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Physiological and transcriptional immune responses of a non-model arthropod to infection with different entomopathogenic groups
Insect immune responses to multiple pathogen groups including viruses, bacteria, fungi, and entomopathogenic nematodes have traditionally been documented in model insects such as Drosophila melanogaster, or medically important insects such as Aedes aegypti. Despite their potential importance in unde...
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Published in: | PloS one 2022-02, Vol.17 (2), p.e0263620 |
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description | Insect immune responses to multiple pathogen groups including viruses, bacteria, fungi, and entomopathogenic nematodes have traditionally been documented in model insects such as Drosophila melanogaster, or medically important insects such as Aedes aegypti. Despite their potential importance in understanding the efficacy of pathogens as biological control agents, these responses are infrequently studied in agriculturally important pests. Additionally, studies that investigate responses of a host species to different pathogen groups are uncommon, and typically focus on only a single time point during infection. As such, a robust understanding of immune system responses over the time of infection is often lacking in many pest species. This study was conducted to understand how 3rd instar larvae of the major insect pest Helicoverpa zea responded through the course of an infection by four different pathogenic groups: viruses, bacteria, fungi, and entomopathogenic nematodes; by sampling at three different times post-inoculation. Physiological immune responses were assessed at 4-, 24-, and 48-hours post-infection by measuring hemolymph phenoloxidase concentrations, hemolymph prophenoloxidase concentrations, hemocyte counts, and encapsulation ability. Transcriptional immune responses were measured at 24-, 48-, and 72-hours post-infection by quantifying the expression of PPO2, Argonaute-2, JNK, Dorsal, and Relish. This gene set covers the major known immune pathways: phenoloxidase cascade, siRNA, JNK pathway, Toll pathway, and IMD pathway. Our results indicate H. zea has an extreme immune response to Bacillus thuringiensis bacteria, a mild response to Helicoverpa armigera nucleopolyhedrovirus, and little-to-no detectable response to either the fungus Beauveria bassiana or Steinernema carpocapsae nematodes. |
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Despite their potential importance in understanding the efficacy of pathogens as biological control agents, these responses are infrequently studied in agriculturally important pests. Additionally, studies that investigate responses of a host species to different pathogen groups are uncommon, and typically focus on only a single time point during infection. As such, a robust understanding of immune system responses over the time of infection is often lacking in many pest species. This study was conducted to understand how 3rd instar larvae of the major insect pest Helicoverpa zea responded through the course of an infection by four different pathogenic groups: viruses, bacteria, fungi, and entomopathogenic nematodes; by sampling at three different times post-inoculation. Physiological immune responses were assessed at 4-, 24-, and 48-hours post-infection by measuring hemolymph phenoloxidase concentrations, hemolymph prophenoloxidase concentrations, hemocyte counts, and encapsulation ability. Transcriptional immune responses were measured at 24-, 48-, and 72-hours post-infection by quantifying the expression of PPO2, Argonaute-2, JNK, Dorsal, and Relish. This gene set covers the major known immune pathways: phenoloxidase cascade, siRNA, JNK pathway, Toll pathway, and IMD pathway. Our results indicate H. zea has an extreme immune response to Bacillus thuringiensis bacteria, a mild response to Helicoverpa armigera nucleopolyhedrovirus, and little-to-no detectable response to either the fungus Beauveria bassiana or Steinernema carpocapsae nematodes.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0263620</identifier><identifier>PMID: 35134064</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Agricultural production ; Analysis ; Animals ; Arthropoda ; Bacillus thuringiensis - pathogenicity ; Bacteria ; Biological control ; Biological Control Agents ; Biology and Life Sciences ; Defense mechanisms ; Entomology ; Entomopathogenic nematodes ; Experiments ; Fungi ; Gene expression ; Genetic aspects ; Genetic transcription ; Hemocytes ; Hemocytes - metabolism ; Hemolymph ; Hemolymph - metabolism ; Immune response ; Immune system ; Immunity ; Infections ; Inoculation ; Insect Proteins - genetics ; Insects ; Larva - immunology ; Larva - metabolism ; Larvae ; Lepidoptera - genetics ; Lepidoptera - immunology ; Medicine and Health Sciences ; MicroRNAs ; Mosquitoes ; Moths - genetics ; Moths - immunology ; Moths - microbiology ; Nematodes ; Nucleopolyhedroviruses - pathogenicity ; Pathogens ; Pest Control - methods ; Pest Control, Biological - methods ; Pests ; Phenoloxidase ; Physiological aspects ; Physiology ; Prophenoloxidase ; Reagents ; siRNA ; Transcription ; Viruses</subject><ispartof>PloS one, 2022-02, Vol.17 (2), p.e0263620</ispartof><rights>COPYRIGHT 2022 Public Library of Science</rights><rights>2022 Black et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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pathogenicity</topic><topic>Bacteria</topic><topic>Biological control</topic><topic>Biological Control Agents</topic><topic>Biology and Life Sciences</topic><topic>Defense mechanisms</topic><topic>Entomology</topic><topic>Entomopathogenic nematodes</topic><topic>Experiments</topic><topic>Fungi</topic><topic>Gene expression</topic><topic>Genetic aspects</topic><topic>Genetic transcription</topic><topic>Hemocytes</topic><topic>Hemocytes - metabolism</topic><topic>Hemolymph</topic><topic>Hemolymph - metabolism</topic><topic>Immune response</topic><topic>Immune system</topic><topic>Immunity</topic><topic>Infections</topic><topic>Inoculation</topic><topic>Insect Proteins - genetics</topic><topic>Insects</topic><topic>Larva - immunology</topic><topic>Larva - metabolism</topic><topic>Larvae</topic><topic>Lepidoptera - genetics</topic><topic>Lepidoptera - immunology</topic><topic>Medicine and Health Sciences</topic><topic>MicroRNAs</topic><topic>Mosquitoes</topic><topic>Moths - genetics</topic><topic>Moths - 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Despite their potential importance in understanding the efficacy of pathogens as biological control agents, these responses are infrequently studied in agriculturally important pests. Additionally, studies that investigate responses of a host species to different pathogen groups are uncommon, and typically focus on only a single time point during infection. As such, a robust understanding of immune system responses over the time of infection is often lacking in many pest species. This study was conducted to understand how 3rd instar larvae of the major insect pest Helicoverpa zea responded through the course of an infection by four different pathogenic groups: viruses, bacteria, fungi, and entomopathogenic nematodes; by sampling at three different times post-inoculation. Physiological immune responses were assessed at 4-, 24-, and 48-hours post-infection by measuring hemolymph phenoloxidase concentrations, hemolymph prophenoloxidase concentrations, hemocyte counts, and encapsulation ability. Transcriptional immune responses were measured at 24-, 48-, and 72-hours post-infection by quantifying the expression of PPO2, Argonaute-2, JNK, Dorsal, and Relish. This gene set covers the major known immune pathways: phenoloxidase cascade, siRNA, JNK pathway, Toll pathway, and IMD pathway. Our results indicate H. zea has an extreme immune response to Bacillus thuringiensis bacteria, a mild response to Helicoverpa armigera nucleopolyhedrovirus, and little-to-no detectable response to either the fungus Beauveria bassiana or Steinernema carpocapsae nematodes.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>35134064</pmid><doi>10.1371/journal.pone.0263620</doi><tpages>e0263620</tpages><orcidid>https://orcid.org/0000-0001-5399-0149</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Agricultural production Analysis Animals Arthropoda Bacillus thuringiensis - pathogenicity Bacteria Biological control Biological Control Agents Biology and Life Sciences Defense mechanisms Entomology Entomopathogenic nematodes Experiments Fungi Gene expression Genetic aspects Genetic transcription Hemocytes Hemocytes - metabolism Hemolymph Hemolymph - metabolism Immune response Immune system Immunity Infections Inoculation Insect Proteins - genetics Insects Larva - immunology Larva - metabolism Larvae Lepidoptera - genetics Lepidoptera - immunology Medicine and Health Sciences MicroRNAs Mosquitoes Moths - genetics Moths - immunology Moths - microbiology Nematodes Nucleopolyhedroviruses - pathogenicity Pathogens Pest Control - methods Pest Control, Biological - methods Pests Phenoloxidase Physiological aspects Physiology Prophenoloxidase Reagents siRNA Transcription Viruses |
title | Physiological and transcriptional immune responses of a non-model arthropod to infection with different entomopathogenic groups |
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