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Mblk-1/E93, an ecdysone related-transcription factor, targets synaptic plasticity-related genes in the honey bee mushroom bodies

Among hymenopteran insects, aculeate species such as bees, ants, and wasps have enlarged and morphologically elaborate mushroom bodies (MBs), a higher-order brain center in the insect, implying their relationship with the advanced behavioral traits of aculeate species. The molecular bases leading to...

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Autores principales: Matsumura, Yasuhiro, To, Taiko Kim, Kunieda, Takekazu, Kohno, Hiroki, Kakutani, Tetsuji, Kubo, Takeo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9734179/
https://www.ncbi.nlm.nih.gov/pubmed/36494426
http://dx.doi.org/10.1038/s41598-022-23329-z
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author Matsumura, Yasuhiro
To, Taiko Kim
Kunieda, Takekazu
Kohno, Hiroki
Kakutani, Tetsuji
Kubo, Takeo
author_facet Matsumura, Yasuhiro
To, Taiko Kim
Kunieda, Takekazu
Kohno, Hiroki
Kakutani, Tetsuji
Kubo, Takeo
author_sort Matsumura, Yasuhiro
collection PubMed
description Among hymenopteran insects, aculeate species such as bees, ants, and wasps have enlarged and morphologically elaborate mushroom bodies (MBs), a higher-order brain center in the insect, implying their relationship with the advanced behavioral traits of aculeate species. The molecular bases leading to the acquisition of complicated MB functions, however, remains unclear. We previously reported the constitutive and MB-preferential expression of an ecdysone-signaling related transcription factor, Mblk-1/E93, in the honey bee brain. Here, we searched for target genes of Mblk-1 in the worker honey bee MBs using chromatin immunoprecipitation sequence analyses and found that Mblk-1 targets several genes involved in synaptic plasticity, learning, and memory abilities. We also demonstrated that Mblk-1 expression is self-regulated via Mblk-1-binding sites, which are located upstream of Mblk-1. Furthermore, we showed that the number of the Mblk-1-binding motif located upstream of Mblk-1 homologs increased associated with evolution of hymenopteran insects. Our findings suggest that Mblk-1, which has been focused on as a developmental gene transiently induced by ecdysone, has acquired a novel expression pattern to play a role in synaptic plasticity in honey bee MBs, raising a possibility that molecular evolution of Mblk-1 may have partly contributed to the elaboration of MB function in insects.
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spelling pubmed-97341792022-12-11 Mblk-1/E93, an ecdysone related-transcription factor, targets synaptic plasticity-related genes in the honey bee mushroom bodies Matsumura, Yasuhiro To, Taiko Kim Kunieda, Takekazu Kohno, Hiroki Kakutani, Tetsuji Kubo, Takeo Sci Rep Article Among hymenopteran insects, aculeate species such as bees, ants, and wasps have enlarged and morphologically elaborate mushroom bodies (MBs), a higher-order brain center in the insect, implying their relationship with the advanced behavioral traits of aculeate species. The molecular bases leading to the acquisition of complicated MB functions, however, remains unclear. We previously reported the constitutive and MB-preferential expression of an ecdysone-signaling related transcription factor, Mblk-1/E93, in the honey bee brain. Here, we searched for target genes of Mblk-1 in the worker honey bee MBs using chromatin immunoprecipitation sequence analyses and found that Mblk-1 targets several genes involved in synaptic plasticity, learning, and memory abilities. We also demonstrated that Mblk-1 expression is self-regulated via Mblk-1-binding sites, which are located upstream of Mblk-1. Furthermore, we showed that the number of the Mblk-1-binding motif located upstream of Mblk-1 homologs increased associated with evolution of hymenopteran insects. Our findings suggest that Mblk-1, which has been focused on as a developmental gene transiently induced by ecdysone, has acquired a novel expression pattern to play a role in synaptic plasticity in honey bee MBs, raising a possibility that molecular evolution of Mblk-1 may have partly contributed to the elaboration of MB function in insects. Nature Publishing Group UK 2022-12-09 /pmc/articles/PMC9734179/ /pubmed/36494426 http://dx.doi.org/10.1038/s41598-022-23329-z Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Matsumura, Yasuhiro
To, Taiko Kim
Kunieda, Takekazu
Kohno, Hiroki
Kakutani, Tetsuji
Kubo, Takeo
Mblk-1/E93, an ecdysone related-transcription factor, targets synaptic plasticity-related genes in the honey bee mushroom bodies
title Mblk-1/E93, an ecdysone related-transcription factor, targets synaptic plasticity-related genes in the honey bee mushroom bodies
title_full Mblk-1/E93, an ecdysone related-transcription factor, targets synaptic plasticity-related genes in the honey bee mushroom bodies
title_fullStr Mblk-1/E93, an ecdysone related-transcription factor, targets synaptic plasticity-related genes in the honey bee mushroom bodies
title_full_unstemmed Mblk-1/E93, an ecdysone related-transcription factor, targets synaptic plasticity-related genes in the honey bee mushroom bodies
title_short Mblk-1/E93, an ecdysone related-transcription factor, targets synaptic plasticity-related genes in the honey bee mushroom bodies
title_sort mblk-1/e93, an ecdysone related-transcription factor, targets synaptic plasticity-related genes in the honey bee mushroom bodies
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9734179/
https://www.ncbi.nlm.nih.gov/pubmed/36494426
http://dx.doi.org/10.1038/s41598-022-23329-z
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