Chen Xinlu, Urban John M, Wurlitzer Jens, Wei Xiuting, Han Jin, E O'Connor Sarah, Rudolf Jeffrey D, Köllner Tobias G, Chen Feng
Department of Plant Sciences, University of Tennessee, Knoxville, TN 37996.
HHMI Research Laboratories, Carnegie Institution for Science, Baltimore, MD 21218.
Proc Natl Acad Sci U S A. 2024 Dec 17;121(51):e2413007121. doi: 10.1073/pnas.2413007121. Epub 2024 Dec 13.
Insects employ terpenoids for communication both within and between species. While terpene synthases derived from isoprenyl diphosphate synthase have been shown to catalyze terpenoid biosynthesis in some insects, canonical terpene synthases (TPS) commonly found in plants, fungi, and bacteria were previously unidentified in insects. This study reveals the presence of genes in insects, likely originating via horizontal gene transfer from noninsect arthropods. By examining 361 insect genomes, we identified genes in five species of the Sciaridae family (fungus gnats). Additionally, genes were found in Collembola (springtails) and Acariformes (mites) among diverse noninsect arthropods. Selected TPS enzymes from Sciaridae, Collembola, and Acariformes display monoterpene, sesquiterpene, and/or diterpene synthase activities. Through comprehensive protein database search and phylogenetic analysis, the genes in Sciaridae were found to be most closely related to those in Acariformes, suggesting transfer of genes from Acariformes to Sciaridae. In the model Sciaridae , all five genes are most highly expressed in adult males, suggesting a sex- and developmental stage-specific role of their terpenoid products. The finding of genes in insects and their possible evolutionary origin through intraphylum gene transfer within arthropods sheds light on metabolic innovation in insects.
昆虫利用萜类化合物在种内和种间进行交流。虽然源自异戊烯基二磷酸合酶的萜烯合酶已被证明可在某些昆虫中催化萜类生物合成，但植物、真菌和细菌中常见的典型萜烯合酶（TPS）此前在昆虫中尚未被鉴定出来。这项研究揭示了昆虫中存在这些基因，它们可能是通过从非昆虫节肢动物的水平基因转移而来。通过检查361个昆虫基因组，我们在菌蚊科（蕈蚊）的五个物种中鉴定出了这些基因。此外，在不同的非昆虫节肢动物中的弹尾目（跳虫）和蜱螨亚纲（螨）中也发现了这些基因。从菌蚊科、弹尾目和蜱螨亚纲中选取的TPS酶表现出单萜、倍半萜和/或二萜合酶活性。通过全面的蛋白质数据库搜索和系统发育分析，发现菌蚊科中的这些基因与蜱螨亚纲中的基因关系最为密切，这表明这些基因从蜱螨亚纲转移到了菌蚊科。在模式菌蚊物种中，所有五个基因在成年雄性中表达量最高，这表明其萜类产物具有性别和发育阶段特异性的作用。昆虫中这些基因的发现以及它们可能通过节肢动物门内的基因转移而产生的进化起源，为昆虫的代谢创新提供了线索。
