TGFβ signaling related genes are involved in hormonal mediation during termite soldier differentiation.

A working knowledge of the proximate factors intrinsic to sterile caste differentiation is necessary to understand the evolution of eusocial insects. Genomic and transcriptomic analyses in social hymenopteran insects have resulted in the hypothesis that sterile castes are generated by the novel func...

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Main Authors: Yudai Masuoka, Hajime Yaguchi, Kouhei Toga, Shuji Shigenobu, Kiyoto Maekawa
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2018-04-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC5912798?pdf=render
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spelling doaj-27e04e557b3f44e3aa4e139c5260a1ce2020-11-25T01:19:27ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042018-04-01144e100733810.1371/journal.pgen.1007338TGFβ signaling related genes are involved in hormonal mediation during termite soldier differentiation.Yudai MasuokaHajime YaguchiKouhei TogaShuji ShigenobuKiyoto MaekawaA working knowledge of the proximate factors intrinsic to sterile caste differentiation is necessary to understand the evolution of eusocial insects. Genomic and transcriptomic analyses in social hymenopteran insects have resulted in the hypothesis that sterile castes are generated by the novel function of co-opted or recruited universal gene networks found in solitary ancestors. However, transcriptome analysis during caste differentiation has not been tested in termites, and evolutionary processes associated with acquiring the caste are still unknown. Termites possess the soldier caste, which is regarded as the first acquired permanently sterile caste in the taxon. In this study, we performed a comparative transcriptome analysis in termite heads during 3 molting processes, i.e., worker, presoldier and soldier molts, under natural conditions in an incipient colony of the damp-wood termite Zootermopsis nevadensis. Although similar expression patterns were observed during each molting process, more than 50 genes were shown to be highly expressed before the presoldier (intermediate stage of soldier) molt. We then performed RNA interference (RNAi) of the candidate 13 genes, including transcription factors and uncharacterized protein genes, during presoldier differentiation induced by juvenile hormone (JH) analog treatment. Presoldiers induced after RNAi of two genes related to TGFβ (Transforming growth factor beta) signaling were extremely unusual and possessed soldier-like phenotypes. These individuals also displayed aggressive behaviors similar to natural soldiers when confronted with Formica ants as hypothetical enemies. These presoldiers never molted into the next instar, presumably due to the decreased expression levels of the molting hormone (20-hydroxyecdysone; 20E) signaling genes. These results suggest that TGFβ signaling was acquired for the novel function of regulating between JH and 20E signaling during soldier differentiation in termites.http://europepmc.org/articles/PMC5912798?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Yudai Masuoka
Hajime Yaguchi
Kouhei Toga
Shuji Shigenobu
Kiyoto Maekawa
spellingShingle Yudai Masuoka
Hajime Yaguchi
Kouhei Toga
Shuji Shigenobu
Kiyoto Maekawa
TGFβ signaling related genes are involved in hormonal mediation during termite soldier differentiation.
PLoS Genetics
author_facet Yudai Masuoka
Hajime Yaguchi
Kouhei Toga
Shuji Shigenobu
Kiyoto Maekawa
author_sort Yudai Masuoka
title TGFβ signaling related genes are involved in hormonal mediation during termite soldier differentiation.
title_short TGFβ signaling related genes are involved in hormonal mediation during termite soldier differentiation.
title_full TGFβ signaling related genes are involved in hormonal mediation during termite soldier differentiation.
title_fullStr TGFβ signaling related genes are involved in hormonal mediation during termite soldier differentiation.
title_full_unstemmed TGFβ signaling related genes are involved in hormonal mediation during termite soldier differentiation.
title_sort tgfβ signaling related genes are involved in hormonal mediation during termite soldier differentiation.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2018-04-01
description A working knowledge of the proximate factors intrinsic to sterile caste differentiation is necessary to understand the evolution of eusocial insects. Genomic and transcriptomic analyses in social hymenopteran insects have resulted in the hypothesis that sterile castes are generated by the novel function of co-opted or recruited universal gene networks found in solitary ancestors. However, transcriptome analysis during caste differentiation has not been tested in termites, and evolutionary processes associated with acquiring the caste are still unknown. Termites possess the soldier caste, which is regarded as the first acquired permanently sterile caste in the taxon. In this study, we performed a comparative transcriptome analysis in termite heads during 3 molting processes, i.e., worker, presoldier and soldier molts, under natural conditions in an incipient colony of the damp-wood termite Zootermopsis nevadensis. Although similar expression patterns were observed during each molting process, more than 50 genes were shown to be highly expressed before the presoldier (intermediate stage of soldier) molt. We then performed RNA interference (RNAi) of the candidate 13 genes, including transcription factors and uncharacterized protein genes, during presoldier differentiation induced by juvenile hormone (JH) analog treatment. Presoldiers induced after RNAi of two genes related to TGFβ (Transforming growth factor beta) signaling were extremely unusual and possessed soldier-like phenotypes. These individuals also displayed aggressive behaviors similar to natural soldiers when confronted with Formica ants as hypothetical enemies. These presoldiers never molted into the next instar, presumably due to the decreased expression levels of the molting hormone (20-hydroxyecdysone; 20E) signaling genes. These results suggest that TGFβ signaling was acquired for the novel function of regulating between JH and 20E signaling during soldier differentiation in termites.
url http://europepmc.org/articles/PMC5912798?pdf=render
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