Jia Qidong, Brown Reid, Köllner Tobias G, Fu Jianyu, Chen Xinlu, Wong Gane Ka-Shu, Gershenzon Jonathan, Peters Reuben J, Chen Feng
Graduate School of Genome Science and Technology, The University of Tennessee, Knoxville, TN 37996.
Roy J. Carver Department of Biochemistry, Biophysics and Molecular Biology, Iowa State University, Ames, IA 50011.
Proc Natl Acad Sci U S A. 2022 Apr 12;119(15):e2100361119. doi: 10.1073/pnas.2100361119. Epub 2022 Apr 8.
As a midsized gene family conserved more by lineage than function, the typical plant terpene synthases (TPSs) could be a valuable tool to examine plant evolution. TPSs are pivotal in biosynthesis of gibberellins and related phytohormones as well as in formation of the extensive arsenal of specialized plant metabolites mediating ecological interactions whose production is often lineage specific. Yet the origin and early evolution of the TPS family is not well understood. Systematic analysis of an array of transcriptomes and sequenced genomes indicated that the TPS family originated after the divergence of land plants from charophytic algae. Phylogenetic and biochemical analyses support the hypothesis that the ancestral TPS gene encoded a bifunctional class I and II diterpene synthase producing the ent-kaurene required for phytohormone production in all extant lineages of land plants. Moreover, the ancestral TPS gene likely underwent duplication at least twice early in land plant evolution. Together these two gave rise to three TPS lineages leading to the extant TPS-c, TPS-e/f, and the remaining TPS (h/d/a/b/g) subfamilies, with the latter dedicated to secondary rather than primary metabolism while the former two contain those genes involved in ent-kaurene production. Nevertheless, parallel evolution from the ent-kaurene–producing class I and class II diterpene synthases has led to roles for TPS-e/f and -c subfamily members in secondary metabolism as well. These results clarify TPS evolutionary history and provide context for the role of these genes in producing the vast diversity of terpenoid natural products observed today in various land plant lineages.
作为一个中等规模的基因家族，其更多地是按谱系而非功能保守下来的，典型的植物萜类合酶（TPSs）可能是研究植物进化的一个有价值的工具。TPSs在赤霉素及相关植物激素的生物合成中起关键作用，同时也参与形成大量介导生态相互作用的植物特殊代谢产物库，这些代谢产物的产生往往具有谱系特异性。然而，TPS家族的起源和早期进化仍未得到很好的理解。对一系列转录组和已测序基因组的系统分析表明，TPS家族起源于陆地植物与轮藻分歧之后。系统发育和生化分析支持这样一种假说，即祖先的TPS基因编码一种双功能的I类和II类二萜合酶，可产生陆地植物所有现存谱系中植物激素合成所需的贝壳杉烯。此外，祖先的TPS基因可能在陆地植物进化早期至少经历了两次复制。这两者共同产生了三个TPS谱系，导致现存的TPS-c、TPS-e/f和其余的TPS（h/d/a/b/g）亚家族，其中后者专门负责次生而非初生代谢，而前两个亚家族包含参与贝壳杉烯合成的基因。尽管如此，从产生贝壳杉烯的I类和II类二萜合酶的平行进化也导致TPS-e/f和-c亚家族成员在次生代谢中也发挥了作用。这些结果阐明了TPS的进化历史，并为这些基因在产生当今各种陆地植物谱系中观察到的大量萜类天然产物中的作用提供了背景信息。
