MAPK-Mediated Transcription Factor GATAd Contributes to Cry1Ac Resistance in Diamondback Moth by Reducing PxmALP Expression

Authors

Le Guo, Hunan Agricultural University, China
Zhouqiang Cheng, Hunan Agricultural University, China
Jianying Qin, Chinese Academy of Agricultural Sciences, China
Dan Sun, Chinese Academy of Agricultural Sciences, China
Shaoli Wang, Chinese Academy of Agricultural Sciences, China
Qingjun Wu, Chinese Academy of Agricultural Sciences, China
Neil Crickmore, University of Sussex, UK
Xuguo Zhou, University of KentuckyFollow
Alejandra Bravo, Universidad Nacional Autónoma de México, Mexico
Mario Soberón, Universidad Nacional Autónoma de México, Mexico
Zhaojiang Guo, Chinese Academy of Agricultural Sciences, China
Youjun Zhang, Chinese Academy of Agricultural Sciences, China

Abstract

The benefits of biopesticides and transgenic crops based on the insecticidal Cry-toxins from Bacillus thuringiensis (Bt) are considerably threatened by insect resistance evolution, thus, deciphering the molecular mechanisms underlying insect resistance to Bt products is of great significance to their sustainable utilization. Previously, we have demonstrated that the down-regulation of PxmALP in a strain of Plutella xylostella (L.) highly resistant to the Bt Cry1Ac toxin was due to a hormone-activated MAPK signaling pathway and contributed to the resistance phenotype. However, the underlying transcriptional regulatory mechanism remains enigmatic. Here, we report that the PxGATAd transcription factor (TF) is responsible for the differential expression of PxmALP observed between the Cry1Ac susceptible and resistant strains. We identified that PxGATAd directly activates PxmALP expression via interacting with a non-canonical but specific GATA-like cis-response element (CRE) located in the PxmALP promoter region. A six-nucleotide insertion mutation in this cis-acting element of the PxmALP promoter from the resistant strain resulted in repression of transcriptional activity, affecting the regulatory performance of PxGATAd. Furthermore, silencing of PxGATAd in susceptible larvae reduced the expression of PxmALP and susceptibility to Cry1Ac toxin. Suppressing PxMAP4K4 expression in the resistant larvae transiently recovered both the expression of PxGATAd and PxmALP, indicating that the PxGATAd is a positive responsive factor involved in the activation of PxmALP promoter and negatively regulated by the MAPK signaling pathway. Overall, this study deciphers an intricate regulatory mechanism of PxmALP gene expression and highlights the concurrent involvement of both trans-regulatory factors and cis-acting elements in Cry1Ac resistance development in lepidopteran insects.

Document Type

Article

Publication Date

2-3-2022

Notes/Citation Information

Published in PLOS Genetics, v. 18, issue 2, 1010037.

© 2022 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)

https://doi.org/10.1371/journal.pgen.1010037

Funding Information

This work was supported by the Laboratory of Lingnan Modern Agriculture Project (NT2021003) to YZ, the National Natural Science Foundation of China (32022074; 32172458) to ZG, the Beijing Key Laboratory for Pest Control and Sustainable Cultivation of Vegetables and the Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences (CAAS-ASTIP-IVFCAAS) to YZ.

Related Content

The final cloned full-length cDNA sequence of P. xylostella GATAd gene was deposited in the GenBank database (accession no. MZ712004). The raw data of the figures and statistical analyses in this study are provided in S1 Data.

Repository Citation

Guo, Le; Cheng, Zhouqiang; Qin, Jianying; Sun, Dan; Wang, Shaoli; Wu, Qingjun; Crickmore, Neil; Zhou, Xuguo; Bravo, Alejandra; Soberón, Mario; Guo, Zhaojiang; and Zhang, Youjun, "MAPK-Mediated Transcription Factor GATAd Contributes to Cry1Ac Resistance in Diamondback Moth by Reducing PxmALP Expression" (2022). Entomology Faculty Publications. 234.
https://uknowledge.uky.edu/entomology_facpub/234