Nuclear receptor HR3 mediates transcriptional regulation of chitin metabolic genes during molting in Tribolium castaneum

• Published in: Pest management science 2022-10, Vol.78 (10), p.4377-4387
• Main Authors: Kim, Bo‐Eun, Choi, Byungyoon, Park, Woo‐Ram, Kim, Yu‐Ji, Mun, Seulgi, Choi, Hueng‐Sik, Kim, Don‐Kyu
• Format: Article
• Language: English
• Subjects: Beetles; Chemical synthesis; Chitin; chitin metabolic gene; Chromatin; Coordination; Cuticles; Degradation; Epicuticle; Gene expression; Gene regulation; Gene sequencing; Genes; Genomes; HR3; Immunoprecipitation; Insects; Larvae; Metabolism; Molting; Morphogenesis; N-Acetylglucosamine; nuclear receptor; Prepupae; Receptors; Sequence analysis; Transcription; Transcriptomes; Tribolium castaneum
• ISSN: 1526-498X; 1526-4998
• DOI: 10.1002/ps.7056

BACKGROUND Chitin, a major component of insect cuticles, plays a critical role in insect molting and morphogenesis. Thus, coordination of chitin remodeling during insect development requires tight transcriptional control of the chitin metabolism genes involved in chitin synthesis, assembly and degradation. However, the molecular mechanism underlying transcriptional coordination of chitin metabolism genes during beetle development is not yet completely understood. RESULTS We cloned the full‐length cDNA encoding hormone receptor 3 (TcHR3) from Tribolium castaneum and showed a critical role of TcHR3 in modulating chitin metabolism gene expression during molting. Genome‐wide transcriptome analysis of HR3‐deficient old larvae using RNA sequencing analysis revealed a positive correlation between TcHR3 and transcription of chitin metabolism genes involved in chitin synthesis and degradation. In addition, HR3 overexpression significantly induced the gene promoter activity of N‐acetylglucosaminidase 1 (NAG1) involved in chitin degradation and UDP‐N‐acetylglucosamine pyrophosphorylase 1 (UAP1) involved in chitin synthesis. Chromatin immunoprecipitation analysis revealed that HR3 could directly bind to HR3‐response element of NAG1 and UAP1 promoters. Finally, HR3‐deficient late instar larvae and prepupae exhibited defects in larval–larval and larval–pupal molting, respectively, leading to eventual larval death because developing larvae were trapped inside the old cuticle as a result of abnormal chitin metabolism. CONCLUSION TcHR3 is a transcriptional regulator of chitin metabolic genes for molting of T. castaneum. Controlling the molting system by TcHR3 might be a new management strategy for selective control of red flour beetle infestation. © 2022 Society of Chemical Industry. TcHR3 upregulates chitin metabolic gene expression for molting in T. castaneum.