The regulation landscape of MAPK signaling cascade for thwarting Bacillus thuringiensis infection in an insect host.

Zhaojiang Guo,Shaoli Wang,Neil Crickmore,Shi Kang,Alejandra Bravo,Qingjun Wu,Mario Soberón,Youjun Zhang,Xuguo Zhou,Rachel M Mcloughlin

doi:10.1371/journal.ppat.1009917

Abstract

Host-pathogen interactions are central components of ecological networks where the MAPK signaling pathways act as central hubs of these complex interactions. We have previously shown that an insect hormone modulated MAPK signaling cascade participates as a general switch to trans-regulate differential expression of diverse midgut genes in the diamondback moth, Plutella xylostella (L.) to cope with the insecticidal action of Cry1Ac toxin, produced by the entomopathogenic bacterium Bacillus thuringiensis (Bt). The relationship between topology and functions of this four-tiered phosphorylation signaling cascade, however, is an uncharted territory. Here, we carried out a genome-wide characterization of all the MAPK orthologs in P. xylostella to define their phylogenetic relationships and to confirm their evolutionary conserved modules. Results from quantitative phosphoproteomic analyses, combined with functional validations studies using specific inhibitors and dsRNAs lead us to establish a MAPK "road map", where p38 and ERK MAPK signaling pathways, in large part, mount a resistance response against Bt toxins through regulating the differential expression of multiple Cry toxin receptors and their non-receptor paralogs in P. xylostella midgut. These data not only advance our understanding of host-pathogen interactions in agricultural pests, but also inform the future development of biopesticides that could suppress Cry resistance phenotypes.

Highlights

Plants and animals live in an environment teeming with multiple pathogens, and have evolved strategies to withstand pathogen attack
We have previously shown that an insect hormone modulated mitogen-activated protein kinase (MAPK) signaling cascade participates as a general switch to trans-regulate differential expression of diverse midgut genes in the diamondback moth, Plutella xylostella (L.) to cope with the insecticidal action of Cry1Ac toxin, produced by the entomopathogenic bacterium Bacillus thuringiensis (Bt)
The MAPK “road map” to overcome Bt toxin in diamondback moth were deposited in the GenBank database

Summary

Introduction

Plants and animals live in an environment teeming with multiple pathogens, and have evolved strategies to withstand pathogen attack. Defense responses through activation of signaling pathways, from pathogen recognition to the induction of immune responses, are crucial in host-pathogen interactions [1,2]. The mitogen-activated protein kinase (MAPK) signaling pathways play crucial roles in the arms race between host and pathogen [3]. The contribution of MAPK signaling cascades in controlling cellular responses to a wide assortment of stimuli and in regulating cellular processes from gene expression to cell death is well established [6]. The largest group of animals on earth, can be infected by a wide range of pathogens, including bacteria, fungi, viruses and parasites [7]. Insect pests have developed intricate strategies to counteract the detrimental effects caused by Bt toxins, defining these molecular mechanisms evolved in insect hosts to counteract Bt infection is pivotal to establish successful strategies to counter insect resistance to Bt toxins [18,19,20,21,22,23]

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