African lungfish genome sheds light on the vertebrate water-to-land transition
Open accessAbstract
Lungfishes are the closest extant relatives of tetrapods and preserve ancestral traits linked with the water-to-land transition. However, their huge genome sizes have hindered understanding of this key transition in evolution. Here, we report a 40-Gb chromosome-level assembly of the African lungfish (Protopterus annectens) genome, which is the largest genome assembly ever reported and has a contig and chromosome N50 of 1.60 Mb and 2.81 Gb, respectively. The large size of the lungfish genome is due mainly to retrotransposons. Genes with ultra-long length show similar expression levels to other genes, indicating that lungfishes have evolved high transcription efficacy to keep gene expression balanced. Together with transcriptome and experimental data, we identified potential genes and regulatory elements related to such terrestrial adaptation traits as pulmonary surfactant, anxiolytic ability, pentadactyl limbs, and pharyngeal remodeling. Our results provide insights and key resources for understanding the evolutionary pathway leading from fishes to humans.
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Wang et al. (2021) sequenced the giant genome of lungfish, the closest fish species to tetrapods.
“Wang et al. (2021) sequenced the giant genome of lungfish, the closest fish species to tetrapods, and Bi et al. (2021) sequenced the genomes of multiple early divergent ray-finned fish.”
From Ancestral developmental potentials in early bony fish contributed to vertebrate water-to-land transition (2021) · cites this paper as Wang et al. (2021)
Comparative genomic analyses from Wang et al. (2021) and Bi et al. (2021) confirmed the presence of ancestral genetic regulatory networks that likely played essential roles in the development and evolution of various biological functions related to vertebrate land invasion.
“Comparative genomic analyses from these two studies confirmed the presence of ancestral genetic regulatory networks that likely played essential roles in the development and evolution of various biological functions related to vertebrate land invasion.”
From Ancestral developmental potentials in early bony fish contributed to vertebrate water-to-land transition (2021) · cites this paper as Wang et al. (2021)
Wang et al. (2021) discovered the gradual loss of actinotrichia proteins in lungfish and tetrapods.
“They also discovered many unique changes related to the fin-to-limb transition, including a 40 amino acid fragment at the beginning of Hoxb13 lost in tetrapods, the gradual loss of actinotrichia proteins in lungfish and tetrapods, and the gain of two tetrapod-specific regulatory elements in the upper region of Hoxc10 essential for lumbar motoneuron development.”
From Ancestral developmental potentials in early bony fish contributed to vertebrate water-to-land transition (2021) · cites this paper as Wang et al. (2021)
Wang et al. (2021) identified a tetrapod-specific regulatory element, located upstream of Hoxa11, which may be a key element for the morphogenesis of the pentadactyl limb.
“In a comparative genomic study on the African lungfish genome, Wang et al. (2021) identified a tetrapod-specific regulatory element, located upstream of Hoxa11, which may be a key element for the morphogenesis of the pentadactyl limb.”
From Ancestral developmental potentials in early bony fish contributed to vertebrate water-to-land transition (2021) · cites this paper as Wang et al. (2021)
Wang et al. (2021) discovered the gain of two tetrapod-specific regulatory elements in the upper region of Hoxc10 essential for lumbar motoneuron development.
“They also discovered many unique changes related to the fin-to-limb transition, including a 40 amino acid fragment at the beginning of Hoxb13 lost in tetrapods, the gradual loss of actinotrichia proteins in lungfish and tetrapods, and the gain of two tetrapod-specific regulatory elements in the upper region of Hoxc10 essential for lumbar motoneuron development.”
From Ancestral developmental potentials in early bony fish contributed to vertebrate water-to-land transition (2021) · cites this paper as Wang et al. (2021)
The SP-C gene emerged from the ancestors of lobe-finned fish, a vertebrate group with enhanced air-breathing ability.
“The SP-C gene emerged from the ancestors of lobe-finned fish, a vertebrate group with enhanced air-breathing ability.”
From Ancestral developmental potentials in early bony fish contributed to vertebrate water-to-land transition (2021) · cites this paper as Wang et al., (2021)
The SP-A and SP-D genes emerged from the ancestors of tetrapods, indicating further improvement in the respiratory ability of terrestrial vertebrates.
“Furthermore, the SP-A and SP-D genes emerged from the ancestors of tetrapods, indicating further improvement in the respiratory ability of terrestrial vertebrates.”
From Ancestral developmental potentials in early bony fish contributed to vertebrate water-to-land transition (2021) · cites this paper as Wang et al., (2021)
The Slc34a2 gene evolved in the common ancestor of lungfish and tetrapods and is highly expressed in the lungs.
“In addition, the Slc34a2 gene, which evolved in the common ancestor of lungfish and tetrapods, is highly expressed in the lungs (Wang et al., 2021).”
From Ancestral developmental potentials in early bony fish contributed to vertebrate water-to-land transition (2021) · cites this paper as Wang et al., 2021
Wang et al. (2021) discovered a 40 amino acid fragment at the beginning of Hoxb13 lost in tetrapods.
“They also discovered many unique changes related to the fin-to-limb transition, including a 40 amino acid fragment at the beginning of Hoxb13 lost in tetrapods, the gradual loss of actinotrichia proteins in lungfish and tetrapods, and the gain of two tetrapod-specific regulatory elements in the upper region of Hoxc10 essential for lumbar motoneuron development.”
From Ancestral developmental potentials in early bony fish contributed to vertebrate water-to-land transition (2021) · cites this paper as Wang et al. (2021)
Wang et al. (2021) discovered a series of evolutionary steps that led to the evolution of genes associated with pulmonary surfactants.
“Wang et al., (2021) discovered a series of evolutionary steps that led to the evolution of genes associated with pulmonary surfactants.”
From Ancestral developmental potentials in early bony fish contributed to vertebrate water-to-land transition (2021) · cites this paper as Wang et al., (2021)
Surfactant protein B (SP-B) is the most ancient member of the SP family, appearing in the ancestors of bony fish.
“Surfactant protein B (SP-B) is the most ancient member of the SP family, appearing in the ancestors of bony fish, consistent with the finding that bony fish ancestors already had a preliminary ability to breathe air.”
From Ancestral developmental potentials in early bony fish contributed to vertebrate water-to-land transition (2021) · cites this paper as Wang et al., (2021)
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References 143 · Cited by 192
- Authors
- Wang, K., Wang, J., Zhu, C., Yang, L., Ren, Y., Ruan, J., Fan, G., Hu, J., Xu, W., Bi, X., Zhu, Y., Song, Y., Chen, H., Ma, T., Zhao, R., Jiang, H., Zhang, B., Feng, C., Yuan, Y., Gan, X., Li, Y., Zeng, H., Liu, Q., Zhang, Y., Shao, F., Hao, S., Zhang, H., Xu, X., Liu, X., Wang, D., Zhu, M., Zhang, G., Zhao, W., Qiu, Q., He, S., & Wang, W.
- Affiliations
- Northwestern Polytechnical University (CN)
- South China Agricultural University (CN)
- Chinese Academy of Sciences (CN)
- Agricultural Genomics Institute at Shenzhen (CN)
- BGI Group (China) (CN)
- Grandomics (China) (CN)
- Northwest A&F University (CN)
- Kunming Institute of Zoology (CN)
- Southwest University (CN)
- Corresponding author
- Zhao, Wenming
- Qiu, Qiang
- He, Shunping
- Wang, Wen
- ORCID
- Wang, Kun
- Wang, Jun
- Zhu, Chenglong
- Yang, Liandong
- Ren, Yandong
- Ruan, Jue
- Fan, Guangyi
- Hu, Jiang
- Xu, Wenjie
- Bi, Xupeng
- Song, Yue
- Chen, Huatao
- Ma, Tiantian
- Zhao, Ruoping
- Jiang, Haifeng
- Zhang, Bin
- Feng, Chenguang
- Yuan, Yuan
- Li, Yongxin
- Zeng, Honghui
- Liu, Qun
- Zhang, Yaolei
- Shao, Feng
- Hao, Shijie
- Zhang, He
- Xu, Xun
- Liu, Xin
- Wang, Depeng
- Zhu, Min
- Zhang, Guojie
- Zhao, Wenming
- Qiu, Qiang
- He, Shunping
- Wang, Wen
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2021-03
- Volume
- 184
- Issue
- 5
- Pages
- 1362-1376.e18
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W3128761396
- Cited by
- 192
- References
- 143
- Citations by year
- 2026: 30 · 2025: 31 · 2024: 40 · 2023: 32 · 2022: 33 · 2021: 26
- FWCI
- 19.69
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 368 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Funders
- Northwestern Polytechnical University
- Chinese Academy of Sciences (XDB13000000)
- National Natural Science Foundation of China (41876179, 31972866)
- National Key Research and Development Program of China (2018YFD0900604)
- Youth Innovation Promotion Association of the Chinese Academy of Sciences
- Villum Fonden (25900)
- Guangdong Province Higher Vocational Colleges and Schools Pearl River Scholar Funded Scheme
- State Key Laboratory of Freshwater Ecology and Biotechnology
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- African lungfish, Protopterus annectens, chromosome-level genome assembly, retrotransposons, transcriptional regulation, pulmonary surfactant, water-to-land transition, tetrapod evolution, vertebrate evolution
- MeSH terms
- Whole Genome Sequencing, Adaptation, Biological, Animals, Biological Evolution, Extremities, Fishes, Phylogeny, Respiratory System, Respiratory Physiological Phenomena, Vertebrates, Animal Fins
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