PI3K/Akt/CncC signaling pathway mediates the response to EPN‐Bt infection in Holotrichia parallela larvae

• Published in: Pest management science Vol. 79; no. 5; pp. 1660 - 1673
• Main Authors: Li, Er‐Tao, Wu, Han‐Jia, Wang, Zhi‐Min, Li, Ke‐Bin, Zhang, Shuai, Cao, Ya‐Zhong, Yin, Jiao
• Format: Journal Article
• Language: English
• Published: Chichester, UK John Wiley & Sons, Ltd 01.05.2023; Wiley Subscription Services, Inc
• Subjects: 1-Phosphatidylinositol 3-kinase; Acetylcholinesterase; AKT protein; Animals; antioxidant enzyme; Antioxidants; Antioxidants - metabolism; bacillus thuringiensis; Bacillus thuringiensis - genetics; Biological control; Coleoptera - physiology; detoxifying enzyme; entomopathogenic nematode; Entomopathogenic nematodes; Enzymatic activity; Enzymes; Exposure; Gene sequencing; Holotrichia parallela; Infections; Kelch-Like ECH-Associated Protein 1 - metabolism; Kinases; Larva - metabolism; Larvae; Midgut; Nematoda; NF-E2-Related Factor 2 - metabolism; Pest control; Phosphatidylinositol 3-Kinase - metabolism; Phosphatidylinositol 3-Kinases - metabolism; Proteins; Proto-Oncogene Proteins c-akt - genetics; Proto-Oncogene Proteins c-akt - metabolism; RNA-mediated interference; Signal Transduction; Signaling; antioxidant enzyme; entomopathogenic nematode; Holotrichia parallela; detoxifying enzyme; bacillus thuringiensis
• ISSN: 1526-498X; 1526-4998
• DOI: 10.1002/ps.7337

Background Combining the entomopathogenic nematode (EPN), Heterorhabditis beicherriana LF strain, and Bacillus thuringiensis (Bt) HBF‐18 strain is a practical strategy to manage the larvae of Holotrichia parallela Motschulsky (white grubs). However, the mechanisms underlying the larval defense response to this combined biocontrol strategy are unknown. Results The activities of some antioxidant enzymes (SOD, POD, CAT) and some detoxifying enzymes (AChE, P‐450, CarE, GST) in grubs showed an activation–inhibition trend throughout the EPN‐Bt exposure time course. Eight potentially key antioxidant and detoxifying enzyme genes in response to EPN‐Bt infection were identified from the midgut of grubs through RNA sequencing. After silencing CAT, CarE18, and GSTs1, the enzyme activities were significantly decreased by 30.29%, 68.80%, and 34.63%, respectively. Meanwhile, the mortality of grubs was increased by 18.40%, 46.30%, and 42.59% after exposure to EPN‐Bt for 1 day. Interestingly, the PI3K/Akt signaling pathway was significantly enriched in KEGG enrichment analysis, and the expression levels of phosphatidylinositol 3‐kinase (PI3K), protein kinase B (Akt), cap ‘n’ collar isoform‐C (CncC), kelch‐like ECH‐associated protein 1 (Keap1), and CarE18 were all up‐regulated when exposed to EPN‐Bt for 1 day. Furthermore, RNAi‐mediated PI3K silencing showed a similar down‐regulated trend between PI3K/Akt/CncC and CarE18. Moreover, silencing PI3K rendered grubs more susceptible to EPN‐Bt and accelerated symbiotic bacteria multiplication in grubs. Conclusion These results suggest that the PI3K/Akt/CncC pathway mediates the expression of CarE18 and participates in the defense response of H. parallela larvae against EPN‐Bt infection. Our data provide valuable insights into the design of appropriate management strategies for this well‐known agricultural pest. © 2022 Society of Chemical Industry. The expression of Heterorhabditis parallela CarE was regulated by the PI3K/Akt/CncC pathway, and this pathway was participate in the defense response to EPN‐Bt infection.