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

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

Research output: Contribution to journalArticle

Abstract

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.

Original languageEnglish (US)
Article numbere1002596
JournalPLoS genetics
Volume8
Issue number3
DOIs
StatePublished - Mar 1 2012

Fingerprint

Fat Body
Honey
Social Behavior
Gene Regulatory Networks
Bees
social behavior
honey
bee
gene expression
honey bees
maturation
Transcription Factors
transcription factors
fat
Gene Expression
binding sites
Binding Sites
Retinoid X Receptors
plasticity
brain

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

Cite this

The transcription factor ultraspiracle influences honey bee social behavior and behavior-related gene expression. / Ament, Seth A.; Wang, Ying; Chen, Chieh Chun; Blatti, Charles A.; Hong, Feng; Liang, Zhengzheng S.; Negre, Nicolas; White, Kevin P.; Rodriguez-Zas, Sandra L.; Mizzen, Craig A.; Sinha, Saurabh; Zhong, Sheng; Robinson, Gene E.

In: PLoS genetics, Vol. 8, No. 3, e1002596, 01.03.2012.

Research output: Contribution to journalArticle

Ament, Seth A. ; Wang, Ying ; Chen, Chieh Chun ; Blatti, Charles A. ; Hong, Feng ; Liang, Zhengzheng S. ; Negre, Nicolas ; White, Kevin P. ; Rodriguez-Zas, Sandra L. ; Mizzen, Craig A. ; Sinha, Saurabh ; Zhong, Sheng ; Robinson, Gene E. / The transcription factor ultraspiracle influences honey bee social behavior and behavior-related gene expression. In: PLoS genetics. 2012 ; Vol. 8, No. 3.
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