Xinlu Chen, Meimei Xu, Jin Han, Mark Schmidt-Dannert, Reuben J Peters, Feng Chen
{"title":"在细菌中发现双功能二萜环化酶/合成酶证明植物萜合成酶基因家族起源于细菌","authors":"Xinlu Chen, Meimei Xu, Jin Han, Mark Schmidt-Dannert, Reuben J Peters, Feng Chen","doi":"10.1093/hr/uhae221","DOIUrl":null,"url":null,"abstract":"Land plants are well known producers of terpenoids that play diverse roles in plant-environment interactions. The vast chemical diversity of terpenoids is initiated by terpene synthases. Plants contain a distinct mid-sized terpene synthase gene family termed TPS, which appears to have an ancient origin in a fused bacterial class I (di)terpene synthase (TS) and class II diterpene cyclase (DTC), corresponding to the catalytically relevant α-domain and βγ-didomains, respectively. However, while such fused tridomain bifunctional (class I/II) diterpene cyclases-synthases (DCSs) have been found in plants (and fungi), no examples have been reported from bacteria, leaving the origin of the fusion event initiating the TPS gene family opaque. Here, discovery of such tridomain bifunctional DCSs in bacteria is reported. Extensive genome mining unearthed five putative bacterial DCSs, with biochemical characterization revealing the expected bifunctional activity for three. Most intriguing was CseDCS, which produces ent-kaurene, an intermediate in plant hormone biosynthesis, as this is the hypothesized activity for the ancestral TPS. Unlike the extant functionally equivalent TPSs, it was possible to split CseDCS into separate, independently acting DTC and TS, with the first producing the expected ent-copalyl diphosphate (CPP), serving as a CPP synthase (CPS), while the second converts this to ent-kaurene, serving as a kaurene synthase (KS). Nevertheless, sequence alignment and mutation analysis revealed intriguing similarities between this cyanobacterial fused CPS-KS and the functionally equivalent TPSs. Regardless of exact relationship, discovery of fused bifunctional DCSs in bacteria supports the hypothesized origin of the plant TPS family from such a bacterial gene.","PeriodicalId":13179,"journal":{"name":"Horticulture Research","volume":null,"pages":null},"PeriodicalIF":8.7000,"publicationDate":"2024-08-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Discovery of bifunctional diterpene cyclases/synthases in bacteria supports a bacterial origin for the plant terpene synthase gene family\",\"authors\":\"Xinlu Chen, Meimei Xu, Jin Han, Mark Schmidt-Dannert, Reuben J Peters, Feng Chen\",\"doi\":\"10.1093/hr/uhae221\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"Land plants are well known producers of terpenoids that play diverse roles in plant-environment interactions. The vast chemical diversity of terpenoids is initiated by terpene synthases. Plants contain a distinct mid-sized terpene synthase gene family termed TPS, which appears to have an ancient origin in a fused bacterial class I (di)terpene synthase (TS) and class II diterpene cyclase (DTC), corresponding to the catalytically relevant α-domain and βγ-didomains, respectively. However, while such fused tridomain bifunctional (class I/II) diterpene cyclases-synthases (DCSs) have been found in plants (and fungi), no examples have been reported from bacteria, leaving the origin of the fusion event initiating the TPS gene family opaque. Here, discovery of such tridomain bifunctional DCSs in bacteria is reported. Extensive genome mining unearthed five putative bacterial DCSs, with biochemical characterization revealing the expected bifunctional activity for three. Most intriguing was CseDCS, which produces ent-kaurene, an intermediate in plant hormone biosynthesis, as this is the hypothesized activity for the ancestral TPS. Unlike the extant functionally equivalent TPSs, it was possible to split CseDCS into separate, independently acting DTC and TS, with the first producing the expected ent-copalyl diphosphate (CPP), serving as a CPP synthase (CPS), while the second converts this to ent-kaurene, serving as a kaurene synthase (KS). Nevertheless, sequence alignment and mutation analysis revealed intriguing similarities between this cyanobacterial fused CPS-KS and the functionally equivalent TPSs. Regardless of exact relationship, discovery of fused bifunctional DCSs in bacteria supports the hypothesized origin of the plant TPS family from such a bacterial gene.\",\"PeriodicalId\":13179,\"journal\":{\"name\":\"Horticulture Research\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":8.7000,\"publicationDate\":\"2024-08-03\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Horticulture Research\",\"FirstCategoryId\":\"97\",\"ListUrlMain\":\"https://doi.org/10.1093/hr/uhae221\",\"RegionNum\":1,\"RegionCategory\":\"农林科学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"Agricultural and Biological Sciences\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Horticulture Research","FirstCategoryId":"97","ListUrlMain":"https://doi.org/10.1093/hr/uhae221","RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"Agricultural and Biological Sciences","Score":null,"Total":0}
Discovery of bifunctional diterpene cyclases/synthases in bacteria supports a bacterial origin for the plant terpene synthase gene family
Land plants are well known producers of terpenoids that play diverse roles in plant-environment interactions. The vast chemical diversity of terpenoids is initiated by terpene synthases. Plants contain a distinct mid-sized terpene synthase gene family termed TPS, which appears to have an ancient origin in a fused bacterial class I (di)terpene synthase (TS) and class II diterpene cyclase (DTC), corresponding to the catalytically relevant α-domain and βγ-didomains, respectively. However, while such fused tridomain bifunctional (class I/II) diterpene cyclases-synthases (DCSs) have been found in plants (and fungi), no examples have been reported from bacteria, leaving the origin of the fusion event initiating the TPS gene family opaque. Here, discovery of such tridomain bifunctional DCSs in bacteria is reported. Extensive genome mining unearthed five putative bacterial DCSs, with biochemical characterization revealing the expected bifunctional activity for three. Most intriguing was CseDCS, which produces ent-kaurene, an intermediate in plant hormone biosynthesis, as this is the hypothesized activity for the ancestral TPS. Unlike the extant functionally equivalent TPSs, it was possible to split CseDCS into separate, independently acting DTC and TS, with the first producing the expected ent-copalyl diphosphate (CPP), serving as a CPP synthase (CPS), while the second converts this to ent-kaurene, serving as a kaurene synthase (KS). Nevertheless, sequence alignment and mutation analysis revealed intriguing similarities between this cyanobacterial fused CPS-KS and the functionally equivalent TPSs. Regardless of exact relationship, discovery of fused bifunctional DCSs in bacteria supports the hypothesized origin of the plant TPS family from such a bacterial gene.
期刊介绍:
Horticulture Research, an open access journal affiliated with Nanjing Agricultural University, has achieved the prestigious ranking of number one in the Horticulture category of the Journal Citation Reports ™ from Clarivate, 2022. As a leading publication in the field, the journal is dedicated to disseminating original research articles, comprehensive reviews, insightful perspectives, thought-provoking comments, and valuable correspondence articles and letters to the editor. Its scope encompasses all vital aspects of horticultural plants and disciplines, such as biotechnology, breeding, cellular and molecular biology, evolution, genetics, inter-species interactions, physiology, and the origination and domestication of crops.