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The gradual establishment of complex coumarin biosynthetic pathway in Apiaceae

文献类型： 外文期刊

作者： Huang, Xin-Cheng 1 ; Tang, Huanying 2 ; Wei, Xuefen 1 ; He, Yuedong 4 ; Hu, Shuaiya 1 ; Wu, Jia-Yi 1 ; Xu, Dingqiao 5 ; Qiao, Fei 6 ; Xue, Jia-Yu 1 ; Zhao, Yucheng 2 ;

作者机构： 1.Nanjing Agr Univ, Acad Adv Interdisciplinary Studies, Coll Hort, Bioinformat Ctr, Nanjing 210095, Jiangsu, Peoples R China

2.China Pharmaceut Univ, Sch Tradit Chinese Pharm, Dept Resources Sci Tradit Chinese Med, Nanjing 210009, Jiangsu, Peoples R China

3.China Pharmaceut Univ, State Key Lab Nat Med, Nanjing 210009, Jiangsu, Peoples R China

4.Hunan Agr Univ, Coll Biosci & Biotechnol, Changsha 410128, Hunan, Peoples R China

5.Shaanxi Univ Chinese Med, Sch Pharm, Xian 712046, Shaanxi, Peoples R China

6.Natl Key Lab Trop Crop Breeding, Sanya 572024, Hainan, Peoples R China

7.Chinese Acad Trop Agr Sci, Trop Crops Genet Resources Inst, Haikou 571101, Hainan, Peoples R China

8.China Pharmaceut Univ, Med Bot Garden, Nanjing 210009, Jiangsu, Peoples R China

期刊名称：NATURE COMMUNICATIONS （ 影响因子：14.7； 五年影响因子：16.1 ）

ISSN：

年卷期： 2024 年 15 卷 1 期

页码：

收录情况： SCI

摘要： Complex coumarins (CCs) represent characteristic metabolites found in Apiaceae plants, possessing significant medical value. Their essential functional role is likely as protectants against pathogens and regulators responding to environmental stimuli. Utilizing genomes and transcriptomes from 34 Apiaceae plants, including our recently sequenced Peucedanum praeruptorum, we conduct comprehensive phylogenetic analyses to reconstruct the detailed evolutionary process of the CC biosynthetic pathway in Apiaceae. Our results show that three key enzymes - p-coumaroyl CoA 2'-hydroxylase (C2'H), C-prenyltransferase (C-PT), and cyclase - originated successively at different evolutionary nodes within Apiaceae through various means of gene duplications: ectopic and tandem duplications. Neofunctionalization endows these enzymes with novel functions necessary for CC biosynthesis, thus completing the pathway. Candidate genes are cloned for heterologous expression and subjected to in vitro enzymatic assays to test our hypothesis regarding the origins of the key enzymes, and the results precisely validate our evolutionary inferences. Among the three enzymes, C-PTs are likely the primary determinant of the structural diversity of CCs (linear/angular), due to divergent activities evolved to target different positions (C-6 or C-8) of umbelliferone. A key amino acid variation (Ala161/Thr161) is identified and proven to play a crucial role in the alteration of enzymatic activity, possibly resulting in distinct binding forms between enzymes and substrates, thereby leading to different products. In conclusion, this study provides a detailed trajectory for the establishment and evolution of the CC biosynthetic pathway in Apiaceae. It explains why only a portion, not all, of Apiaceae plants can produce CCs and reveals the mechanisms of CC structural diversity among different Apiaceae plants. This study explores the origin and evolution of complex coumarin (CC) biosynthetic pathway in Apiaceae. The results explain why CCs are only detected in limited Apiaceae species, and clarify the mechanism underlying the linear and angular configurations of Apiaceae CCs.

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