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

Journal or Publishing Institution: PLoS Genetics

Study: http://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1005124

Author(s): Guo, Z., Kang, S., Chen, D., Wu, Q., Wang, S., Xie, W., Zhu, X., Baxter, S.W., Zhou, X., Jurat-Fuentes, J.L. and Zhang, Y.

Article Type: Peer Reviewed Study

Record ID: 890

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. xylostellastrains 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 ABCC3in 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.

Keywords: Intestines; Animals; Moths; Bacillus; Alkaline Phosphatase; Bacterial Proteins; ATP-Binding Cassette Transporters; Insect Proteins; Endotoxins; MAP Kinase Signaling System; Protein Binding; Insecticide Resistance; Hemolysin Proteins; Biological Control Agents, Resistance, Cry1Ac toxin, Diamondback moth

Citation: Guo, Z., Kang, S., Chen, D., Wu, Q., Wang, S., Xie, W., Zhu, X., Baxter, S.W., Zhou, X., Jurat-Fuentes, J.L. and Zhang, Y., 2015. MAPK signaling pathway alters expression of midgut ALP and ABCC genes and causes resistance to Bacillus thuringiensis Cry1Ac toxin in diamondback moth. PLoS Genetics, 11(4), p.e1005124.