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

Pest Manag Sci. 2023 May;79(5):1660-1673. doi: 10.1002/ps.7337. Epub 2023 Jan 12.

Abstract

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.

Keywords: Holotrichia parallela; antioxidant enzyme; bacillus thuringiensis; detoxifying enzyme; entomopathogenic nematode.

MeSH terms

  • Animals
  • Antioxidants / metabolism
  • Bacillus thuringiensis* / genetics
  • Coleoptera* / physiology
  • Kelch-Like ECH-Associated Protein 1 / metabolism
  • Larva / metabolism
  • NF-E2-Related Factor 2 / metabolism
  • Nematoda*
  • Phosphatidylinositol 3-Kinase / metabolism
  • Phosphatidylinositol 3-Kinases / metabolism
  • Proto-Oncogene Proteins c-akt / genetics
  • Proto-Oncogene Proteins c-akt / metabolism
  • Signal Transduction

Substances

  • Proto-Oncogene Proteins c-akt
  • Phosphatidylinositol 3-Kinases
  • Kelch-Like ECH-Associated Protein 1
  • Phosphatidylinositol 3-Kinase
  • Antioxidants
  • NF-E2-Related Factor 2