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

Abstract

Background 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. Results 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. Conclusions 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.

Chromosome-Level Genome Assembly of Papilio elwesi Leech, 1889 (Lepidoptera: Papilionidae)

“…These rapid expansion families included those responsible for cuticle formation (cuticular protein: 17; chitin-binding type-2 domain-containing protein: 15; insect cuticle protein: 7), detoxification metabolism (glutathione S-transferase: 14; cytochrome P450: 5), digestion (trypsin: 11), juvenile hormone synthesis (farnesyl pyrophosphate synthase: 9), chemosensation (gustatory receptor: 8; PBP/GOBP family: 8; odorant receptor: 5), immunity (cecropin family: 7), and so on ( Table S10 , Figure 1 b). We speculate that these expanded families are related to foraging and adaptation to the host plant, as terpenoid-derived metabolites in Lauraceae trees, such as linalool, have recently been reported to act on the expressions of cuticular proteins and cytochrome P450s simultaneously [ 80 ]. The GO and KEGG enrichments of the rapid expansion families further indicate that their functions are involved in detoxification, metabolism, alarm pheromone, and some functions regarding biological processes for which we could not discover the specific meaning ( Figure S3 ).…”

D(+)-Camphor as the key phytochemical cue is promising for the trap monitoring in a new monophagous camphor tree borer Pagiophloeus tsushimanus (Coleoptera: Curculionidae)

“…In our previous study, an interesting phenomenon found during early indoor and eld observation is that P. tsushimanus always has a special preference for C. camphora to other Lauraceae trees (Li et al, 2021). However, it is di cult to establish a stable population on close species (Li et al 2019). At present, the mechanism of host identi cation and location of this pest and key phytochemicals in above process are still unclear.…”

Insecticidal activity and underlying molecular mechanisms of a phytochemical plumbagin against Spodoptera frugiperda

“…Recently, rapid and remarkable developments in sequencing technology and increasing numbers of complete insect genomes have opened up new avenues for exploring global transcriptome changes reflecting the physiological state of insect pests to plant metabolites exposures, unveiling previously unknown mechanisms and mining functional genes (Lin et al, 2023;Li et al, 2023). Huang et al (2018) used RNA-Seq and qPCR to characterize the expression levels of detoxification genes, especially P450 genes in Sitophilus zeamais responding to terpinen-4-ol, the main constituent of Melaleuca alternifolia essential oil.…”

“…Huang et al (2018) used RNA-Seq and qPCR to characterize the expression levels of detoxification genes, especially P450 genes in Sitophilus zeamais responding to terpinen-4-ol, the main constituent of Melaleuca alternifolia essential oil. Li et al (2023) analyzed transcriptome profiling of linalool-exposed Pagiophloeus tsushimanus larvae using RNA-seq and single-molecule real-time sequencing. Gene ontology enrichment of DEGs revealed that overall upregulation of DEGs encoding cytochrome P450s and cuticular proteins was the primary response characteristic in larvae upon exposure to linalool.…”