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.
Highlights
The potential of insecticide application is fading away worldwide, as their efficacy against insect pests is diminished by the evolution of resistance [1]
The rapid evolution of insect resistance to Bacillus thuringiensis (Bt) insecticidal Cry toxins is frequently associated with reduced expression of diverse midgut genes that code for Cry-toxin receptors
Membrane-bound alkaline phosphatase is a known receptor for Cry1Ac toxin in diverse insects and here, we report the transcriptional regulatory mechanism of the PxmALP gene related to Cry1Ac resistance in P. xylostella
Summary
The potential of insecticide application is fading away worldwide, as their efficacy against insect pests is diminished by the evolution of resistance [1]. Formulations with Bt toxins and transgenic crops expressing Bt insecticidal toxin genes have been widely adopted for pest management worldwide, providing unprecedented economic, ecological, and social benefits [3,4,5,6,7]. The ability of insects to adapt to Bt toxins supports the conclusion that the rapid evolution of resistance by insects is a major threat for the future application and success of Bt-based products [8, 9]. The midgut receptors of Bt toxins include proteins such as cadherin-like (CAD), aminopeptidase-N (APN), alkaline phosphatase (ALP) and ATP-binding cassette (ABC) transporters [12]. The regulatory mechanisms involved in the expression of these midgut receptors are unclear
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