Coding and Non-coding RNAs: Molecular Basis of Forest-Insect Outbreaks.

Sufang Zhang,Zhang Zhen,Fu Liu,Zhongwu Yang,Sifan Shen,Xiangbo Kong

doi:10.3389/fcell.2020.00369

Abstract

Insect population dynamics are closely related to ‘human’ ecological and economic environments, and a central focus of research is outbreaks. However, the lack of molecular-based investigations restricts our understanding of the intrinsic mechanisms responsible for insect outbreaks. In this context, the moth Dendrolimus punctatus Walker can serve as an ideal model species for insect population dynamics research because it undergoes periodic outbreaks. Here, high-throughput whole-transcriptome sequencing was performed using D. punctatus, sampled during latent and outbreak periods, to systemically explore the molecular basis of insect outbreaks and to identify the involved non-coding RNA (ncRNA) regulators, namely microRNAs, long non-coding RNAs, and circular RNAs. Differentially expressed mRNAs of D. punctatus from different outbreak periods were involved in developmental, reproductive, immune, and chemosensory processes; results that were consistent with the physiological differences in D. punctatus during differing outbreak periods. Targets analysis of the non-coding RNAs indicated that long non-coding RNAs could be the primary ncRNA regulators of D. punctatus outbreaks, while circular RNAs mainly regulated synapses and cell junctions. The target genes of differentially expressed microRNAs mainly regulated the metabolic and reproductive pathways during the D. punctatus outbreaks. Developmental, multi-organismal, and reproductive processes, as well as biological adhesion, characterized the competing endogenous RNA network. Chemosensory and immune genes closely related to the outbreak of D. punctatus were further analyzed in detail: from their ncRNA regulators’ analysis, we deduce that both lncRNA and miRNA may play significant roles. This is the first report to examine the molecular basis of coding and non-coding RNAs’ roles in insect outbreaks. The results provide potential biomarkers for control targets in forest insect management, as well as fresh insights into underlying outbreak-related mechanisms, which could be used for improving insect control strategies in the future.

Highlights

As the most abundant and diverse animals on earth, insects play important roles in ecosystems, and their population dynamics are closely related to humans’ ecological and economic environments
The low-density insects was collected from an area where less than 10% of the trees were damaged by D. punctatus, and the insects were rare on the damaged trees; the high-density insects was collected from an area where more than 80% of the trees were damaged by D. punctatus; many insects were visible on these pine tree and so they were easy to collect
The results indicated that the physiological differences between low- and high-density D. punctatus matched well to the functions of identified differentially expressed genes (DEGs)

Summary

Introduction

As the most abundant and diverse animals on earth, insects play important roles in ecosystems, and their population dynamics are closely related to humans’ ecological and economic environments. In the same habitat, only small numbers of species may undergo an outbreak, while most of the other co-occurring species maintain low and stable population sizes within the community (Alison, 1991). This indicates that outbreaking species may respond to changes in biological and/or abiotic factors differently from that of non-outbreaking species, and the former may have an intrinsic motivation differing from the latter (Myers, 1993). The physiological responses of outbreak species to some factors have been heavily researched (Berryman, 1988; Veran et al, 2015); the molecular basis of these responses is still unclear, which limits our understanding of the intrinsic mechanisms responsible for insect outbreaks

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Discussion

Conclusion