Evolution of the gene regulatory network of body axis by enhancer hijacking in amphioxus
A central goal of evolutionary developmental biology is to decipher the evolutionary pattern of gene regulatory networks (GRNs) that control embryonic development, and the mechanism underlying GRNs evolution. The Nodal signaling that governs the body axes of deuterostomes exhibits a conserved GRN or...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2024-01-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/89615 |
| _version_ | 1797353194088562688 |
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| author | Chenggang Shi Shuang Chen Huimin Liu Rongrong Pan Shiqi Li Yanhui Wang Xiaotong Wu Jingjing Li Xuewen Li Chaofan Xing Xian Liu Yiquan Wang Qingming Qu Guang Li |
| author_facet | Chenggang Shi Shuang Chen Huimin Liu Rongrong Pan Shiqi Li Yanhui Wang Xiaotong Wu Jingjing Li Xuewen Li Chaofan Xing Xian Liu Yiquan Wang Qingming Qu Guang Li |
| author_sort | Chenggang Shi |
| collection | DOAJ |
| description | A central goal of evolutionary developmental biology is to decipher the evolutionary pattern of gene regulatory networks (GRNs) that control embryonic development, and the mechanism underlying GRNs evolution. The Nodal signaling that governs the body axes of deuterostomes exhibits a conserved GRN orchestrated principally by Nodal, Gdf1/3, and Lefty. Here we show that this GRN has been rewired in cephalochordate amphioxus. We found that while the amphioxus Gdf1/3 ortholog exhibited nearly no embryonic expression, its duplicate Gdf1/3-like, linked to Lefty, was zygotically expressed in a similar pattern as Lefty. Consistent with this, while Gdf1/3-like mutants showed defects in axial development, Gdf1/3 mutants did not. Further transgenic analyses showed that the intergenic region between Gdf1/3-like and Lefty could drive reporter gene expression as that of the two genes. These results indicated that Gdf1/3-like has taken over the axial development role of Gdf1/3 in amphioxus, possibly through hijacking Lefty enhancers. We finally demonstrated that, to compensate for the loss of maternal Gdf1/3 expression, Nodal has become an indispensable maternal factor in amphioxus and its maternal mutants caused axial defects as Gdf1/3-like mutants. We therefore demonstrated a case that the evolution of GRNs could be triggered by enhancer hijacking events. This pivotal event has allowed the emergence of a new GRN in extant amphioxus, presumably through a stepwise process. In addition, the co-expression of Gdf1/3-like and Lefty achieved by a shared regulatory region may have provided robustness during body axis formation, which provides a selection-based hypothesis for the phenomena called developmental system drift. |
| first_indexed | 2024-03-08T13:27:36Z |
| format | Article |
| id | doaj.art-794160da2f264070a31d7534a35a4cc6 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-03-08T13:27:36Z |
| publishDate | 2024-01-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-794160da2f264070a31d7534a35a4cc62024-01-17T13:47:29ZengeLife Sciences Publications LtdeLife2050-084X2024-01-011310.7554/eLife.89615Evolution of the gene regulatory network of body axis by enhancer hijacking in amphioxusChenggang Shi0https://orcid.org/0000-0002-5592-2761Shuang Chen1Huimin Liu2Rongrong Pan3Shiqi Li4Yanhui Wang5Xiaotong Wu6Jingjing Li7Xuewen Li8Chaofan Xing9Xian Liu10Yiquan Wang11Qingming Qu12https://orcid.org/0000-0002-8291-8493Guang Li13https://orcid.org/0000-0002-5543-5349State Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, ChinaA central goal of evolutionary developmental biology is to decipher the evolutionary pattern of gene regulatory networks (GRNs) that control embryonic development, and the mechanism underlying GRNs evolution. The Nodal signaling that governs the body axes of deuterostomes exhibits a conserved GRN orchestrated principally by Nodal, Gdf1/3, and Lefty. Here we show that this GRN has been rewired in cephalochordate amphioxus. We found that while the amphioxus Gdf1/3 ortholog exhibited nearly no embryonic expression, its duplicate Gdf1/3-like, linked to Lefty, was zygotically expressed in a similar pattern as Lefty. Consistent with this, while Gdf1/3-like mutants showed defects in axial development, Gdf1/3 mutants did not. Further transgenic analyses showed that the intergenic region between Gdf1/3-like and Lefty could drive reporter gene expression as that of the two genes. These results indicated that Gdf1/3-like has taken over the axial development role of Gdf1/3 in amphioxus, possibly through hijacking Lefty enhancers. We finally demonstrated that, to compensate for the loss of maternal Gdf1/3 expression, Nodal has become an indispensable maternal factor in amphioxus and its maternal mutants caused axial defects as Gdf1/3-like mutants. We therefore demonstrated a case that the evolution of GRNs could be triggered by enhancer hijacking events. This pivotal event has allowed the emergence of a new GRN in extant amphioxus, presumably through a stepwise process. In addition, the co-expression of Gdf1/3-like and Lefty achieved by a shared regulatory region may have provided robustness during body axis formation, which provides a selection-based hypothesis for the phenomena called developmental system drift.https://elifesciences.org/articles/89615gene regulatory networkNodal signalingbody axisamphioxusenhancer hijacking |
| spellingShingle | Chenggang Shi Shuang Chen Huimin Liu Rongrong Pan Shiqi Li Yanhui Wang Xiaotong Wu Jingjing Li Xuewen Li Chaofan Xing Xian Liu Yiquan Wang Qingming Qu Guang Li Evolution of the gene regulatory network of body axis by enhancer hijacking in amphioxus eLife gene regulatory network Nodal signaling body axis amphioxus enhancer hijacking |
| title | Evolution of the gene regulatory network of body axis by enhancer hijacking in amphioxus |
| title_full | Evolution of the gene regulatory network of body axis by enhancer hijacking in amphioxus |
| title_fullStr | Evolution of the gene regulatory network of body axis by enhancer hijacking in amphioxus |
| title_full_unstemmed | Evolution of the gene regulatory network of body axis by enhancer hijacking in amphioxus |
| title_short | Evolution of the gene regulatory network of body axis by enhancer hijacking in amphioxus |
| title_sort | evolution of the gene regulatory network of body axis by enhancer hijacking in amphioxus |
| topic | gene regulatory network Nodal signaling body axis amphioxus enhancer hijacking |
| url | https://elifesciences.org/articles/89615 |
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