Single-cell RNA Sequencing Reveals Thoracolumbar Vertebra Heterogeneity and Rib-genesis in Pigs.

Jianbo LI; Ligang WANG; Dawei YU; Junfeng HAO; Longchao ZHANG; Adeniyi C ADEOLA; Bingyu MAO; Yun GAO; Shifang WU; Chunling ZHU; Yongqing ZHANG; Jilong REN; Changgai MU; David M IRWIN; Lixian WANG; Tang HAI; Haibing XIE; Yaping ZHANG

Genomics, Proteomics & Bioinformatics 2021;19(3):423-436

doi:10.1016/j.gpb.2021.09.008

Single-cell RNA Sequencing Reveals Thoracolumbar Vertebra Heterogeneity and Rib-genesis in Pigs.

Jianbo LI ¹ ; Ligang WANG ² ; Dawei YU ³ ; Junfeng HAO ⁴ ; Longchao ZHANG ² ; Adeniyi C ADEOLA ⁵ ; Bingyu MAO ⁶ ; Yun GAO ⁵ ; Shifang WU ⁵ ; Chunling ZHU ⁵ ; Yongqing ZHANG ⁷ ; Jilong REN ³ ; Changgai MU ¹ ; David M IRWIN ⁶ ; Lixian WANG ² ; Tang HAI ⁸ ; Haibing XIE ⁹ ; Yaping ZHANG ¹⁰

Affiliations

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1. State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China; Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming 650223, China.

2. Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China.

3. State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.

4. Core Facility for Protein Research, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China.

5. State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.

6. State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China; Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario M5S1A8, Canada.

7. State Key Laboratory for Molecular and Developmental Biology, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 10010, China.

8. State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China. Electronic address: haitang@ioz.ac.cn.

9. State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China. Electronic address: xiehb@mail.kiz.ac.cn.

10. State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China; Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming 650223, China; Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming 650223, China. Electronic address: zhangyp@mail.kiz.ac.cn.

Keywords

Angiogenesis; Osteogenesis; Rib-genesis; Thoracolumbar vertebra transition; scRNA-seq

Country

China

Language

English

Abstract

Development of thoracolumbar vertebra (TLV) and rib primordium (RP) is a common evolutionary feature across vertebrates, although whole-organism analysis of the expression dynamics of TLV- and RP-related genes has been lacking. Here, we investigated the single-cell transcriptome landscape of thoracic vertebra (TV), lumbar vertebra (LV), and RP cells from a pig embryo at 27 days post-fertilization (dpf) and identified six cell types with distinct gene expression signatures. In-depth dissection of the gene expression dynamics and RNA velocity revealed a coupled process of osteogenesis and angiogenesis during TLV and RP development. Further analysis of cell type-specific and strand-specific expression uncovered the extremely high level of HOXA10 3'-UTR sequence specific to osteoblasts of LV cells, which may function as anti-HOXA10-antisense by counteracting the HOXA10-antisense effect to determine TLV transition. Thus, this work provides a valuable resource for understanding embryonic osteogenesis and angiogenesis underlying vertebrate TLV and RP development at the cell type-specific resolution, which serves as a comprehensive view on the transcriptional profile of animal embryo development.

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