Unveiling gene expression regulation of the Bacillus thuringiensis Cry3Aa toxin receptor ADAM10 by the potato dietary miR171c in Colorado potato beetle

• Published in: Pest management science 2022-09, Vol.78 (9), p.3760-3768
• Main Authors: Robles‐Fort, Aida, Pescador‐Dionisio, Sara, García‐Robles, Inmaculada, Sentandreu, Vicente, Martínez‐Ramírez, Amparo C., Real, M. Dolores, Rausell, Carolina
• Format: Article
• Language: English
• Subjects: ADAM10; Bacillus thuringiensis; Beetles; Colorado potato beetle; Cry3A toxin; dietary miRNAs; Gene expression; Gene regulation; Host plants; Insecticide resistance; Insecticides; Larvae; MicroRNAs; miR171c; miRNA; Nutrition; Pest control; Pests; Plant protection; Potatoes; Receptors; Ribonucleic acid; RNA; Statistical analysis; Tomatoes; Toxicity; Toxins; Vegetables
• ISSN: 1526-498X; 1526-4998
• DOI: 10.1002/ps.6743

BACKGROUND The Colorado potato beetle (CPB) is a worldwide devastating pest of potato plants and other Solanaceae characterized by its remarkable ability to evolve resistance to insecticides. Bacillus thuringiensis (Bt) Cry3Aa toxin represents an environmentally safe alternative for CPB control but larvae susceptibility to this toxin has been reported to vary depending on the host plant on which larvae feed. To gain more insight into how nutrition mediates Bt tolerance through effects on gene expression, here we explored the post‐transcriptional regulation by microRNAs (miRNAs) of the CPB‐ADAM10 gene encoding the Cry3Aa toxin functional receptor ADAM10. RESULTS The lower CPB‐ADAM10 gene expression in CPB larvae fed on potato plants cv. Vivaldi than those fed on potato cv. Monalisa or tomato plants was inversely related to Cry3Aa toxicity. By high‐throughput sequencing we identified seven CPB miRNAs and one potato miRNA predicted to base pair with the CPB‐ADAM10 messenger RNA. No differential expression of the endogenous lde‐miR1175‐5p was found in larvae feeding on any of the two potato plant varieties. However, statistically significant increased amounts of potato stu‐miR171c‐5p were detected in CPB larvae fed on potato cv. Vivaldi compared to larvae fed on potato cv. Monalisa. CONCLUSION Our results support a role for dietary miRNAs in Bt toxicity by regulating the CPB‐ADAM10 gene encoding the Cry3Aa toxin receptor ADAM10 in CPB larvae and opening up the possibility of exploiting plant natural variation in miRNAs to provide more sustainable potato crop protection against CPB. © 2021 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. Increased amounts in CPB larvae midgut of the dietary stu‐miR‐171c‐5p predicted to regulate the Cry3Aa toxin functional receptor CPB‐ADAM10 gene correlated with lower CPB‐ADAM10 gene expression and reduced Cry3Aa toxicity.