Tolerance to dietary linalool primarily involves co-expression of cytochrome P450s and cuticular proteins in Pagiophloeus tsushimanus (Coleoptera: Curculionidae) larvae using SMRT sequencing and RNA-seq

• Published in: BMC genomics Vol. 24; no. 1; p. 34
• Main Authors: Li, Shouyin, Li, Hui, Chen, Cong, Hao, Dejun
• Format: Journal Article
• Language: English
• Published: England BioMed Central Ltd 19-01-2023; BioMed Central; BMC
• Subjects: Alternative splicing; Analysis; Animals; Annotations; Beetles; Camphor; Camphor trees; Co-expression networks analysis; Coleoptera; Coleoptera - genetics; Curculionidae; Cytochrome; Cytochrome P-450; Cytochrome P-450 Enzyme System - genetics; Cytochromes; Damage localization; Diet; Digestive enzymes; DNA sequencing; Ecological effects; Food and nutrition; Gene expression; Gene Expression Profiling; Genetic aspects; Genomes; Genomics; Heat shock proteins; Herbivores; Host adaptation; Influence; Information processing; Insecticides; Insects; Juvenile hormones; Larva - genetics; Larvae; Linalool; Metabolites; Non-coding RNA; Pest outbreaks; Pests; Physiological effects; Physiology; Phytochemicals; Plant metabolites; Plant-pathogen relationships; Proteins; Reactive oxygen species; Real time; Ribonucleic acid; RNA; RNA sequencing; RNA, Long Noncoding - genetics; RNA-Seq; Simple sequence repeats; Single-molecule real-time sequencing; Specialist pest; Splicing; Terpenoid-derived metabolites; Transcription factors; Transcriptome; Transcriptomes; Trees; Varieties; Weevils - genetics; China; Camphor trees; Terpenoid-derived metabolites; Co-expression networks analysis; Specialist pest; Host adaptation; Single-molecule real-time sequencing
• ISSN: 1471-2164; 1471-2164
• DOI: 10.1186/s12864-023-09117-7

Pagiophloeus tsushimanus (Coleoptera: Curculionidae), an emerging forest pest exclusively infesting camphor trees, has recently caused severe ecological and economic damage in localized areas in China. Its population outbreak depends largely on the capacity to overcome the pressure of terpenoid-derived metabolites (e.g. linalool) from camphor trees. At present, the molecular basis of physiological adaptation of P. tsushimanus to dietary linalool is poorly understood, and there is no available reference genome or transcriptome.
Herein, we constructed the transcriptome profiling of P. tsushimanus larvae reared on linalool-infused diets using RNA sequencing and single-molecule real-time sequencing. A total of 20,325 high-quality full-length transcripts were identified as a reference transcriptome, of which 14,492 protein-coding transcripts including 130 transcription factors (TFs), and 5561 long non-coding RNAs (lncRNAs) were detected. Also, 30 alternative splicing events and 8049 simple sequence repeats were captured. Gene ontology enrichment of differential expressed transcripts revealed that overall up-regulation of both cytochrome P450s (CYP450s) and cuticular proteins (CPs), was the primary response characteristic against dietary linalool. Other physiological effects possibly caused by linalool exposure, such as increase in Reactive Oxygen Species (ROS) and hormetic stimulation, were compensated by a handful of induced genes encoding antioxidases, heat shock proteins (HSPs), juvenile hormone (JH) epoxide hydrolases, and digestive enzymes. Additionally, based on co-expression networks analysis, a diverse array of hub lncRNAs and TFs co-expressed with CYP450s and CPs were screened as the potential gene regulators. Temporal expression of candidate transcripts determined by quantitative real-time PCR also indicated a cooperative relationship between the inductions of CYP450s and CPs upon exposure to linalool.
Our present study provides an important transcriptome resource of P. tsushimanus, and lays a valuable foundation for understanding how this specialist pest copes with chemical challenges in its specific host environments.