JAK/STAT signaling regulated intestinal regeneration defends insect pests against pore-forming toxins produced by Bacillus thuringiensis

• Published in: PLoS pathogens Vol. 20; no. 1; p. e1011823
• Main Authors: Wang, Zeyu, Yang, Yanchao, Li, Sirui, Ma, Weihua, Wang, Kui, Soberón, Mario, Yan, Shuo, Shen, Jie, Francis, Frederic, Bravo, Alejandra, Zhang, Jie
• Format: Journal Article Web Resource
• Language: English
• Published: United States Public Library of Science 18.01.2024; Public Library of Science (PLoS)
• Subjects: Agrochemicals; Analysis; Apoptosis; Bacillus thuringiensis; Biological control; Biology and Life Sciences; Biopesticides; Cell cycle; Cell differentiation; Cell proliferation; Chemical pest control; Crop diseases; Crops; Defense mechanisms; Double-stranded RNA; Effectiveness; Entomologie & lutte antiravageur; Entomology & pest control; Epithelium; Gastrointestinal tract; Gene expression; Genes; Health aspects; Insect pests; Insects; Intestine; Intoxication; Kinases; Larvae; Life sciences; Ligands; Medicine and Health Sciences; Nanoparticles; Pest control; Pesticides; Pests; Plant diseases; Pore formation; Prevention; Proteins; Regeneration; Rice; Risk factors; RNA interference; Sciences du vivant; STAT signalling; Stem cells; Sublethal dosage; Toxicity; Toxins; Transcription factors; Tyrosine; China
• ISSN: 1553-7374; 1553-7366; 1553-7374
• DOI: 10.1371/journal.ppat.1011823

A variety of coordinated host-cell responses are activated as defense mechanisms against pore-forming toxins (PFTs). Bacillus thuringiensis (Bt) is a worldwide used biopesticide whose efficacy and precise application methods limits its use to replace synthetic pesticides in agricultural settings. Here, we analyzed the intestinal defense mechanisms of two lepidopteran insect pests after intoxication with sublethal dose of Bt PFTs to find out potential functional genes. We show that larval intestinal epithelium was initially damaged by the PFTs and that larval survival was observed after intestinal epithelium regeneration. Further analyses showed that the intestinal regeneration caused by Cry9A protein is regulated through c-Jun NH (2) terminal kinase (JNK) and Janus tyrosine kinase/signal transducer and activator of transcription (JAK/STAT) signaling pathways. JAK/STAT signaling regulates intestinal regeneration through proliferation and differentiation of intestinal stem cells to defend three different Bt proteins including Cry9A, Cry1F or Vip3A in both insect pests, Chilo suppressalis and Spodoptera frugiperda . Consequently, a nano-biopesticide was designed to improve pesticidal efficacy based on the combination of Stat double stranded RNA (dsRNA)-nanoparticles and Bt strain. This formulation controlled insect pests with better effect suggesting its potential use to reduce the use of synthetic pesticides in agricultural settings for pest control.