Transcriptome Profiling Reveals a Novel Mechanism of Antiviral Immunity Upon Sacbrood Virus Infection in Honey Bee Larvae (Apis cerana)

The honey bee is one of the most important pollinators in the agricultural system and is responsible for pollinating a third of all food we eat. Sacbrood virus (SBV) is a member of the virus family Iflaviridae and affects honey bee larvae and causes particularly devastating disease in the Asian hone...

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Main Authors: Yulong Guo, Zhengyi Zhang, Mingsheng Zhuang, Liuhao Wang, Kai Li, Jun Yao, Huipeng Yang, Jiaxing Huang, Yue Hao, Fan Ying, Hira Mannan, Jie Wu, Yanping Chen, Jilian Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.615893/full
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language English
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author Yulong Guo
Zhengyi Zhang
Mingsheng Zhuang
Mingsheng Zhuang
Liuhao Wang
Liuhao Wang
Kai Li
Jun Yao
Huipeng Yang
Jiaxing Huang
Yue Hao
Fan Ying
Hira Mannan
Jie Wu
Yanping Chen
Jilian Li
spellingShingle Yulong Guo
Zhengyi Zhang
Mingsheng Zhuang
Mingsheng Zhuang
Liuhao Wang
Liuhao Wang
Kai Li
Jun Yao
Huipeng Yang
Jiaxing Huang
Yue Hao
Fan Ying
Hira Mannan
Jie Wu
Yanping Chen
Jilian Li
Transcriptome Profiling Reveals a Novel Mechanism of Antiviral Immunity Upon Sacbrood Virus Infection in Honey Bee Larvae (Apis cerana)
Frontiers in Microbiology
Apis cerana
Chinese Sacbrood virus
transcriptome
antimicrobial peptides
Sirtuins
author_facet Yulong Guo
Zhengyi Zhang
Mingsheng Zhuang
Mingsheng Zhuang
Liuhao Wang
Liuhao Wang
Kai Li
Jun Yao
Huipeng Yang
Jiaxing Huang
Yue Hao
Fan Ying
Hira Mannan
Jie Wu
Yanping Chen
Jilian Li
author_sort Yulong Guo
title Transcriptome Profiling Reveals a Novel Mechanism of Antiviral Immunity Upon Sacbrood Virus Infection in Honey Bee Larvae (Apis cerana)
title_short Transcriptome Profiling Reveals a Novel Mechanism of Antiviral Immunity Upon Sacbrood Virus Infection in Honey Bee Larvae (Apis cerana)
title_full Transcriptome Profiling Reveals a Novel Mechanism of Antiviral Immunity Upon Sacbrood Virus Infection in Honey Bee Larvae (Apis cerana)
title_fullStr Transcriptome Profiling Reveals a Novel Mechanism of Antiviral Immunity Upon Sacbrood Virus Infection in Honey Bee Larvae (Apis cerana)
title_full_unstemmed Transcriptome Profiling Reveals a Novel Mechanism of Antiviral Immunity Upon Sacbrood Virus Infection in Honey Bee Larvae (Apis cerana)
title_sort transcriptome profiling reveals a novel mechanism of antiviral immunity upon sacbrood virus infection in honey bee larvae (apis cerana)
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2021-06-01
description The honey bee is one of the most important pollinators in the agricultural system and is responsible for pollinating a third of all food we eat. Sacbrood virus (SBV) is a member of the virus family Iflaviridae and affects honey bee larvae and causes particularly devastating disease in the Asian honey bees, Apis cerana. Chinese Sacbrood virus (CSBV) is a geographic strain of SBV identified in China and has resulted in mass death of honey bees in China in recent years. However, the molecular mechanism underlying SBV infection in the Asian honey bee has remained unelucidated. In this present study, we employed high throughput next-generation sequencing technology to study the host transcriptional responses to CSBV infection in A. cerana larvae, and were able to identify genome-wide differentially expressed genes associated with the viral infection. Our study identified 2,534 differentially expressed genes (DEGs) involved in host innate immunity including Toll and immune deficiency (IMD) pathways, RNA interference (RNAi) pathway, endocytosis, etc. Notably, the expression of genes encoding antimicrobial peptides (abaecin, apidaecin, hymenoptaecin, and defensin) and core components of RNAi such as Dicer-like and Ago2 were found to be significantly upregulated in CSBV infected larvae. Most importantly, the expression of Sirtuin target genes, a family of signaling proteins involved in metabolic regulation, apoptosis, and intracellular signaling was found to be changed, providing the first evidence of the involvement of Sirtuin signaling pathway in insects’ immune response to a virus infection. The results obtained from this study provide novel insights into the molecular mechanism and immune responses involved in CSBV infection, which in turn will contribute to the development of diagnostics and treatment for the diseases in honey bees.
topic Apis cerana
Chinese Sacbrood virus
transcriptome
antimicrobial peptides
Sirtuins
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.615893/full
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spelling doaj-8dd7b7b32451449c8d2fb16875ce6eef2021-06-02T15:29:01ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-06-011210.3389/fmicb.2021.615893615893Transcriptome Profiling Reveals a Novel Mechanism of Antiviral Immunity Upon Sacbrood Virus Infection in Honey Bee Larvae (Apis cerana)Yulong Guo0Zhengyi Zhang1Mingsheng Zhuang2Mingsheng Zhuang3Liuhao Wang4Liuhao Wang5Kai Li6Jun Yao7Huipeng Yang8Jiaxing Huang9Yue Hao10Fan Ying11Hira Mannan12Jie Wu13Yanping Chen14Jilian Li15Key Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, ChinaKey Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, ChinaKey Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, ChinaShanghai Suosheng Biotechnology Co., Ltd., Shanghai, ChinaKey Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, ChinaCollege of Resources and Environmental Sciences, Henan Institute of Science and Technology, Xinxiang, ChinaKey Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, ChinaKey Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, ChinaKey Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, ChinaKey Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, ChinaKey Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, ChinaGuizhou Provincial Animal and Poultry Genetic Resources Management Station, Guiyang, ChinaDepartment of Entomology, Faculty of Crop Protection, Sindh Agriculture University, Tando Jam, PakistanKey Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, ChinaUnited States Department of Agriculture (USD) – Agricultural Research Service (ARS) Bee Research Laboratory, Beltsville, MD, United StatesKey Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, ChinaThe honey bee is one of the most important pollinators in the agricultural system and is responsible for pollinating a third of all food we eat. Sacbrood virus (SBV) is a member of the virus family Iflaviridae and affects honey bee larvae and causes particularly devastating disease in the Asian honey bees, Apis cerana. Chinese Sacbrood virus (CSBV) is a geographic strain of SBV identified in China and has resulted in mass death of honey bees in China in recent years. However, the molecular mechanism underlying SBV infection in the Asian honey bee has remained unelucidated. In this present study, we employed high throughput next-generation sequencing technology to study the host transcriptional responses to CSBV infection in A. cerana larvae, and were able to identify genome-wide differentially expressed genes associated with the viral infection. Our study identified 2,534 differentially expressed genes (DEGs) involved in host innate immunity including Toll and immune deficiency (IMD) pathways, RNA interference (RNAi) pathway, endocytosis, etc. Notably, the expression of genes encoding antimicrobial peptides (abaecin, apidaecin, hymenoptaecin, and defensin) and core components of RNAi such as Dicer-like and Ago2 were found to be significantly upregulated in CSBV infected larvae. Most importantly, the expression of Sirtuin target genes, a family of signaling proteins involved in metabolic regulation, apoptosis, and intracellular signaling was found to be changed, providing the first evidence of the involvement of Sirtuin signaling pathway in insects’ immune response to a virus infection. The results obtained from this study provide novel insights into the molecular mechanism and immune responses involved in CSBV infection, which in turn will contribute to the development of diagnostics and treatment for the diseases in honey bees.https://www.frontiersin.org/articles/10.3389/fmicb.2021.615893/fullApis ceranaChinese Sacbrood virustranscriptomeantimicrobial peptidesSirtuins