MAPK Signaling Pathway Alters Expression of Midgut ALP and ABCC Genes and Causes Resistance to Bacillus thuringiensis Cry1Ac Toxin in Diamondback Moth

Authors

Zhaojiang Guo, Chinese Academy of Agricultural Sciences, China
Shi Kang, Chinese Academy of Agricultural Sciences, China
Defeng Chen, Chinese Academy of Agricultural Sciences, China
Qingjun Wu, Chinese Academy of Agricultural Sciences, China
Shaoli Wang, Chinese Academy of Agricultural Sciences, China
Wen Xie, Chinese Academy of Agricultural Sciences, China
Xun Zhu, Chinese Academy of Agricultural Sciences, China
Simon W. Baxter, University of Adelaide, Australia
Xuguo Zhou, University of KentuckyFollow
Juan Luis Jurat-Fuentes, University of Tennessee
Youjun Zhang, Chinese Academy of Agricultural Sciences, China

Abstract

Insecticidal crystal toxins derived from the soil bacterium Bacillus thuringiensis (Bt) are widely used as biopesticide sprays or expressed in transgenic crops to control insect pests. However, large-scale use of Bt has led to field-evolved resistance in several lepidopteran pests. Resistance to Bt Cry1Ac toxin in the diamondback moth, Plutella xylostella (L.), was previously mapped to a multigenic resistance locus (BtR-1). Here, we assembled the 3.15 Mb BtR-1 locus and found high-level resistance to Cry1Ac and Bt biopesticide in four independent P. xylostella strains were all associated with differential expression of a midgut membrane-bound alkaline phosphatase (ALP) outside this locus and a suite of ATP-binding cassette transporter subfamily C (ABCC) genes inside this locus. The interplay between these resistance genes is controlled by a previously uncharacterized trans-regulatory mechanism via the mitogen-activated protein kinase (MAPK) signaling pathway. Molecular, biochemical, and functional analyses have established ALP as a functional Cry1Ac receptor. Phenotypic association experiments revealed that the recessive Cry1Ac resistance was tightly linked to down-regulation of ALP, ABCC2 and ABCC3, whereas it was not linked to up-regulation of ABCC1. Silencing of ABCC2 and ABCC3 in susceptible larvae reduced their susceptibility to Cry1Ac but did not affect the expression of ALP, whereas suppression of MAP4K4, a constitutively transcriptionally-activated MAPK upstream gene within the BtR-1 locus, led to a transient recovery of gene expression thereby restoring the susceptibility in resistant larvae. These results highlight a crucial role for ALP and ABCC genes in field-evolved resistance to Cry1Ac and reveal a novel trans-regulatory signaling mechanism responsible for modulating the expression of these pivotal genes in P. xylostella.

Document Type

Article

Publication Date

4-13-2015

Notes/Citation Information

Published in PLOS Genetics, v. 11, no. 4, article e1005124, p. 1-32.

© 2015 Guo et al.

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

Digital Object Identifier (DOI)

http://dx.doi.org/10.1371/journal.pgen.1005124

Funding Information

This work was supported by the National Natural Science Foundation of China (30871659; 30471159; 31201532), the 863 Program (2012AA101502), the Agricultural Science and Technology Innovation Program, the Beijing Key Laboratory for Pest Control and Sustainable Cultivation of Vegetables, and the Biotechnology Risk Assessment Grant Program competitive grants Nos. 2010-33522-21700 and 2014-33522-22215 from the USDA National Institute of Food and Agriculture. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Repository Citation

Guo, Zhaojiang; Kang, Shi; Chen, Defeng; Wu, Qingjun; Wang, Shaoli; Xie, Wen; Zhu, Xun; Baxter, Simon W.; Zhou, Xuguo; Jurat-Fuentes, Juan Luis; and Zhang, Youjun, "MAPK Signaling Pathway Alters Expression of Midgut ALP and ABCC Genes and Causes Resistance to Bacillus thuringiensis Cry1Ac Toxin in Diamondback Moth" (2015). Entomology Faculty Publications. 87.
https://uknowledge.uky.edu/entomology_facpub/87