco that is widely used in cigarettes and in the agricultural, chemical, and pharmaceutical industries. However, the research on nicotine is mostly limited to its synthesis pathways, and only a few studies have explored the effects of other metabolic pathways on nicotine precursors. Regulating the nicotine content in tobacco can greatly promoting the application of nicotine in other fields. In this study, we performed global data-independent acquisition proteomics analysis of four tobacco varieties. Of the four varieties, one had high nicotine content and three had a low nicotine content. A total of 31,259 distinct peptides and 6,018 proteins across two samples were identified. A total of 45 differentially expressed proteins (DEPs) co-existed in the three comparison groups and were mainly involved in the transport and metallic processes of the substances. Most DEPs were enriched in the biosynthesis of secondary metals, glutathione metabolism, carbon metabolism, and glycolysis/gluconeogenesis. In addition, the weighted gene co-expression network analysis identified an expression module closely related to the nicotine content (Brown, r = 0.74, P = 0.006). Gene Ontology annotation and Kyoto Encyclopaedia of Genes and Genomes enrichment analysis showed that the module proteins were mainly involved in the synthesis and metabolism of nicotine precursors such as arginine, ornithine aspartate, proline, and glutathione. The increased levels of these precursors lead to the synthesis and accumulation of nicotine in plants. More importantly, these proteins regulate nicotine synthesis by affecting the formation of putrescine, which is the core intermediate product in nicotine anabolism. Our results provide a reference for tobacco variety selection with a suitable nicotine content and regulation of the nicotine content. Additionally, the results highlight the importance of other precursor metabolism in nicotine synthesis. |
| first_indexed | 2024-04-13T03:44:52Z |
| format | Article |
| id | doaj.art-a68d902a494c4564823376164eb7a023 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-04-13T03:44:52Z |
| publishDate | 2022-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-a68d902a494c4564823376164eb7a0232022-12-22T03:04:03ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-04-011310.3389/fpls.2022.860455860455Proteomics and Co-expression Network Analysis Reveal the Importance of Hub Proteins and Metabolic Pathways in Nicotine Synthesis and Accumulation in Tobacco (Nicotiana tabacum L.)Zejun Mo0Zejun Mo1Lili Duan2Lili Duan3Yuanyuan Pu4Yuanyuan Pu5Zonglin Tian6Zonglin Tian7Yuzhou Ke8Yuzhou Ke9Wen Luo10Wen Luo11Kai Pi12Kai Pi13Ying Huang14Ying Huang15Qiong Nie16Qiong Nie17Renxiang Liu18Renxiang Liu19College of Agriculture, Guizhou University, Guiyang, ChinaKey Laboratory of Tobacco Quality in Guizhou Province, Guiyang, ChinaCollege of Agriculture, Guizhou University, Guiyang, ChinaKey Laboratory of Tobacco Quality in Guizhou Province, Guiyang, ChinaCollege of Agriculture, Guizhou University, Guiyang, ChinaKey Laboratory of Tobacco Quality in Guizhou Province, Guiyang, ChinaKey Laboratory of Tobacco Quality in Guizhou Province, Guiyang, ChinaCollege of Tobacco, Guizhou University, Guiyang, ChinaKey Laboratory of Tobacco Quality in Guizhou Province, Guiyang, ChinaCollege of Tobacco, Guizhou University, Guiyang, ChinaKey Laboratory of Tobacco Quality in Guizhou Province, Guiyang, ChinaCollege of Tobacco, Guizhou University, Guiyang, ChinaKey Laboratory of Tobacco Quality in Guizhou Province, Guiyang, ChinaCollege of Tobacco, Guizhou University, Guiyang, ChinaKey Laboratory of Tobacco Quality in Guizhou Province, Guiyang, ChinaCollege of Tobacco, Guizhou University, Guiyang, ChinaKey Laboratory of Tobacco Quality in Guizhou Province, Guiyang, ChinaCollege of Tobacco, Guizhou University, Guiyang, ChinaKey Laboratory of Tobacco Quality in Guizhou Province, Guiyang, ChinaCollege of Tobacco, Guizhou University, Guiyang, ChinaNicotine is a unique alkaloid present in tobacco that is widely used in cigarettes and in the agricultural, chemical, and pharmaceutical industries. However, the research on nicotine is mostly limited to its synthesis pathways, and only a few studies have explored the effects of other metabolic pathways on nicotine precursors. Regulating the nicotine content in tobacco can greatly promoting the application of nicotine in other fields. In this study, we performed global data-independent acquisition proteomics analysis of four tobacco varieties. Of the four varieties, one had high nicotine content and three had a low nicotine content. A total of 31,259 distinct peptides and 6,018 proteins across two samples were identified. A total of 45 differentially expressed proteins (DEPs) co-existed in the three comparison groups and were mainly involved in the transport and metallic processes of the substances. Most DEPs were enriched in the biosynthesis of secondary metals, glutathione metabolism, carbon metabolism, and glycolysis/gluconeogenesis. In addition, the weighted gene co-expression network analysis identified an expression module closely related to the nicotine content (Brown, r = 0.74, P = 0.006). Gene Ontology annotation and Kyoto Encyclopaedia of Genes and Genomes enrichment analysis showed that the module proteins were mainly involved in the synthesis and metabolism of nicotine precursors such as arginine, ornithine aspartate, proline, and glutathione. The increased levels of these precursors lead to the synthesis and accumulation of nicotine in plants. More importantly, these proteins regulate nicotine synthesis by affecting the formation of putrescine, which is the core intermediate product in nicotine anabolism. Our results provide a reference for tobacco variety selection with a suitable nicotine content and regulation of the nicotine content. Additionally, the results highlight the importance of other precursor metabolism in nicotine synthesis.https://www.frontiersin.org/articles/10.3389/fpls.2022.860455/fullnicotineproteomicsweighted gene co-expression network analysismetabolitesenzyme activityNicotiana tabacum |
| spellingShingle | Zejun Mo Zejun Mo Lili Duan Lili Duan Yuanyuan Pu Yuanyuan Pu Zonglin Tian Zonglin Tian Yuzhou Ke Yuzhou Ke Wen Luo Wen Luo Kai Pi Kai Pi Ying Huang Ying Huang Qiong Nie Qiong Nie Renxiang Liu Renxiang Liu Proteomics and Co-expression Network Analysis Reveal the Importance of Hub Proteins and Metabolic Pathways in Nicotine Synthesis and Accumulation in Tobacco (Nicotiana tabacum L.) Frontiers in Plant Science nicotine proteomics weighted gene co-expression network analysis metabolites enzyme activity Nicotiana tabacum |
| title | Proteomics and Co-expression Network Analysis Reveal the Importance of Hub Proteins and Metabolic Pathways in Nicotine Synthesis and Accumulation in Tobacco (Nicotiana tabacum L.) |
| title_full | Proteomics and Co-expression Network Analysis Reveal the Importance of Hub Proteins and Metabolic Pathways in Nicotine Synthesis and Accumulation in Tobacco (Nicotiana tabacum L.) |
| title_fullStr | Proteomics and Co-expression Network Analysis Reveal the Importance of Hub Proteins and Metabolic Pathways in Nicotine Synthesis and Accumulation in Tobacco (Nicotiana tabacum L.) |
| title_full_unstemmed | Proteomics and Co-expression Network Analysis Reveal the Importance of Hub Proteins and Metabolic Pathways in Nicotine Synthesis and Accumulation in Tobacco (Nicotiana tabacum L.) |
| title_short | Proteomics and Co-expression Network Analysis Reveal the Importance of Hub Proteins and Metabolic Pathways in Nicotine Synthesis and Accumulation in Tobacco (Nicotiana tabacum L.) |
| title_sort | proteomics and co expression network analysis reveal the importance of hub proteins and metabolic pathways in nicotine synthesis and accumulation in tobacco nicotiana tabacum l |
| topic | nicotine proteomics weighted gene co-expression network analysis metabolites enzyme activity Nicotiana tabacum |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2022.860455/full |
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