Molecular mechanisms of phenotypic plasticity: Explorations of DNA methylation and transcriptional regulation using the honey bee

Wang, Ying

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Description

Title

Molecular mechanisms of phenotypic plasticity: Explorations of DNA methylation and transcriptional regulation using the honey bee

Author(s)

Wang, Ying

Issue Date

2011-01-21T22:44:13Z

Director of Research (if dissertation) or Advisor (if thesis)

• Robinson, Gene E.
• Mizzen, Craig A.

Doctoral Committee Chair(s)

Clayton, David F.

Committee Member(s)

• Robinson, Gene E.
• Mizzen, Craig A.
• Jones, Peter L.
• Robertson, Hugh M.
• Schoenherr, Christopher J.

Department of Study

Cell & Developmental Biology

Discipline

Cell and Developmental Biology

Degree Granting Institution

University of Illinois at Urbana-Champaign

Degree Name

Ph.D.

Degree Level

Dissertation

Keyword(s)

• honey bee
• DNA methylation
• chromatin immunoprecipitation -genomic tiling arrays (ChIP-chip)
• transcription regulation
• behavioral maturation
• natural lipid loss

Abstract

Honey bee behavioral maturation exemplifies phenotypic plasticity, the ability of a single genotype to produce multiple phenotypes in response to environmental conditions (Scheiner, 1993; West-Eberhard, 1989). Behavioral maturation in honey bees is characterized by a socially regulated transition of adult worker bees from brood caring (“nursing”) to foraging outside hives (Winston, 1991). It involves a suite of behavioral and physiological changes regulated by multiple environmental and internal factors. With the sequenced honey bee genome (Honey Bee Genome Sequencing Consortium, 2006), and development of genomic techniques, honey bee behavioral maturation provides a platform to understand molecular mechanisms underlying phenotypic plasticity. It has been demonstrated that phenotypic plasticity is associated with massive gene expression changes (Aubin-Horth & Renn, 2009). Therefore, it is essential to understand mechanisms of transcriptional regulation related to alternative phenotypes. This thesis focuses on two important aspects of transcriptional regulation: DNA methylation and transcription regulation by a nuclear receptor, Ultraspiracle (USP). Chapter 2 presents results that demonstrate that there is a functional CpG methylation system in honey bees, the first well-characterized functional DNA methylation system in insects. Catalytically active orthologs of vertebrate DNA methyltransferase (Dnmts) were identified along with methylated genes. Compared to vertebrate genomes, DNA methylations in honey bees are sparse, and all of the identified methylations are intragenic, similar to results shown in other invertebrates. Differences in DNA methylation density and positions suggest possibly different functions of DNA methylation in vertebrates and invertebrates. The characterization of a DNA methylation system in honey bees paves the way to study its function in honey bee behavioral maturation. This paper was published in 2006 in Science 314: 645-647. Chapter 3 presents a review of nutritional regulation of honey bee behavioral maturation and propose systems biology approaches to reveal the gene regulatory networks (GRNs) underlying behavioral maturation. It was published in 2010 in Wiley Interdisciplinary Reviews: Systems Biology and Medicine (published online in advance of print). Chapter 4 presents results on transcriptional regulation related to behavioral maturation in the context of fat bodies gene expression change. As a first step, we focus on transcription regulation by USP, a nuclear receptor implicated in JH signaling. USP was first demonstrated to regulate behavioral maturation. usp knockdown in honey bee workers’ fat bodies significantly delayed onset of foraging. Genome-wide USP binding sites were then mapped in the fat bodies of nurses and foragers respectively. No difference of USP binding was detected, suggesting USP regulates gene expression depending on the availability of co-factors or ligands and chromatin environments. Functional analysis of USP putative genes reveals several genes involved in multiple signaling pathways in behavioral maturation, raising the possibility that USP works as a master regulator to integrate different signals during honey bee behavioral maturation.

Graduation Semester

2010-12

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Copyright 2010 Ying Wang

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