Partner of neuropeptide bursicon homodimer pburs mediates a novel antimicrobial peptide Ten3LP via Dif/Dorsal2 in Tribolium castaneum

Authors: LI, JINGJING - University Of Missouri; BO, LYU - University Of Missouri; BI, JINGXIU - University Of Missouri; SHAN, RUIQI - University Of Missouri; Stanley, David; FENG, QUILI - South China Normal University; SONG, QISHENG - University Of Missouri

Submitted to: International Journal of Biological Macromolecules
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/13/2023
Publication Date: 7/16/2023
Citation: Li, J., Bo, L., Bi, J., Shan, R., Stanley, D.W., Feng, Q., Song, Q. 2023. Partner of neuropeptide bursicon homodimer pburs mediates a novel antimicrobial peptide Ten3LP via Dif/Dorsal2 in Tribolium castaneum. International Journal of Biological Macromolecules. 247. Article 125840. https://doi.org/10.1016/j.ijbiomac.2023.125840.
DOI: https://doi.org/10.1016/j.ijbiomac.2023.125840

Interpretive Summary: Insects protect themselves from lethal infections through a several immune reactions to infections. The problem is that these effective immune reactions can reduce the effectiveness of biological control of pest insect programs that use insect-specific bacteria and fungi to control pests. The insect immune systems can lead to control failures and enormous crop losses. Scientists around the world are working to identify specific targets that reduce the effectiveness of insect immune systems. We carried out research on the red flour beetle, a serious world-wide pest of stored grains. These beetles create tunnels within stored grain that effectively destroys the grain. Because the grain is stored for human food production, classical insecticides cannot be applied. Our work identified a set of genes that signal immune reactions. Blocking expression of these genes disrupted their ability to protect themselves and led to beetle deaths due to infections. These genes now become new targets to reduce populations of red flour beetles. This work will be used by scientists and engineers around the world to develop new red flour beetle-specific pest control technologies. The overall effect will be production of safe, attractive and healthy foods for a growing human population.

Technical Abstract: Bursicon is a cystine knot family neuropeptide, composed of two subunits, burs and partner of burs (pburs) subunits. It can form heterodimers that regulate cuticle sclerotization and wing maturation and homodimers of burs and pburs have been found to signal different biological functions in mediating innate immunity, midgut stem cell proliferation and energy homeostasis, and reproductive physiology in model insects Drosophila melanogaster and Tribolium castaneum, a serious pest of stored grains at the global level. Here, we report on the role of pburs homodimer in signaling innate immunity in larvae of T. castaneum. Through transcriptome analysis we identified a set of immune-related genes that respond to pburs RNAi. Treating larvae with recombinant-pburs (r-pburs) protein led to up-regulation of AMP genes in vivo and in vitro. The upregulation of AMP most genes was working through NF-'B transcription factor Relish. We also report on identification and characterization of a novel AMP, Tenecin 3-like peptide, regulated by pburs via NF-'B transcription factor Dorsal-related immunity factor (Dif)/Drosal2, but not Relish. We conducted Ten3LP RNAi, synthesized a r-Ten3LP and used bacterial inhibition assays to investigate Ten3LP is an AMP specific for fungus and Gram-positive bacterium, activated by pburs via the Toll pathway. These findings identify new molecular targets that may potentially be developed into a novel and necessary stored grain pest management technology.