The transcription factor ultraspiracle influences honey bee social behavior and behavior-related gene expression.

Behavior is among the most dynamic animal phenotypes, modulated by a variety of internal and external stimuli. Behavioral differences are associated with large-scale changes in gene expression, but little is known about how these changes are regulated. Here we show how a transcription factor (TF), u...

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Main Authors: Seth A Ament, Ying Wang, Chieh-Chun Chen, Charles A Blatti, Feng Hong, Zhengzheng S Liang, Nicolas Negre, Kevin P White, Sandra L Rodriguez-Zas, Craig A Mizzen, Saurabh Sinha, Sheng Zhong, Gene E Robinson
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC3315457?pdf=render
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spelling doaj-6f667518b7c84552b233218414d001672020-11-25T01:04:30ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042012-01-0183e100259610.1371/journal.pgen.1002596The transcription factor ultraspiracle influences honey bee social behavior and behavior-related gene expression.Seth A AmentYing WangChieh-Chun ChenCharles A BlattiFeng HongZhengzheng S LiangNicolas NegreKevin P WhiteSandra L Rodriguez-ZasCraig A MizzenSaurabh SinhaSheng ZhongGene E RobinsonBehavior is among the most dynamic animal phenotypes, modulated by a variety of internal and external stimuli. Behavioral differences are associated with large-scale changes in gene expression, but little is known about how these changes are regulated. Here we show how a transcription factor (TF), ultraspiracle (usp; the insect homolog of the Retinoid X Receptor), working in complex transcriptional networks, can regulate behavioral plasticity and associated changes in gene expression. We first show that RNAi knockdown of USP in honey bee abdominal fat bodies delayed the transition from working in the hive (primarily "nursing" brood) to foraging outside. We then demonstrate through transcriptomics experiments that USP induced many maturation-related transcriptional changes in the fat bodies by mediating transcriptional responses to juvenile hormone. These maturation-related transcriptional responses to USP occurred without changes in USP's genomic binding sites, as revealed by ChIP-chip. Instead, behaviorally related gene expression is likely determined by combinatorial interactions between USP and other TFs whose cis-regulatory motifs were enriched at USP's binding sites. Many modules of JH- and maturation-related genes were co-regulated in both the fat body and brain, predicting that usp and cofactors influence shared transcriptional networks in both of these maturation-related tissues. Our findings demonstrate how "single gene effects" on behavioral plasticity can involve complex transcriptional networks, in both brain and peripheral tissues.http://europepmc.org/articles/PMC3315457?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Seth A Ament
Ying Wang
Chieh-Chun Chen
Charles A Blatti
Feng Hong
Zhengzheng S Liang
Nicolas Negre
Kevin P White
Sandra L Rodriguez-Zas
Craig A Mizzen
Saurabh Sinha
Sheng Zhong
Gene E Robinson
spellingShingle Seth A Ament
Ying Wang
Chieh-Chun Chen
Charles A Blatti
Feng Hong
Zhengzheng S Liang
Nicolas Negre
Kevin P White
Sandra L Rodriguez-Zas
Craig A Mizzen
Saurabh Sinha
Sheng Zhong
Gene E Robinson
The transcription factor ultraspiracle influences honey bee social behavior and behavior-related gene expression.
PLoS Genetics
author_facet Seth A Ament
Ying Wang
Chieh-Chun Chen
Charles A Blatti
Feng Hong
Zhengzheng S Liang
Nicolas Negre
Kevin P White
Sandra L Rodriguez-Zas
Craig A Mizzen
Saurabh Sinha
Sheng Zhong
Gene E Robinson
author_sort Seth A Ament
title The transcription factor ultraspiracle influences honey bee social behavior and behavior-related gene expression.
title_short The transcription factor ultraspiracle influences honey bee social behavior and behavior-related gene expression.
title_full The transcription factor ultraspiracle influences honey bee social behavior and behavior-related gene expression.
title_fullStr The transcription factor ultraspiracle influences honey bee social behavior and behavior-related gene expression.
title_full_unstemmed The transcription factor ultraspiracle influences honey bee social behavior and behavior-related gene expression.
title_sort transcription factor ultraspiracle influences honey bee social behavior and behavior-related gene expression.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2012-01-01
description Behavior is among the most dynamic animal phenotypes, modulated by a variety of internal and external stimuli. Behavioral differences are associated with large-scale changes in gene expression, but little is known about how these changes are regulated. Here we show how a transcription factor (TF), ultraspiracle (usp; the insect homolog of the Retinoid X Receptor), working in complex transcriptional networks, can regulate behavioral plasticity and associated changes in gene expression. We first show that RNAi knockdown of USP in honey bee abdominal fat bodies delayed the transition from working in the hive (primarily "nursing" brood) to foraging outside. We then demonstrate through transcriptomics experiments that USP induced many maturation-related transcriptional changes in the fat bodies by mediating transcriptional responses to juvenile hormone. These maturation-related transcriptional responses to USP occurred without changes in USP's genomic binding sites, as revealed by ChIP-chip. Instead, behaviorally related gene expression is likely determined by combinatorial interactions between USP and other TFs whose cis-regulatory motifs were enriched at USP's binding sites. Many modules of JH- and maturation-related genes were co-regulated in both the fat body and brain, predicting that usp and cofactors influence shared transcriptional networks in both of these maturation-related tissues. Our findings demonstrate how "single gene effects" on behavioral plasticity can involve complex transcriptional networks, in both brain and peripheral tissues.
url http://europepmc.org/articles/PMC3315457?pdf=render
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