Organization of the Addax Major Histocompatibility Complex Provides Insights Into Ruminant Evolution
Ruminants are critical as prey in transferring solar energy fixed by plants into carnivorous species, yet the genetic signature of the driving forces leading to the evolutionary success of the huge number of ruminant species remains largely unknown. Here we report a complete DNA map of the major his...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-02-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fimmu.2020.00260/full |
| _version_ | 1819231655487864832 |
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| author | Chaokun Li Chaokun Li Rui Huang Rui Huang Fangyuan Nie Fangyuan Nie Jiujie Li Wen Zhu Xiaoqian Shi Xiaoqian Shi Yu Guo Yu Guo Yan Chen Shiyu Wang Limeng Zhang Longxin Chen Runting Li Xuefeng Liu Changming Zheng Chenglin Zhang Runlin Z. Ma Runlin Z. Ma Runlin Z. Ma |
| author_facet | Chaokun Li Chaokun Li Rui Huang Rui Huang Fangyuan Nie Fangyuan Nie Jiujie Li Wen Zhu Xiaoqian Shi Xiaoqian Shi Yu Guo Yu Guo Yan Chen Shiyu Wang Limeng Zhang Longxin Chen Runting Li Xuefeng Liu Changming Zheng Chenglin Zhang Runlin Z. Ma Runlin Z. Ma Runlin Z. Ma |
| author_sort | Chaokun Li |
| collection | DOAJ |
| description | Ruminants are critical as prey in transferring solar energy fixed by plants into carnivorous species, yet the genetic signature of the driving forces leading to the evolutionary success of the huge number of ruminant species remains largely unknown. Here we report a complete DNA map of the major histocompatibility complex (MHC) of the addax (Addax nasomaculatus) genome by sequencing a total of 47 overlapping BAC clones previously mapped to cover the MHC region. The addax MHC is composed of 3,224,151 nucleotides, harboring a total of 150 coding genes, 50 tRNA genes, and 14 non-coding RNA genes. The organization of addax MHC was found to be highly conserved to those of sheep and cattle, highlighted by a large piece of chromosome inversion that divided the MHC class II into IIa and IIb subregions. It is now highly possible that all of the ruminant species in the family of Bovidae carry the same chromosome inversion in the MHC region, inherited from a common ancestor of ruminants. Phylogenetic analysis indicated that DY, a ruminant-specific gene located at the boundary of the inversion and highly expressed in dendritic cells, was possibly evolved from DQ, with an estimated divergence time ~140 million years ago. Homology modeling showed that the overall predicted structure of addax DY was similar to that of HLA-DQ2. However, the pocket properties of P1, P4, P6, and P9, which were critical for antigen binding in the addax DY, showed certain distinctive features. Structural analysis suggested that the populations of peptide antigens presented by addax DY and HLA-DQ2 were quite diverse, which in theory could serve to promote microbial regulation in the rumen by ruminant species, contributing to enhanced grass utilization ability. In summary, the results of our study helped to enhance our understanding of the MHC evolution and provided additional supportive evidence to our previous hypothesis that an ancient chromosome inversion in the MHC region of the last common ancestor of ruminants may have contributed to the evolutionary success of current ruminants on our planet. |
| first_indexed | 2024-12-23T11:48:25Z |
| format | Article |
| id | doaj.art-719f54e8b3bf43f8aeeab79c66d07838 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-12-23T11:48:25Z |
| publishDate | 2020-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-719f54e8b3bf43f8aeeab79c66d078382022-12-21T17:48:16ZengFrontiers Media S.A.Frontiers in Immunology1664-32242020-02-011110.3389/fimmu.2020.00260508833Organization of the Addax Major Histocompatibility Complex Provides Insights Into Ruminant EvolutionChaokun Li0Chaokun Li1Rui Huang2Rui Huang3Fangyuan Nie4Fangyuan Nie5Jiujie Li6Wen Zhu7Xiaoqian Shi8Xiaoqian Shi9Yu Guo10Yu Guo11Yan Chen12Shiyu Wang13Limeng Zhang14Longxin Chen15Runting Li16Xuefeng Liu17Changming Zheng18Chenglin Zhang19Runlin Z. Ma20Runlin Z. Ma21Runlin Z. Ma22School of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, ChinaSchool of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, ChinaSchool of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, ChinaSchool of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaSchool of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaSchool of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, ChinaSchool of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, ChinaSchool of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaSchool of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaMolecular Biology Laboratory of Zhengzhou Normal University, Zhengzhou, ChinaMolecular Biology Laboratory of Zhengzhou Normal University, Zhengzhou, ChinaMolecular Biology Laboratory of Zhengzhou Normal University, Zhengzhou, ChinaBeijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo, Beijing, ChinaBeijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo, Beijing, ChinaBeijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo, Beijing, ChinaSchool of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, ChinaMolecular Biology Laboratory of Zhengzhou Normal University, Zhengzhou, ChinaRuminants are critical as prey in transferring solar energy fixed by plants into carnivorous species, yet the genetic signature of the driving forces leading to the evolutionary success of the huge number of ruminant species remains largely unknown. Here we report a complete DNA map of the major histocompatibility complex (MHC) of the addax (Addax nasomaculatus) genome by sequencing a total of 47 overlapping BAC clones previously mapped to cover the MHC region. The addax MHC is composed of 3,224,151 nucleotides, harboring a total of 150 coding genes, 50 tRNA genes, and 14 non-coding RNA genes. The organization of addax MHC was found to be highly conserved to those of sheep and cattle, highlighted by a large piece of chromosome inversion that divided the MHC class II into IIa and IIb subregions. It is now highly possible that all of the ruminant species in the family of Bovidae carry the same chromosome inversion in the MHC region, inherited from a common ancestor of ruminants. Phylogenetic analysis indicated that DY, a ruminant-specific gene located at the boundary of the inversion and highly expressed in dendritic cells, was possibly evolved from DQ, with an estimated divergence time ~140 million years ago. Homology modeling showed that the overall predicted structure of addax DY was similar to that of HLA-DQ2. However, the pocket properties of P1, P4, P6, and P9, which were critical for antigen binding in the addax DY, showed certain distinctive features. Structural analysis suggested that the populations of peptide antigens presented by addax DY and HLA-DQ2 were quite diverse, which in theory could serve to promote microbial regulation in the rumen by ruminant species, contributing to enhanced grass utilization ability. In summary, the results of our study helped to enhance our understanding of the MHC evolution and provided additional supportive evidence to our previous hypothesis that an ancient chromosome inversion in the MHC region of the last common ancestor of ruminants may have contributed to the evolutionary success of current ruminants on our planet.https://www.frontiersin.org/article/10.3389/fimmu.2020.00260/fullMHCAddax nasomaculatusruminantchromosome inversionevolutionDY |
| spellingShingle | Chaokun Li Chaokun Li Rui Huang Rui Huang Fangyuan Nie Fangyuan Nie Jiujie Li Wen Zhu Xiaoqian Shi Xiaoqian Shi Yu Guo Yu Guo Yan Chen Shiyu Wang Limeng Zhang Longxin Chen Runting Li Xuefeng Liu Changming Zheng Chenglin Zhang Runlin Z. Ma Runlin Z. Ma Runlin Z. Ma Organization of the Addax Major Histocompatibility Complex Provides Insights Into Ruminant Evolution Frontiers in Immunology MHC Addax nasomaculatus ruminant chromosome inversion evolution DY |
| title | Organization of the Addax Major Histocompatibility Complex Provides Insights Into Ruminant Evolution |
| title_full | Organization of the Addax Major Histocompatibility Complex Provides Insights Into Ruminant Evolution |
| title_fullStr | Organization of the Addax Major Histocompatibility Complex Provides Insights Into Ruminant Evolution |
| title_full_unstemmed | Organization of the Addax Major Histocompatibility Complex Provides Insights Into Ruminant Evolution |
| title_short | Organization of the Addax Major Histocompatibility Complex Provides Insights Into Ruminant Evolution |
| title_sort | organization of the addax major histocompatibility complex provides insights into ruminant evolution |
| topic | MHC Addax nasomaculatus ruminant chromosome inversion evolution DY |
| url | https://www.frontiersin.org/article/10.3389/fimmu.2020.00260/full |
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