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

Zhaojiang Guo,Lijun Gong,Jianying Qin,Shi Kang,Shaoli Wang,Junlei Zhou,Liuhong Zhu,Xuguo Zhou,Dan Sun,Le Guo,Qingjun Wu,Yang Bai,Fan Ye,Youjun Zhang,Neil Crickmore

doi:10.1038/s41467-020-16608-8

Abstract

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.

Highlights

The arms race between entomopathogenic bacteria and their insect hosts is an excellent model for decoding the intricate coevolutionary processes of host-pathogen interaction
Based on currently available transcriptome and genome databases of P. xylostella, 18 M1 aminopeptidase genes including 15 aminopeptidase N (APN) genes were identified in silico, and their full-length cDNA sequences were successfully cloned except for PxAPN3b (Supplementary Table 1 and Supplementary Fig. 1a)
We found that the APN1-12 gene cluster possesses highly conserved synteny in both gene order and orientation in different lepidopteran insects, indicating that it has undergone tandem gene duplication during insect genome evolution (Fig. 1a)

Summary

Introduction

The arms race between entomopathogenic bacteria and their insect hosts is an excellent model for decoding the intricate coevolutionary processes of host-pathogen interaction. 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. APN proteins are a class of endoproteases catalyzing the cleavage of neutral amino acids from the N-terminus of protein or polypeptide substrates[30] They belong to the M1 family (metallo-type) of zinc-dependent aminopeptidases that are implicated in many physiological processes of diverse organisms[31]. Whether the differential expression of these PxAPN genes associated with Cry1Ac resistance was trans-regulated by the MAPK cascade in P

Methods

Results

Conclusion