A midgut transcriptional regulatory loop favors an insect host to withstand a bacterial pathogen

作者：Zhaojiang Guo, Liuhong Zhu, Zhouqiang Cheng, Lina Dong, Le Guo, Yang Bai, Qingjun Wu, Shaoli Wang, Xin Yang, Wen Xie, Neil Crickmore, Xuguo Zhou, René Lafont, Youjun Zhang · 发表于：The Innovation · 年份：2024 · DOI：10.1016/j.xinn.2024.100675 · 被引用次数：23 · 研究领域：Insect Resistance and Genetics、Insect and Arachnid Ecology and Behavior、Insect and Pesticide Research

•Increased titer of the insect hormone 20-hydroxyecdysone (20E) facilitates an insect host, Plutella xylostella, to defeat its bacterial pathogen Bacillus thuringiensis (Bt).•Glucose dehydrogenase (GLD) was identified as a new insect ecdysone-degrading enzyme that can metabolize 20E.•A midgut miRNA initiated epigenetic regulatory pathway represses GLD activity and elevates 20E titer to resist the Bt pathogen.•An as-yet uncharacterized negative feedback loop reduces excess 20E to balance hormonal homeostasis.•This study provides new insights into the immunological landscape of classical insect hormones and the molecular basis of host-pathogen coevolution. Mounting evidence suggests that insect hormones associated with growth and development also participate in pathogen defense. We have discovered a previously undescribed midgut transcriptional control pathway that modulates the availability of 20-hydroxyecdysone (20E) in a worldwide insect pest (Plutella xylostella), allowing it to defeat the major virulence factor of an insect pathogen Bacillus thuringiensis (Bt). A reduction of the transcriptional inhibitor (PxDfd) increases the expression of a midgut microRNA (miR-8545), which in turn represses the expression of a newly identified ecdysteroid-degrading glucose dehydrogenase (PxGLD). Downregulation of PxGLD reduces 20E degradation to increase 20E titer and concurrently triggers a transcriptional negative feedback loop to mitigate 20E overproduction. The moderately elevated 2...