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Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts

Animals often exhibit dramatically behavioral plasticity depending on their internal physiological state, yet little is known about the underlying molecular mechanisms. The migratory locust, Locusta migratoria, provides an excellent model for addressing these questions because of their famous phase...

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Autores principales: Guo, Wei, Song, Juan, Yang, Pengcheng, Chen, Xiangyong, Chen, Dafeng, Ren, Dani, Kang, Le, Wang, Xianhui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7213744/
https://www.ncbi.nlm.nih.gov/pubmed/32348297
http://dx.doi.org/10.1371/journal.pgen.1008762
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author Guo, Wei
Song, Juan
Yang, Pengcheng
Chen, Xiangyong
Chen, Dafeng
Ren, Dani
Kang, Le
Wang, Xianhui
author_facet Guo, Wei
Song, Juan
Yang, Pengcheng
Chen, Xiangyong
Chen, Dafeng
Ren, Dani
Kang, Le
Wang, Xianhui
author_sort Guo, Wei
collection PubMed
description Animals often exhibit dramatically behavioral plasticity depending on their internal physiological state, yet little is known about the underlying molecular mechanisms. The migratory locust, Locusta migratoria, provides an excellent model for addressing these questions because of their famous phase polyphenism involving remarkably behavioral plasticity between gregarious and solitarious phases. Here, we report that a major insect hormone, juvenile hormone, is involved in the regulation of this behavioral plasticity related to phase change by influencing the expression levels of olfactory-related genes in the migratory locust. We found that the treatment of juvenile hormone analog, methoprene, can significantly shift the olfactory responses of gregarious nymphs from attraction to repulsion to the volatiles released by gregarious nymphs. In contrast, the repulsion behavior of solitarious nymphs significantly decreased when they were treated with precocene or injected with double-stranded RNA of JHAMT, a juvenile hormone acid O-methyltransferase. Further, JH receptor Met or JH-response gene Kr-h1 knockdown phenocopied the JH-deprivation effects on olfactory behavior. RNA-seq analysis identified 122 differentially expressed genes in antennae after methoprene application on gregarious nymphs. Interestingly, several olfactory-related genes were especially enriched, including takeout (TO) and chemosensory protein (CSP) which have key roles in behavioral phase change of locusts. Furthermore, methoprene application and Met or Kr-h1 knockdown resulted in simultaneous changes of both TO1 and CSP3 expression to reverse pattern, which mediated the transition between repulsion and attraction responses to gregarious volatiles. Our results suggest the regulatory roles of a pleiotropic hormone in locust behavioral plasticity through modulating gene expression in the peripheral olfactory system.
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spelling pubmed-72137442020-05-26 Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts Guo, Wei Song, Juan Yang, Pengcheng Chen, Xiangyong Chen, Dafeng Ren, Dani Kang, Le Wang, Xianhui PLoS Genet Research Article Animals often exhibit dramatically behavioral plasticity depending on their internal physiological state, yet little is known about the underlying molecular mechanisms. The migratory locust, Locusta migratoria, provides an excellent model for addressing these questions because of their famous phase polyphenism involving remarkably behavioral plasticity between gregarious and solitarious phases. Here, we report that a major insect hormone, juvenile hormone, is involved in the regulation of this behavioral plasticity related to phase change by influencing the expression levels of olfactory-related genes in the migratory locust. We found that the treatment of juvenile hormone analog, methoprene, can significantly shift the olfactory responses of gregarious nymphs from attraction to repulsion to the volatiles released by gregarious nymphs. In contrast, the repulsion behavior of solitarious nymphs significantly decreased when they were treated with precocene or injected with double-stranded RNA of JHAMT, a juvenile hormone acid O-methyltransferase. Further, JH receptor Met or JH-response gene Kr-h1 knockdown phenocopied the JH-deprivation effects on olfactory behavior. RNA-seq analysis identified 122 differentially expressed genes in antennae after methoprene application on gregarious nymphs. Interestingly, several olfactory-related genes were especially enriched, including takeout (TO) and chemosensory protein (CSP) which have key roles in behavioral phase change of locusts. Furthermore, methoprene application and Met or Kr-h1 knockdown resulted in simultaneous changes of both TO1 and CSP3 expression to reverse pattern, which mediated the transition between repulsion and attraction responses to gregarious volatiles. Our results suggest the regulatory roles of a pleiotropic hormone in locust behavioral plasticity through modulating gene expression in the peripheral olfactory system. Public Library of Science 2020-04-29 /pmc/articles/PMC7213744/ /pubmed/32348297 http://dx.doi.org/10.1371/journal.pgen.1008762 Text en © 2020 Guo et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Guo, Wei
Song, Juan
Yang, Pengcheng
Chen, Xiangyong
Chen, Dafeng
Ren, Dani
Kang, Le
Wang, Xianhui
Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts
title Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts
title_full Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts
title_fullStr Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts
title_full_unstemmed Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts
title_short Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts
title_sort juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7213744/
https://www.ncbi.nlm.nih.gov/pubmed/32348297
http://dx.doi.org/10.1371/journal.pgen.1008762
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