Nutritionally Driven Differential Gene Expression Leads to Heterochronic Brain Development in Honeybee Castes

Author(s)

Moda, Livia Maria ^{[1, 2]} ; Vieira, Joseana ^[2] ; Guimaraes Freire, Anna Claudia ^[2] ; Bonatti, Vanessa ^{[1, 2]} ; Bomtorin, Ana Durvalina ^[1] ; Barchuk, Angel Roberto ^[2] ; Paulino Simoes, Zila Luz ^[3]

Affiliation

^[1] Univ SaPaulo FMRP, Dept Genet, Sao Paulo - Brazil

^[2] Univ Fed Alfenas, UNIFAL MG, Inst Ciencias Biomed, Dept Biol Celular Tecidual & Desenvolvimento, Alfenas, MG - Brazil

^[3] Univ Sao Paulo FFCLRP, Dept Biol, Sao Paulo - Brazil

• Document type: Journal article
• Source: PLoS One; v. 8, n. 5 MAY 30 2013.
• Web of Science Citations: 13

Abstract

The differential feeding regimes experienced by the queen and worker larvae of the honeybee Apis mellifera shape a complex endocrine response cascade that ultimately gives rise to differences in brain morphologies. Brain development analyzed at the morphological level from the third (L3) through fifth (L5) larval instars revealed an asynchrony between queens and workers. In the feeding phase of the last larval instar (L5F), two well-formed structures, pedunculi and calyces, are identifiable in the mushroom bodies of queens, both of which are not present in workers until a later phase (spinning phase, L5S). Genome-wide expression analyses and normalized transcript expression experiments monitoring specific genes revealed that this differential brain development starts earlier, during L3. Analyzing brains from L3 through L5S1 larvae, we identified 21 genes with caste-specific transcription patterns (e. g., APC-4, GlcAT-P, fax, kr-h1 and shot), which encode proteins that are potentially involved in the development of brain tissues through controlling the cell proliferation rate (APC4, kr-h1) and fasciculation (GlcAT-P, fax, and shot). Shot, whose expression is known to be required for axon extension and cell proliferation, was found to be transcribed at significantly higher levels in L4 queens compared with worker larvae. Moreover, the protein encoded by this gene was immunolocalized to the cytoplasm of cells near the antennal lobe neuropiles and proximal to the Kenyon cells in the brains of L4 queens. In conclusion, during the larval period, the brains of queens are larger and develop more rapidly than workers' brains, which represents a developmental heterochrony reflecting the effect of the differential feeding regime of the two castes on nervous system development. Furthermore, this differential development is characterized by caste-specific transcriptional profiles of a set of genes, thus pointing to a link between differential nutrition and differential neurogenesis via genes that control cell proliferation and fasciculation. (AU)

• FAPESP's process: 09/00810-7 - Differential brain development and transcription profile of genes related to neurogenesis in castes of Apis mellifera
• Grantee: Lívia Maria Rosatto Moda
• Support Opportunities: Scholarships in Brazil - Post-Doctoral
• FAPESP's process: 05/03926-5 - Functional genomics of Apis mellifera: search for new genes and functional networks in the context of development, different castes and reproduction
• Grantee: Zilá Luz Paulino Simões
• Support Opportunities: Research Projects - Thematic Grants
• FAPESP's process: 09/05675-0 - Differential gene expression and induction of morphological characters in Apis mellifera
• Grantee: Ana Durvalina Bomtorin
• Support Opportunities: Scholarships in Brazil - Doctorate