Gene Regulation during Carapacial Ridge Development of <i>Mauremys reevesii</i>: The Development of Carapacial Ridge, Ribs and Scutes
The unique topological structure of a turtle shell, including the special ribs–scapula relationship, is an evolutionarily novelty of amniotes. The carapacial ridge is a key embryonic tissue for inducing turtle carapace morphologenesis. However, the gene expression profiles and molecular regulatory m...
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| Format: | Article |
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MDPI AG
2022-09-01
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| Series: | Genes |
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| Online Access: | https://www.mdpi.com/2073-4425/13/9/1676 |
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| author | Jiayu Yang Yingying Xia Shaohu Li Tingting Chen Jilong Zhang Zhiyuan Weng Huiwei Zheng Minxuan Jin Chuanhe Bao Shiping Su Yangyang Liang Jun Zhang |
| author_facet | Jiayu Yang Yingying Xia Shaohu Li Tingting Chen Jilong Zhang Zhiyuan Weng Huiwei Zheng Minxuan Jin Chuanhe Bao Shiping Su Yangyang Liang Jun Zhang |
| author_sort | Jiayu Yang |
| collection | DOAJ |
| description | The unique topological structure of a turtle shell, including the special ribs–scapula relationship, is an evolutionarily novelty of amniotes. The carapacial ridge is a key embryonic tissue for inducing turtle carapace morphologenesis. However, the gene expression profiles and molecular regulatory mechanisms that occur during carapacial ridge development, including the regulation mechanism of rib axis arrest, the development mechanism of the carapacial ridge, and the differentiation between soft-shell turtles and hard-shell turtles, are not fully understood. In this study, we obtained genome-wide gene expression profiles during the carapacial ridge development of <i>Mauremys reevesii</i> using RNA-sequencing by using carapacial ridge tissues from stage 14, 15 and 16 turtle embryos. In addition, a differentially expressed genes (DEGs) analysis and a gene set enrichment analysis (GSEA) of three comparison groups were performed. Furthermore, a Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis was used to analyze the pathway enrichment of the differentially expressed genes of the three comparative groups. The result displayed that the Wnt signaling pathway was substantially enriched in the CrTK14 vs. the CrTK15 comparison group, while the Hedgehog signaling pathway was significantly enriched in the CrTK15 vs. the CrTK16 group. Moreover, the regulatory network of the Wnt signaling pathway showed that Wnt signaling pathways might interact with <i>Fgfs</i>, <i>Bmps</i>, and <i>Shh</i> to form a regulatory network to regulate the carapacial ridge development. Next, WGCNA was used to cluster and analyze the expression genes during the carapacial ridge development of <i>M. reevesii</i> and <i>P. sinensis</i>. Further, a KEGG functional enrichment analysis of the carapacial ridge correlation gene modules was performed. Interesting, these results indicated that the Wnt signaling pathway and the MAPK signaling pathway were significantly enriched in the gene modules that were highly correlated with the stage 14 and stage 15 carapacial ridge samples of the two species. The Hedgehog signaling pathway was significantly enriched in the modules that were strongly correlated with the stage 16 carapacial ridge samples of <i>M. reevesii</i>, however, the PI3K-Akt signaling and the TGF-β signaling pathways were significantly enriched in the modules that were strongly correlated with the stage 16 carapacial ridge samples of <i>P. sinensis</i>. Furthermore, we found that those modules that were strongly correlated with the stage 14 carapacial ridge samples of <i>M. reevesii</i> and <i>P. sinensis</i> contained <i>Wnts</i> and <i>Lef1</i>. While the navajo white 3 module which was strongly correlated with the stage 16 carapacial ridge samples of <i>M. reevesii</i> contained <i>Shh</i> and <i>Ptchs</i>. The dark green module strongly correlated with the stage 16 carapacial ridge samples of <i>P. sinensis which</i> contained <i>Col1a1</i>, <i>Col1a2</i>, and <i>Itga8</i>. Consequently, this study systematically revealed the signaling pathways and genes that regulate the carapacial ridge development of <i>M. reevesii</i> and <i>P. sinensis</i>, which provides new insights for revealing the molecular mechanism that is underlying the turtle’s body structure. |
| first_indexed | 2024-03-09T23:55:53Z |
| format | Article |
| id | doaj.art-ceccca7902cd432c878a62f3379fbd5b |
| institution | Directory Open Access Journal |
| issn | 2073-4425 |
| language | English |
| last_indexed | 2024-03-09T23:55:53Z |
| publishDate | 2022-09-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Genes |
| spelling | doaj.art-ceccca7902cd432c878a62f3379fbd5b2023-11-23T16:26:21ZengMDPI AGGenes2073-44252022-09-01139167610.3390/genes13091676Gene Regulation during Carapacial Ridge Development of <i>Mauremys reevesii</i>: The Development of Carapacial Ridge, Ribs and ScutesJiayu Yang0Yingying Xia1Shaohu Li2Tingting Chen3Jilong Zhang4Zhiyuan Weng5Huiwei Zheng6Minxuan Jin7Chuanhe Bao8Shiping Su9Yangyang Liang10Jun Zhang11College of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, ChinaCollege of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, ChinaCollege of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, ChinaCollege of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, ChinaCollege of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, ChinaCollege of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, ChinaCollege of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, ChinaCollege of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, ChinaCollege of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, ChinaCollege of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, ChinaFisheries Research Institute, Anhui Academy of Agricultural Sciences, Hefei 230041, ChinaCollege of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, ChinaThe unique topological structure of a turtle shell, including the special ribs–scapula relationship, is an evolutionarily novelty of amniotes. The carapacial ridge is a key embryonic tissue for inducing turtle carapace morphologenesis. However, the gene expression profiles and molecular regulatory mechanisms that occur during carapacial ridge development, including the regulation mechanism of rib axis arrest, the development mechanism of the carapacial ridge, and the differentiation between soft-shell turtles and hard-shell turtles, are not fully understood. In this study, we obtained genome-wide gene expression profiles during the carapacial ridge development of <i>Mauremys reevesii</i> using RNA-sequencing by using carapacial ridge tissues from stage 14, 15 and 16 turtle embryos. In addition, a differentially expressed genes (DEGs) analysis and a gene set enrichment analysis (GSEA) of three comparison groups were performed. Furthermore, a Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis was used to analyze the pathway enrichment of the differentially expressed genes of the three comparative groups. The result displayed that the Wnt signaling pathway was substantially enriched in the CrTK14 vs. the CrTK15 comparison group, while the Hedgehog signaling pathway was significantly enriched in the CrTK15 vs. the CrTK16 group. Moreover, the regulatory network of the Wnt signaling pathway showed that Wnt signaling pathways might interact with <i>Fgfs</i>, <i>Bmps</i>, and <i>Shh</i> to form a regulatory network to regulate the carapacial ridge development. Next, WGCNA was used to cluster and analyze the expression genes during the carapacial ridge development of <i>M. reevesii</i> and <i>P. sinensis</i>. Further, a KEGG functional enrichment analysis of the carapacial ridge correlation gene modules was performed. Interesting, these results indicated that the Wnt signaling pathway and the MAPK signaling pathway were significantly enriched in the gene modules that were highly correlated with the stage 14 and stage 15 carapacial ridge samples of the two species. The Hedgehog signaling pathway was significantly enriched in the modules that were strongly correlated with the stage 16 carapacial ridge samples of <i>M. reevesii</i>, however, the PI3K-Akt signaling and the TGF-β signaling pathways were significantly enriched in the modules that were strongly correlated with the stage 16 carapacial ridge samples of <i>P. sinensis</i>. Furthermore, we found that those modules that were strongly correlated with the stage 14 carapacial ridge samples of <i>M. reevesii</i> and <i>P. sinensis</i> contained <i>Wnts</i> and <i>Lef1</i>. While the navajo white 3 module which was strongly correlated with the stage 16 carapacial ridge samples of <i>M. reevesii</i> contained <i>Shh</i> and <i>Ptchs</i>. The dark green module strongly correlated with the stage 16 carapacial ridge samples of <i>P. sinensis which</i> contained <i>Col1a1</i>, <i>Col1a2</i>, and <i>Itga8</i>. Consequently, this study systematically revealed the signaling pathways and genes that regulate the carapacial ridge development of <i>M. reevesii</i> and <i>P. sinensis</i>, which provides new insights for revealing the molecular mechanism that is underlying the turtle’s body structure.https://www.mdpi.com/2073-4425/13/9/1676<i>Mauremys reevesii</i>carapace ridgeturtleWnt signaling pathwayHedgehog signaling pathway |
| spellingShingle | Jiayu Yang Yingying Xia Shaohu Li Tingting Chen Jilong Zhang Zhiyuan Weng Huiwei Zheng Minxuan Jin Chuanhe Bao Shiping Su Yangyang Liang Jun Zhang Gene Regulation during Carapacial Ridge Development of <i>Mauremys reevesii</i>: The Development of Carapacial Ridge, Ribs and Scutes Genes <i>Mauremys reevesii</i> carapace ridge turtle Wnt signaling pathway Hedgehog signaling pathway |
| title | Gene Regulation during Carapacial Ridge Development of <i>Mauremys reevesii</i>: The Development of Carapacial Ridge, Ribs and Scutes |
| title_full | Gene Regulation during Carapacial Ridge Development of <i>Mauremys reevesii</i>: The Development of Carapacial Ridge, Ribs and Scutes |
| title_fullStr | Gene Regulation during Carapacial Ridge Development of <i>Mauremys reevesii</i>: The Development of Carapacial Ridge, Ribs and Scutes |
| title_full_unstemmed | Gene Regulation during Carapacial Ridge Development of <i>Mauremys reevesii</i>: The Development of Carapacial Ridge, Ribs and Scutes |
| title_short | Gene Regulation during Carapacial Ridge Development of <i>Mauremys reevesii</i>: The Development of Carapacial Ridge, Ribs and Scutes |
| title_sort | gene regulation during carapacial ridge development of i mauremys reevesii i the development of carapacial ridge ribs and scutes |
| topic | <i>Mauremys reevesii</i> carapace ridge turtle Wnt signaling pathway Hedgehog signaling pathway |
| url | https://www.mdpi.com/2073-4425/13/9/1676 |
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