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

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,...

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Main Authors: Sufang Zhang, Sifan Shen, Zhongwu Yang, Xiangbo Kong, Fu Liu, Zhang Zhen
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-06-01
Series:Frontiers in Cell and Developmental Biology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fcell.2020.00369/full
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author Sufang Zhang
Sifan Shen
Zhongwu Yang
Xiangbo Kong
Fu Liu
Zhang Zhen
author_facet Sufang Zhang
Sifan Shen
Zhongwu Yang
Xiangbo Kong
Fu Liu
Zhang Zhen
author_sort Sufang Zhang
collection DOAJ
description 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.
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spelling doaj.art-f8406c1dabb443f984c1947eca05a7582022-12-22T00:36:39ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2020-06-01810.3389/fcell.2020.00369534063Coding and Non-coding RNAs: Molecular Basis of Forest-Insect OutbreaksSufang Zhang0Sifan Shen1Zhongwu Yang2Xiangbo Kong3Fu Liu4Zhang Zhen5Key Laboratory of Forest Protection of State Forestry and Grassland Administration, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing, ChinaKey Laboratory of Forest Protection of State Forestry and Grassland Administration, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing, ChinaForestry Comprehensive Development Center of Guilin, Guilin, ChinaKey Laboratory of Forest Protection of State Forestry and Grassland Administration, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing, ChinaKey Laboratory of Forest Protection of State Forestry and Grassland Administration, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing, ChinaKey Laboratory of Forest Protection of State Forestry and Grassland Administration, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing, ChinaInsect 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.https://www.frontiersin.org/article/10.3389/fcell.2020.00369/fullforest insectoutbreakwhole-transcriptome sequencinglncRNAceRNA
spellingShingle Sufang Zhang
Sifan Shen
Zhongwu Yang
Xiangbo Kong
Fu Liu
Zhang Zhen
Coding and Non-coding RNAs: Molecular Basis of Forest-Insect Outbreaks
Frontiers in Cell and Developmental Biology
forest insect
outbreak
whole-transcriptome sequencing
lncRNA
ceRNA
title Coding and Non-coding RNAs: Molecular Basis of Forest-Insect Outbreaks
title_full Coding and Non-coding RNAs: Molecular Basis of Forest-Insect Outbreaks
title_fullStr Coding and Non-coding RNAs: Molecular Basis of Forest-Insect Outbreaks
title_full_unstemmed Coding and Non-coding RNAs: Molecular Basis of Forest-Insect Outbreaks
title_short Coding and Non-coding RNAs: Molecular Basis of Forest-Insect Outbreaks
title_sort coding and non coding rnas molecular basis of forest insect outbreaks
topic forest insect
outbreak
whole-transcriptome sequencing
lncRNA
ceRNA
url https://www.frontiersin.org/article/10.3389/fcell.2020.00369/full
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AT sifanshen codingandnoncodingrnasmolecularbasisofforestinsectoutbreaks
AT zhongwuyang codingandnoncodingrnasmolecularbasisofforestinsectoutbreaks
AT xiangbokong codingandnoncodingrnasmolecularbasisofforestinsectoutbreaks
AT fuliu codingandnoncodingrnasmolecularbasisofforestinsectoutbreaks
AT zhangzhen codingandnoncodingrnasmolecularbasisofforestinsectoutbreaks