Dataset Information

Regulation of behaviorally associated gene networks in worker honey bee ovaries.

ABSTRACT: Several lines of evidence support genetic links between ovary size and division of labor in worker honey bees. However, it is largely unknown how ovaries influence behavior. To address this question, we first performed transcriptional profiling on worker ovaries from two genotypes that differ in social behavior and ovary size. Then, we contrasted the differentially expressed ovarian genes with six sets of available brain transcriptomes. Finally, we probed behavior-related candidate gene networks in wild-type ovaries of different sizes. We found differential expression in 2151 ovarian transcripts in these artificially selected honey bee strains, corresponding to approximately 20.3% of the predicted gene set of honey bees. Differences in gene expression overlapped significantly with changes in the brain transcriptomes. Differentially expressed genes were associated with neural signal transmission (tyramine receptor, TYR) and ecdysteroid signaling; two independently tested nuclear hormone receptors (HR46 and ftz-f1) were also significantly correlated with ovary size in wild-type bees. We suggest that the correspondence between ovary and brain transcriptomes identified here indicates systemic regulatory networks among hormones (juvenile hormone and ecdysteroids), pheromones (queen mandibular pheromone), reproductive organs and nervous tissues in worker honey bees. Furthermore, robust correlations between ovary size and neuraland endocrine response genes are consistent with the hypothesized roles of the ovaries in honey bee behavioral regulation.

SUBMITTER: Wang Y

PROVIDER: S-EPMC3233392 | biostudies-literature | 2012 Jan

REPOSITORIES: biostudies-literature

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Regulation of behaviorally associated gene networks in worker honey bee ovaries.

Wang Ying Y Kocher Sarah D SD Linksvayer Timothy A TA Grozinger Christina M CM Page Robert E RE Amdam Gro V GV

The Journal of experimental biology 20120101 Pt 1

Several lines of evidence support genetic links between ovary size and division of labor in worker honey bees. However, it is largely unknown how ovaries influence behavior. To address this question, we first performed transcriptional profiling on worker ovaries from two genotypes that differ in social behavior and ovary size. Then, we contrasted the differentially expressed ovarian genes with six sets of available brain transcriptomes. Finally, we probed behavior-related candidate gene networks ...[more]

PMID: 22162860

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Project description:BACKGROUND:The evolution of reproductive self-sacrifice is well understood from kin theory, yet our understanding of how actual genes influence the expression of reproductive altruism is only beginning to take shape. As a model in the molecular study of social behaviour, the honey bee Apis mellifera has yielded hundreds of genes associated in their expression with differences in reproductive status of females, including genes directly associated with sterility, yet there has not been an attempt to link these candidates into functional networks that explain how workers regulate sterility in the presence of queen pheromone. In this study we use available microarray data and a co-citation analysis to describe what gene interactions might regulate a worker's response to ovary suppressing queen pheromone. RESULTS:We reconstructed a total of nine gene networks that vary in size and gene composition, but that are significantly enriched for genes of reproductive function. The networks identify, for the first time, which candidate microarray genes are of functional importance, as evidenced by their degree of connectivity to other genes within each of the inferred networks. Our study identifies single genes of interest related to oogenesis, including eggless, and further implicates pathways related to insulin, ecdysteroid, and dopamine signaling as potentially important to reproductive decision making in honey bees. CONCLUSIONS:The networks derived here appear to be variable in gene composition, hub gene identity, and the overall interactions they describe. One interpretation is that workers use different networks to control personal reproduction via ovary activation, perhaps as a function of age or environmental circumstance. Alternatively, the multiple networks inferred here may represent segments of the larger, single network that remains unknown in its entirety. The networks generated here are provisional but do offer a new multi-gene framework for understanding how honey bees regulate personal reproduction within their highly social breeding system.

Project description:Protein phosphorylation is known to regulate a comprehensive scenario of critical cellular processes. However, phosphorylation-mediated regulatory networks in honey bee embryogenesis are mainly unknown. We identified 6342 phosphosites from 2438 phosphoproteins and predicted 168 kinases in the honey bee embryo. Generally, the worker and drone develop similar phosphoproteome architectures and major phosphorylation events during embryogenesis. In 24 h embryos, protein kinases A play vital roles in regulating cell proliferation and blastoderm formation. At 48–72 h, kinase subfamily dual-specificity tyrosine-regulated kinase, cyclin-dependent kinase (CDK), and induced pathways related to protein synthesis and morphogenesis suggest the centrality to enhance the germ layer development, organogenesis, and dorsal closure. Notably, workers and drones formulated distinct phosphoproteome signatures. For 24 h embryos, the highly phosphorylated serine/threonine-protein kinase minibrain, microtubule-associated serine/threonine-protein kinase 2 (MAST2), and phosphorylation of mitogen-activated protein kinase 3 (MAPK3) at Thr564 in workers, are likely to regulate the late onset of cell proliferation; in contrast, drone embryos enhanced the expression of CDK12, MAPK3, and MAST2 to promote the massive synthesis of proteins and cytoskeleton. In 48 h, the induced serine/threonine-protein kinase and CDK12 in worker embryos signify their roles in the construction of embryonic tissues and organs; however, the highly activated kinases CDK1, raf homolog serine/threonine-protein kinase, and MAST2 in drone embryos may drive the large-scale establishment of tissues and organs. In 72 h, the activated pathways and kinases associated with cell growth and tissue differentiation in worker embryos may promote the configuration of rudimentary organs. However, kinases implicated in cytoskeleton organization in drone embryos may drive the blastokinesis and dorsal closure. Our hitherto most comprehensive phosphoproteome offers a valuable resource for signaling research on phosphorylation dynamics in honey bee embryos.

Dataset Information

Regulation of behaviorally associated gene networks in worker honey bee ovaries.

Publications

Regulation of behaviorally associated gene networks in worker honey bee ovaries.

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