Abstract
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.
| Original language | English |
|---|---|
| Pages (from-to) | 702-709 |
| Number of pages | 8 |
| Journal | Biology Open |
| Volume | 4 |
| Issue number | 6 |
| DOIs | |
| Publication status | Published - Jun 15 2015 |
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Keywords
- Epigenetic silencing
- Gene expression
- Hox genes
- Insec
- Polycomb group genes
ASJC Scopus subject areas
- Biochemistry, Genetics and Molecular Biology(all)
- Agricultural and Biological Sciences(all)
Cite this
Short germ insects utilize both the ancestral and derived mode of polycomb group-mediated epigenetic silencing of hox genes. / Matsuoka, Yuji; Bando, Tetsuya; Watanabe, Takahito; Ishimaru, Yoshiyasu; Noji, Sumihare; Popadić, Aleksandar; Mito, Taro.
In: Biology Open, Vol. 4, No. 6, 15.06.2015, p. 702-709.Research output: Contribution to journal › Article
}
TY - JOUR
T1 - Short germ insects utilize both the ancestral and derived mode of polycomb group-mediated epigenetic silencing of hox genes
AU - Matsuoka, Yuji
AU - Bando, Tetsuya
AU - Watanabe, Takahito
AU - Ishimaru, Yoshiyasu
AU - Noji, Sumihare
AU - Popadić, Aleksandar
AU - Mito, Taro
PY - 2015/6/15
Y1 - 2015/6/15
N2 - 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.
AB - 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.
KW - Epigenetic silencing
KW - Gene expression
KW - Hox genes
KW - Insec
KW - Polycomb group genes
UR - http://www.scopus.com/inward/record.url?scp=84979708796&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=84979708796&partnerID=8YFLogxK
U2 - 10.1242/bio.201411064
DO - 10.1242/bio.201411064
M3 - Article
AN - SCOPUS:84979708796
VL - 4
SP - 702
EP - 709
JO - Biology Open
JF - Biology Open
SN - 2046-6390
IS - 6
ER -