Insight into the regulation of the Nrf2 pathway in response to ascovirus infection in Spodoptera exigua

BACKGROUND Ascoviruses are a type of entomopathogenic microorganism with high biological pest control potential and are expected to contribute to the natural control of lepidopteran pests. However, knowledge of the molecular mechanism underlying the biocidal activity of ascovirus on its host insects...

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Veröffentlicht in:Pest management science 2023-03, Vol.79 (3), p.1123-1130
Hauptverfasser: Jin, Ruoheng, Xiao, Zhengkun, Nakai, Madoka, Huang, Guo‐Hua
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Xiao, Zhengkun
Nakai, Madoka
Huang, Guo‐Hua
description BACKGROUND Ascoviruses are a type of entomopathogenic microorganism with high biological pest control potential and are expected to contribute to the natural control of lepidopteran pests. However, knowledge of the molecular mechanism underlying the biocidal activity of ascovirus on its host insects remains limited. RESULTS In this study, the relative enzyme activity of superoxide dismutase and peroxidase, as well as the expression level of Spodoptera exigua peroxidase (SePOD), were found to be significantly increased at 6 h post infection with Heliothis virescens ascovirus 3h (HvAV‐3h). H2O2 accumulation and enhanced expression of NADPH Oxidase (SeNOX) were also observed. In addition, Nuclear Factor erythroid 2‐Related Factor 2 (SeNrf2) and muscle aponeurosis fibromatosis (SeMaf) were overexpressed following infection with HvAV‐3h. Silencing of SeNrf2 decreased the expression of SePOD, whereas the mortality of SeNrf2‐silenced larvae and viral genome copy number also increased. Further RNA interference of SeNOX significantly decreased expression of SeNrf2 and SePOD and therefore increased the mortality and viral genome copy number of the ascovirus‐infected host. CONCLUSION The HvAV‐3h activated Nrf2/ARE pathway of S. exigua and reactive oxygen species were found to respond to ascovirus infection by regulating alterations in antioxidant enzyme genes mediated by the host Nrf2/ARE pathway. These findings enhance our knowledge of ascovirus–host interactions and lay the foundation for the application of ascoviruses in biological pest control. © 2022 Society of Chemical Industry. This study demonstrated an antioxidant system in hosts dealing with ascovirus infection. In response to reactive oxygen species damage caused by Heliothis virescens ascovirus 3h, Nrf2/ARE pathway‐mediated overexpression of antioxidant enzyme genes activates the antioxidative defense system for their own protection in Spodoptera exigua larvae.
doi_str_mv 10.1002/ps.7284
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However, knowledge of the molecular mechanism underlying the biocidal activity of ascovirus on its host insects remains limited. RESULTS In this study, the relative enzyme activity of superoxide dismutase and peroxidase, as well as the expression level of Spodoptera exigua peroxidase (SePOD), were found to be significantly increased at 6 h post infection with Heliothis virescens ascovirus 3h (HvAV‐3h). H2O2 accumulation and enhanced expression of NADPH Oxidase (SeNOX) were also observed. In addition, Nuclear Factor erythroid 2‐Related Factor 2 (SeNrf2) and muscle aponeurosis fibromatosis (SeMaf) were overexpressed following infection with HvAV‐3h. Silencing of SeNrf2 decreased the expression of SePOD, whereas the mortality of SeNrf2‐silenced larvae and viral genome copy number also increased. Further RNA interference of SeNOX significantly decreased expression of SeNrf2 and SePOD and therefore increased the mortality and viral genome copy number of the ascovirus‐infected host. CONCLUSION The HvAV‐3h activated Nrf2/ARE pathway of S. exigua and reactive oxygen species were found to respond to ascovirus infection by regulating alterations in antioxidant enzyme genes mediated by the host Nrf2/ARE pathway. These findings enhance our knowledge of ascovirus–host interactions and lay the foundation for the application of ascoviruses in biological pest control. © 2022 Society of Chemical Industry. This study demonstrated an antioxidant system in hosts dealing with ascovirus infection. 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However, knowledge of the molecular mechanism underlying the biocidal activity of ascovirus on its host insects remains limited. RESULTS In this study, the relative enzyme activity of superoxide dismutase and peroxidase, as well as the expression level of Spodoptera exigua peroxidase (SePOD), were found to be significantly increased at 6 h post infection with Heliothis virescens ascovirus 3h (HvAV‐3h). H2O2 accumulation and enhanced expression of NADPH Oxidase (SeNOX) were also observed. In addition, Nuclear Factor erythroid 2‐Related Factor 2 (SeNrf2) and muscle aponeurosis fibromatosis (SeMaf) were overexpressed following infection with HvAV‐3h. Silencing of SeNrf2 decreased the expression of SePOD, whereas the mortality of SeNrf2‐silenced larvae and viral genome copy number also increased. Further RNA interference of SeNOX significantly decreased expression of SeNrf2 and SePOD and therefore increased the mortality and viral genome copy number of the ascovirus‐infected host. CONCLUSION The HvAV‐3h activated Nrf2/ARE pathway of S. exigua and reactive oxygen species were found to respond to ascovirus infection by regulating alterations in antioxidant enzyme genes mediated by the host Nrf2/ARE pathway. These findings enhance our knowledge of ascovirus–host interactions and lay the foundation for the application of ascoviruses in biological pest control. © 2022 Society of Chemical Industry. This study demonstrated an antioxidant system in hosts dealing with ascovirus infection. 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However, knowledge of the molecular mechanism underlying the biocidal activity of ascovirus on its host insects remains limited. RESULTS In this study, the relative enzyme activity of superoxide dismutase and peroxidase, as well as the expression level of Spodoptera exigua peroxidase (SePOD), were found to be significantly increased at 6 h post infection with Heliothis virescens ascovirus 3h (HvAV‐3h). H2O2 accumulation and enhanced expression of NADPH Oxidase (SeNOX) were also observed. In addition, Nuclear Factor erythroid 2‐Related Factor 2 (SeNrf2) and muscle aponeurosis fibromatosis (SeMaf) were overexpressed following infection with HvAV‐3h. Silencing of SeNrf2 decreased the expression of SePOD, whereas the mortality of SeNrf2‐silenced larvae and viral genome copy number also increased. Further RNA interference of SeNOX significantly decreased expression of SeNrf2 and SePOD and therefore increased the mortality and viral genome copy number of the ascovirus‐infected host. CONCLUSION The HvAV‐3h activated Nrf2/ARE pathway of S. exigua and reactive oxygen species were found to respond to ascovirus infection by regulating alterations in antioxidant enzyme genes mediated by the host Nrf2/ARE pathway. These findings enhance our knowledge of ascovirus–host interactions and lay the foundation for the application of ascoviruses in biological pest control. © 2022 Society of Chemical Industry. This study demonstrated an antioxidant system in hosts dealing with ascovirus infection. In response to reactive oxygen species damage caused by Heliothis virescens ascovirus 3h, Nrf2/ARE pathway‐mediated overexpression of antioxidant enzyme genes activates the antioxidative defense system for their own protection in Spodoptera exigua larvae.</abstract><cop>Chichester, UK</cop><pub>John Wiley &amp; Sons, Ltd</pub><pmid>36349417</pmid><doi>10.1002/ps.7284</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0002-6841-0095</orcidid></addata></record>
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source MEDLINE; Wiley Online Library Journals Frontfile Complete
subjects Animals
antioxidant
Ascoviridae - genetics
ascovirus
Biocides
Copy number
Enzymatic activity
Enzyme activity
Enzymes
Gene expression
Genomes
Hydrogen peroxide
Infections
Insects
Larva - genetics
Larvae
Mortality
Muscles
NAD(P)H oxidase
NADPH oxidase
NF-E2-Related Factor 2 - genetics
Nrf2 pathway
Peroxidase
Peroxidases
Pest control
Pests
Reactive oxygen species
RNA-mediated interference
Spodoptera
Spodoptera exigua
Superoxide dismutase
title Insight into the regulation of the Nrf2 pathway in response to ascovirus infection in Spodoptera exigua
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