Single-cell analysis of the amphioxus hepatic caecum and vertebrate liver reveals genetic mechanisms of vertebrate liver evolution

doi:10.1038/s41559-024-02510-9

. 2024 Aug 16.

doi: 10.1038/s41559-024-02510-9. Online ahead of print.

Single-cell analysis of the amphioxus hepatic caecum and vertebrate liver reveals genetic mechanisms of vertebrate liver evolution

Baosheng Wu^#^{1

2}, Wenjie Xu^#¹, Kunjin Wu^#^{3

4}, Ye Li^#¹, Mingliang Hu^#¹, Chenguang Feng¹, Chenglong Zhu¹, Jiangmin Zheng¹, Xinxin Cui¹, Jing Li^{3

4}, Deqian Fan¹, Fenghua Zhang¹, Yuxuan Liu¹, Jinping Chen², Chang Liu^{3

4}, Guang Li⁵, Qiang Qiu⁶, Kai Qu^{7

8}, Wen Wang^{9

10}, Kun Wang^{11

12}

Affiliations

¹ Shaanxi Key Laboratory of Qinling Ecological Intelligent Monitoring and Protection, School of Ecology and Environment, Northwestern Polytechnical University, Xi'an, China.
² Guangdong Key Laboratory of Animal Conservation and Resource Utilization, Institute of Zoology, Guangdong Academy of Sciences, Guangzhou, China.
³ Key Laboratory of Surgical Critical Care and Life Support (Xi'an Jiaotong University), Ministry of Education, Xi'an, China.
⁴ Department of Hepatobiliary Surgery and Liver Transplantation, The Second Affiliated Hospital of Xi'an Jiaotong University, Xi'an, China.
⁵ State Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, China. guangli@xmu.edu.cn.
⁶ Shaanxi Key Laboratory of Qinling Ecological Intelligent Monitoring and Protection, School of Ecology and Environment, Northwestern Polytechnical University, Xi'an, China. qiuqiang@lzu.edu.cn.
⁷ Key Laboratory of Surgical Critical Care and Life Support (Xi'an Jiaotong University), Ministry of Education, Xi'an, China. qukai001@xjtu.edu.cn.
⁸ Department of Hepatobiliary Surgery and Liver Transplantation, The Second Affiliated Hospital of Xi'an Jiaotong University, Xi'an, China. qukai001@xjtu.edu.cn.
⁹ Shaanxi Key Laboratory of Qinling Ecological Intelligent Monitoring and Protection, School of Ecology and Environment, Northwestern Polytechnical University, Xi'an, China. wenwang@nwpu.edu.cn.
¹⁰ New Cornerstone Science Laboratory, Xi'an, China. wenwang@nwpu.edu.cn.
¹¹ Shaanxi Key Laboratory of Qinling Ecological Intelligent Monitoring and Protection, School of Ecology and Environment, Northwestern Polytechnical University, Xi'an, China. wangkun@nwpu.edu.cn.
¹² Laboratory for Marine Biology and Biotechnology, Qingdao Marine Science and Technology Center, Qingdao, China. wangkun@nwpu.edu.cn.

^# Contributed equally.

PMID: 39152328
DOI: 10.1038/s41559-024-02510-9

Single-cell analysis of the amphioxus hepatic caecum and vertebrate liver reveals genetic mechanisms of vertebrate liver evolution

Baosheng Wu et al. Nat Ecol Evol. 2024.

. 2024 Aug 16.

doi: 10.1038/s41559-024-02510-9. Online ahead of print.

Authors

Affiliations

¹ Shaanxi Key Laboratory of Qinling Ecological Intelligent Monitoring and Protection, School of Ecology and Environment, Northwestern Polytechnical University, Xi'an, China.
² Guangdong Key Laboratory of Animal Conservation and Resource Utilization, Institute of Zoology, Guangdong Academy of Sciences, Guangzhou, China.
³ Key Laboratory of Surgical Critical Care and Life Support (Xi'an Jiaotong University), Ministry of Education, Xi'an, China.
⁴ Department of Hepatobiliary Surgery and Liver Transplantation, The Second Affiliated Hospital of Xi'an Jiaotong University, Xi'an, China.
⁵ State Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, China. guangli@xmu.edu.cn.
⁶ Shaanxi Key Laboratory of Qinling Ecological Intelligent Monitoring and Protection, School of Ecology and Environment, Northwestern Polytechnical University, Xi'an, China. qiuqiang@lzu.edu.cn.
⁷ Key Laboratory of Surgical Critical Care and Life Support (Xi'an Jiaotong University), Ministry of Education, Xi'an, China. qukai001@xjtu.edu.cn.
⁸ Department of Hepatobiliary Surgery and Liver Transplantation, The Second Affiliated Hospital of Xi'an Jiaotong University, Xi'an, China. qukai001@xjtu.edu.cn.
⁹ Shaanxi Key Laboratory of Qinling Ecological Intelligent Monitoring and Protection, School of Ecology and Environment, Northwestern Polytechnical University, Xi'an, China. wenwang@nwpu.edu.cn.
¹⁰ New Cornerstone Science Laboratory, Xi'an, China. wenwang@nwpu.edu.cn.
¹¹ Shaanxi Key Laboratory of Qinling Ecological Intelligent Monitoring and Protection, School of Ecology and Environment, Northwestern Polytechnical University, Xi'an, China. wangkun@nwpu.edu.cn.
¹² Laboratory for Marine Biology and Biotechnology, Qingdao Marine Science and Technology Center, Qingdao, China. wangkun@nwpu.edu.cn.

^# Contributed equally.

PMID: 39152328
DOI: 10.1038/s41559-024-02510-9

Abstract

The evolution of the vertebrate liver is a prime example of the evolution of complex organs, yet the driving genetic factors behind it remain unknown. Here we study the evolutionary genetics of liver by comparing the amphioxus hepatic caecum and the vertebrate liver, as well as examining the functional transition within vertebrates. Using in vivo and in vitro experiments, single-cell/nucleus RNA-seq data and gene knockout experiments, we confirm that the amphioxus hepatic caecum and vertebrate liver are homologous organs and show that the emergence of ohnologues from two rounds of whole-genome duplications greatly contributed to the functional complexity of the vertebrate liver. Two ohnologues, kdr and flt4, play an important role in the development of liver sinusoidal endothelial cells. In addition, we found that liver-related functions such as coagulation and bile production evolved in a step-by-step manner, with gene duplicates playing a crucial role. We reconstructed the genetic footprint of the transfer of haem detoxification from the liver to the spleen during vertebrate evolution. Together, these findings challenge the previous hypothesis that organ evolution is primarily driven by regulatory elements, underscoring the importance of gene duplicates in the emergence and diversification of a complex organ.

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References

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[1] Gregory, T. R. The evolution of complex organs. Evolution 1, 358–389 (2008).

[2] Gregory, T. R. The evolution of complex organs. Evolution 1, 358–389 (2008).

[3] Kawakami, K. & Murakami, Y. Preface to vertebrate brains: evolution, structures and functions. Dev. Growth Differ. 59, 160–162 (2017). - PubMed - DOI

[4] Kawakami, K. & Murakami, Y. Preface to vertebrate brains: evolution, structures and functions. Dev. Growth Differ. 59, 160–162 (2017). - PubMed - DOI

[5] Malarkey, D. E., Johnson, K., Ryan, L., Boorman, G. & Maronpot, R. R. New insights into functional aspects of liver morphology. Toxicol. Pathol. 33, 27–34 (2005). - PubMed - DOI

[6] Malarkey, D. E., Johnson, K., Ryan, L., Boorman, G. & Maronpot, R. R. New insights into functional aspects of liver morphology. Toxicol. Pathol. 33, 27–34 (2005). - PubMed - DOI

[7] Carroll, S. B. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134, 25–36 (2008). - PubMed - DOI

[8] Carroll, S. B. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134, 25–36 (2008). - PubMed - DOI

[9] Hoekstra, H. E. & Coyne, J. A. The locus of evolution: evo devo and the genetics of adaptation. Evolution 61, 995–1016 (2007). - PubMed - DOI

[10] Hoekstra, H. E. & Coyne, J. A. The locus of evolution: evo devo and the genetics of adaptation. Evolution 61, 995–1016 (2007). - PubMed - DOI

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Single-cell analysis of the amphioxus hepatic caecum and vertebrate liver reveals genetic mechanisms of vertebrate liver evolution

Affiliations

Single-cell analysis of the amphioxus hepatic caecum and vertebrate liver reveals genetic mechanisms of vertebrate liver evolution

Authors

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Abstract

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