Short germ insects utilize both the ancestral and derived mode of Polycomb group-mediated epigenetic silencing of Hox genes

In insect species that undergo long germ segmentation, such as Drosophila, all segments are specified simultaneously at the early blastoderm stage. As embryogenesis progresses, the expression boundaries of Hox genes are established by repression of gap genes, which is subsequently replaced by Polyco...

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Main Authors: Yuji Matsuoka, Tetsuya Bando, Takahito Watanabe, Yoshiyasu Ishimaru, Sumihare Noji, Aleksandar Popadić, Taro Mito
Format: Article
Language:English
Published: The Company of Biologists 2015-07-01
Series:Biology Open
Subjects:
Online Access:http://bio.biologists.org/content/4/6/702
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spelling doaj-86d7b35a4f124e89b01bb028d631d5922021-06-02T17:59:57ZengThe Company of BiologistsBiology Open2046-63902015-07-014670270910.1242/bio.201411064201411064Short germ insects utilize both the ancestral and derived mode of Polycomb group-mediated epigenetic silencing of Hox genesYuji Matsuoka0Tetsuya Bando1Takahito Watanabe2Yoshiyasu Ishimaru3Sumihare Noji4Aleksandar Popadić5Taro Mito6 Department of Life Systems, Institute of Technology and Science, The University of Tokushima Graduate School, 2-1 Minami-Jyosanjima-cho, Tokushima City, Tokushima 770-8506, Japan Department of Life Systems, Institute of Technology and Science, The University of Tokushima Graduate School, 2-1 Minami-Jyosanjima-cho, Tokushima City, Tokushima 770-8506, Japan Center for Collaboration among Agriculture, Industry and Commerce, The University of Tokushima, 2-24 Shinkura-cho, Tokushima City, Tokushima 770-8501, Japan Department of Life Systems, Institute of Technology and Science, The University of Tokushima Graduate School, 2-1 Minami-Jyosanjima-cho, Tokushima City, Tokushima 770-8506, Japan Center for Collaboration among Agriculture, Industry and Commerce, The University of Tokushima, 2-24 Shinkura-cho, Tokushima City, Tokushima 770-8501, Japan Biological Sciences Department, Wayne State University, Detroit, MI 48202, USA Department of Life Systems, Institute of Technology and Science, The University of Tokushima Graduate School, 2-1 Minami-Jyosanjima-cho, Tokushima City, Tokushima 770-8506, Japan In insect species that undergo long germ segmentation, such as Drosophila, all segments are specified simultaneously at the early blastoderm stage. As embryogenesis progresses, the expression boundaries of Hox genes are established by repression of gap genes, which is subsequently replaced by Polycomb group (PcG) silencing. At present, however, it is not known whether patterning occurs this way in a more ancestral (short germ) mode of embryogenesis, where segments are added gradually during posterior elongation. In this study, two members of the PcG family, Enhancer of zeste (E(z)) and Suppressor of zeste 12 (Su(z)12), were analyzed in the short germ cricket, Gryllus bimaculatus. Results suggest that although stepwise negative regulation by gap and PcG genes is present in anterior members of the Hox cluster, it does not account for regulation of two posterior Hox genes, abdominal-A (abd-A) and Abdominal-B (Abd-B). Instead, abd-A and Abd-B are predominantly regulated by PcG genes, which is the mode present in vertebrates. These findings suggest that an intriguing transition of the PcG-mediated silencing of Hox genes may have occurred during animal evolution. The ancestral bilaterian state may have resembled the current vertebrate mode of regulation, where PcG-mediated silencing of Hox genes occurs before their expression is initiated and is responsible for the establishment of individual expression domains. Then, during insect evolution, the repression by transcription factors may have been acquired in anterior Hox genes of short germ insects, while PcG silencing was maintained in posterior Hox genes.http://bio.biologists.org/content/4/6/702Epigenetic silencingGene expressionHox genesInsectPolycomb group genes
collection DOAJ
language English
format Article
sources DOAJ
author Yuji Matsuoka
Tetsuya Bando
Takahito Watanabe
Yoshiyasu Ishimaru
Sumihare Noji
Aleksandar Popadić
Taro Mito
spellingShingle Yuji Matsuoka
Tetsuya Bando
Takahito Watanabe
Yoshiyasu Ishimaru
Sumihare Noji
Aleksandar Popadić
Taro Mito
Short germ insects utilize both the ancestral and derived mode of Polycomb group-mediated epigenetic silencing of Hox genes
Biology Open
Epigenetic silencing
Gene expression
Hox genes
Insect
Polycomb group genes
author_facet Yuji Matsuoka
Tetsuya Bando
Takahito Watanabe
Yoshiyasu Ishimaru
Sumihare Noji
Aleksandar Popadić
Taro Mito
author_sort Yuji Matsuoka
title Short germ insects utilize both the ancestral and derived mode of Polycomb group-mediated epigenetic silencing of Hox genes
title_short Short germ insects utilize both the ancestral and derived mode of Polycomb group-mediated epigenetic silencing of Hox genes
title_full Short germ insects utilize both the ancestral and derived mode of Polycomb group-mediated epigenetic silencing of Hox genes
title_fullStr Short germ insects utilize both the ancestral and derived mode of Polycomb group-mediated epigenetic silencing of Hox genes
title_full_unstemmed Short germ insects utilize both the ancestral and derived mode of Polycomb group-mediated epigenetic silencing of Hox genes
title_sort short germ insects utilize both the ancestral and derived mode of polycomb group-mediated epigenetic silencing of hox genes
publisher The Company of Biologists
series Biology Open
issn 2046-6390
publishDate 2015-07-01
description In insect species that undergo long germ segmentation, such as Drosophila, all segments are specified simultaneously at the early blastoderm stage. As embryogenesis progresses, the expression boundaries of Hox genes are established by repression of gap genes, which is subsequently replaced by Polycomb group (PcG) silencing. At present, however, it is not known whether patterning occurs this way in a more ancestral (short germ) mode of embryogenesis, where segments are added gradually during posterior elongation. In this study, two members of the PcG family, Enhancer of zeste (E(z)) and Suppressor of zeste 12 (Su(z)12), were analyzed in the short germ cricket, Gryllus bimaculatus. Results suggest that although stepwise negative regulation by gap and PcG genes is present in anterior members of the Hox cluster, it does not account for regulation of two posterior Hox genes, abdominal-A (abd-A) and Abdominal-B (Abd-B). Instead, abd-A and Abd-B are predominantly regulated by PcG genes, which is the mode present in vertebrates. These findings suggest that an intriguing transition of the PcG-mediated silencing of Hox genes may have occurred during animal evolution. The ancestral bilaterian state may have resembled the current vertebrate mode of regulation, where PcG-mediated silencing of Hox genes occurs before their expression is initiated and is responsible for the establishment of individual expression domains. Then, during insect evolution, the repression by transcription factors may have been acquired in anterior Hox genes of short germ insects, while PcG silencing was maintained in posterior Hox genes.
topic Epigenetic silencing
Gene expression
Hox genes
Insect
Polycomb group genes
url http://bio.biologists.org/content/4/6/702
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