Nutritionally driven differential gene expression leads to heterochronic brain development in honeybee castes.

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 fif...

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Autores principales:	Lívia Maria Moda, Joseana Vieira, Anna Cláudia Guimarães Freire, Vanessa Bonatti, Ana Durvalina Bomtorin, Angel Roberto Barchuk, Zilá Luz Paulino Simões
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2013
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/b1bbc172dbd64f66b6a45ac4b9d8d57d
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spelling	oai:doaj.org-article:b1bbc172dbd64f66b6a45ac4b9d8d57d2021-11-18T07:43:47ZNutritionally driven differential gene expression leads to heterochronic brain development in honeybee castes.1932-620310.1371/journal.pone.0064815https://doaj.org/article/b1bbc172dbd64f66b6a45ac4b9d8d57d2013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23738002/?tool=EBIhttps://doaj.org/toc/1932-6203The 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.Lívia Maria ModaJoseana VieiraAnna Cláudia Guimarães FreireVanessa BonattiAna Durvalina BomtorinAngel Roberto BarchukZilá Luz Paulino SimõesPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 8, Iss 5, p e64815 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Lívia Maria Moda Joseana Vieira Anna Cláudia Guimarães Freire Vanessa Bonatti Ana Durvalina Bomtorin Angel Roberto Barchuk Zilá Luz Paulino Simões Nutritionally driven differential gene expression leads to heterochronic brain development in honeybee castes.
description	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.
format	article
author	Lívia Maria Moda Joseana Vieira Anna Cláudia Guimarães Freire Vanessa Bonatti Ana Durvalina Bomtorin Angel Roberto Barchuk Zilá Luz Paulino Simões
author_facet	Lívia Maria Moda Joseana Vieira Anna Cláudia Guimarães Freire Vanessa Bonatti Ana Durvalina Bomtorin Angel Roberto Barchuk Zilá Luz Paulino Simões
author_sort	Lívia Maria Moda
title	Nutritionally driven differential gene expression leads to heterochronic brain development in honeybee castes.
title_short	Nutritionally driven differential gene expression leads to heterochronic brain development in honeybee castes.
title_full	Nutritionally driven differential gene expression leads to heterochronic brain development in honeybee castes.
title_fullStr	Nutritionally driven differential gene expression leads to heterochronic brain development in honeybee castes.
title_full_unstemmed	Nutritionally driven differential gene expression leads to heterochronic brain development in honeybee castes.
title_sort	nutritionally driven differential gene expression leads to heterochronic brain development in honeybee castes.
publisher	Public Library of Science (PLoS)
publishDate	2013
url	https://doaj.org/article/b1bbc172dbd64f66b6a45ac4b9d8d57d
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Nutritionally driven differential gene expression leads to heterochronic brain development in honeybee castes.

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