MAPK-dependent hormonal signaling plasticity contributes to overcoming Bacillus thuringiensis toxin action in an insect host

• Published in: Nature communications Vol. 11; no. 1; pp. 3003 - 14
• Main Authors: Guo, Zhaojiang, Kang, Shi, Sun, Dan, Gong, Lijun, Zhou, Junlei, Qin, Jianying, Guo, Le, Zhu, Liuhong, Bai, Yang, Ye, Fan, Wu, Qingjun, Wang, Shaoli, Crickmore, Neil, Zhou, Xuguo, Zhang, Youjun
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 12-06-2020; Nature Publishing Group; Nature Portfolio
• Subjects: 13/1; 13/109; 13/89; 13/95; 14/19; 38/39; 38/91; 45/77; 631/250/516; 631/326/41/1319; 631/45/776/1176; 631/601/1466; 82/58; 82/80; Aminopeptidase; Animals; Bacillus thuringiensis; Bacillus thuringiensis - metabolism; Bacillus thuringiensis - physiology; Bacillus thuringiensis Toxins; Bacterial Proteins - metabolism; Bacterial Toxins - metabolism; Butterflies & moths; CD13 Antigens - classification; CD13 Antigens - genetics; CD13 Antigens - metabolism; Crosstalk; Endotoxins - metabolism; Gene Expression Regulation; Hemolysin Proteins - metabolism; Hormones; Host-Pathogen Interactions; Humanities and Social Sciences; Insect Hormones - metabolism; Insect Proteins - classification; Insect Proteins - genetics; Insect Proteins - metabolism; Insecticide Resistance - genetics; Insects; Juvenile hormones; MAP kinase; Midgut; Mitogen-Activated Protein Kinases - metabolism; Moths - genetics; Moths - metabolism; Moths - microbiology; multidisciplinary; Pathogens; Pest resistance; Pests; Phylogeny; Physiology; Plastic properties; Plasticity; Science; Science (multidisciplinary); Sf9 Cells; Signal Transduction; Signaling; Spodoptera; Toxins; Virulence
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-020-16608-8

The arms race between entomopathogenic bacteria and their insect hosts is an excellent model for decoding the intricate coevolutionary processes of host-pathogen interaction. Here, we demonstrate that the MAPK signaling pathway is a general switch to
trans
-regulate differential expression of aminopeptidase N and other midgut genes in an insect host, diamondback moth (
Plutella xylostella
), thereby countering the virulence effect of
Bacillus thuringiensis
(Bt) toxins. Moreover, the MAPK cascade is activated and fine-tuned by the crosstalk between two major insect hormones, 20-hydroxyecdysone (20E) and juvenile hormone (JH) to elicit an important physiological response (i.e. Bt resistance) without incurring the significant fitness costs often associated with pathogen resistance. Hormones are well known to orchestrate physiological trade-offs in a wide variety of organisms, and our work decodes a hitherto undescribed function of these classic hormones and suggests that hormonal signaling plasticity is a general cross-kingdom strategy to fend off pathogens.
Bacillus thuringiensis
(Bt) is an important bioinsecticide, but high-level resistance has been rapidly evolving in agricultural pests. Here, Guo et al. show that the MAPK cascade can be activated by enhanced upstream insect hormone signals to counter Bt virulence in the diamondback moth.