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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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 |
work_keys_str_mv |
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