Ancient origin and conserved gene function in terpene pheromone and defense evolution of stink bugs and hemipteran insects

Ancient origin and conserved gene function in terpene pheromone and defense evolution of stink bugs and hemipteran insects
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萜类信息素的古老起源和保守基因功能以及椿象和半翅目昆虫的防御进化

DOI:
10.1016/j.ibmb.2022.103879
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发表时间:
2023
影响因子:
3.8
通讯作者:
Weber, Donald C.
Weber, Donald C.
中科院分区:
农林科学2区
文献类型:
--
作者:
Rebholz, Zarley;Lancaster, Jason;Larose, Hailey;Khrimian, Ashot;Luck, Katrin;Sparks, Michael E.;Gendreau, Kerry L.;Shewade, Leena;Köllner, Tobias G.;Weber, Donald C.

文献摘要

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昆虫利用各种各样的小分子,如大类萜烯的代谢产物,进行种内和种间的通讯和防御。这些分子通过专门的代谢途径合成;然而,参与萜烯生物合成的酶的起源及其在昆虫基因组中的进化仍然知之甚少。我们解决了这个问题,通过调查异戊二烯基二磷酸合酶(IDS)的进化与萜烯合酶(TPS)功能的家庭中的蝽(蝽科)的大订单刺吸半翅目昆虫。蝽象包括全球害虫地位的物种,其中许多释放结构相关的15碳倍半萜作为性或聚集信息素。我们提供的证据表明,IDS型TPS酶的出现在1亿多年前的Pentatomid进化开始时,与开花植物的进化相吻合。不同地理来源的蝽象都保持着小的IDS型家族,这些家族具有保守的TPS功能基因,这与植物中TPS基因的多样性形成了鲜明对比。在其他半翅目昆虫中的扩展基因挖掘和系统发育分析进一步提供了证据,证明在tertoxin介导的化学相互作用的假定选择下,古老的IDS样基因的出现,并且这个过程独立于甲虫中IDS型TPS基因的类似进化。我们的研究结果进一步表明,TPS多样化的昆虫和植物在化学相互作用中的基因功能化的不同模式。
Insects use diverse arrays of small molecules such as metabolites of the large class of terpenes for intra- and inter-specific communication and defense. These molecules are synthesized by specialized metabolic pathways; however, the origin of enzymes involved in terpene biosynthesis and their evolution in insect genomes is still poorly understood. We addressed this question by investigating the evolution of isoprenyl diphosphate synthase (IDS)-like genes with terpene synthase (TPS) function in the family of stink bugs (Pentatomidae) within the large order of piercing–sucking Hemipteran insects. Stink bugs include species of global pest status, many of which emit structurally related 15-carbon sesquiterpenes as sex or aggregation pheromones. We provide evidence for the emergence of IDS-type TPS enzymes at the onset of pentatomid evolution over 100 million years ago, coinciding with the evolution of flowering plants. Stink bugs of different geographical origin maintain small IDS-type families with genes of conserved TPS function, which stands in contrast to the diversification of TPS genes in plants. Expanded gene mining and phylogenetic analysis in other hemipteran insects further provides evidence for an ancient emergence of IDS-like genes under presumed selection for terpene-mediated chemical interactions, and this process occurred independently from a similar evolution of IDS-type TPS genes in beetles. Our findings further suggest differences in TPS diversification in insects and plants in conjunction with different modes of gene functionalization in chemical interactions.