Primary Metabolism co-Opted for Defensive Chemical Production in the Carabid Beetle, Harpalus pensylvanicus

Primary Metabolism co-Opted for Defensive Chemical Production in the Carabid Beetle, Harpalus pensylvanicus
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DOI:
10.1007/s10886-021-01253-2
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发表时间:
2021-03
影响因子:
2.3
通讯作者:
Adam M. Rork;Sihang Xu;A. Attygalle;T. Renner
Adam M. Rork;Sihang Xu;A. Attygalle;T. Renner
中科院分区:
环境科学与生态学2区
文献类型:
--
作者:
Adam M. Rork;Sihang Xu;A. Attygalle;T. Renner

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在所描述的大约100万种昆虫中,地面甲虫(鞘翅目:步甲科)由于其合成的防御化合物的多样性,长期以来一直吸引着进化生物学家的注意。甲虫化学物质是用腹部的防御性腺体产生的,代表着250多种化合物,其中包括威慑捕食者的甲酸,甲酸在昆虫门至少三次演变为一种防御策略。尽管甲酸是一种广泛的防御方法,但昆虫对甲酸的生物合成知之甚少。以往的研究表明,一碳(C1)代谢的叶酸循环可能在蚂蚁防御级甲酸的产生中发挥关键作用,这是核苷酸生物合成的一个途径。在这里,我们报告了甲酸生产地甲哈帕勒斯的防御腺转录组。参与叶酸代谢的全套基因在H。防御腺中的表达有显著差异。与身体其他部位的基因表达谱进行比较时。我们还发现了另外两条可能参与防御级甲酸生物合成的途径,犬尿氨酸途径和蛋氨酸回收循环。此外,我们在分泌叶中发现了一系列差异表达的基因,这些基因参与了甲酸生物合成所必需的辅因子的生物合成和运输,以及可能参与解毒包括甲酸在内的次生代谢物的基因。我们还对参与叶酸周期(MTHFD)的主要基因家族的进化进行了深入的研究,并提出叶酸周期基因的高表达而不是基因复制和/或新功能可能对防御级甲酸的生物合成更重要。潘西尔瓦尼克斯。这在鞘翅目中提供了第一个证据,也是昆虫纲中为数不多的几个例子之一,表明初级代谢过程被用于防御性化学生物合成。我们的结果揭示了甲酸在甲虫防御腺中生物合成的潜在机制,并为进一步研究昆虫基于甲酸的化学防御策略的进化提供了基础。
Of the approximately one million described insect species, ground beetles (Coleoptera: Carabidae) have long captivated the attention of evolutionary biologists due to the diversity of defensive compounds they synthesize. Produced using defensive glands in the abdomen, ground beetle chemicals represent over 250 compounds including predator-deterring formic acid, which has evolved as a defensive strategy at least three times across Insecta. Despite being a widespread method of defense, formic acid biosynthesis is poorly understood in insects. Previous studies have suggested that the folate cycle of one-carbon (C1) metabolism, a pathway involved in nucleotide biosynthesis, may play a key role in defensive-grade formic acid production in ants. Here, we report on the defensive gland transcriptome of the formic acid-producing ground beetleHarpalus pensylvanicus. The full suite of genes involved in the folate cycle of C1 metabolism are significantly differentially expressed in the defensive glands ofH. pensylvanicuswhen compared to gene expression profiles in the rest of the body. We also find support for two additional pathways potentially involved in the biosynthesis of defensive-grade formic acid, the kynurenine pathway and the methionine salvage cycle. Additionally, we have found an array of differentially expressed genes in the secretory lobes involved in the biosynthesis and transport of cofactors necessary for formic acid biosynthesis, as well as genes presumably involved in the detoxification of secondary metabolites including formic acid. We also provide insight into the evolution of the predominant gene family involved in the folate cycle (MTHFD) and suggest that high expression of folate cycle genes rather than gene duplication and/or neofunctionalization may be more important for defensive-grade formic acid biosynthesis inH. pensylvanicus. This provides the first evidence in Coleoptera and one of a few examples in Insecta of a primary metabolic process being co-opted for defensive chemical biosynthesis. Our results shed light on potential mechanisms of formic acid biosynthesis in the defensive glands of a ground beetle and provide a foundation for further studies into the evolution of formic acid-based chemical defense strategies in insects.