Functional annotation of the cattle genome through systematic discovery and characterization of chromatin states and butyrate-induced variations
Abstract Background The functional annotation of genomes, including chromatin accessibility and modifications, is important for understanding and effectively utilizing the increased amount of genome sequences reported. However, while such annotation has been well explored in a diverse set of tissues...
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| Format: | Article |
| Language: | English |
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BMC
2019-08-01
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| Series: | BMC Biology |
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| Online Access: | http://link.springer.com/article/10.1186/s12915-019-0687-8 |
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| author | Lingzhao Fang Shuli Liu Mei Liu Xiaolong Kang Shudai Lin Bingjie Li Erin E. Connor Ransom L. Baldwin Albert Tenesa Li Ma George E. Liu Cong-jun Li |
| author_facet | Lingzhao Fang Shuli Liu Mei Liu Xiaolong Kang Shudai Lin Bingjie Li Erin E. Connor Ransom L. Baldwin Albert Tenesa Li Ma George E. Liu Cong-jun Li |
| author_sort | Lingzhao Fang |
| collection | DOAJ |
| description | Abstract Background The functional annotation of genomes, including chromatin accessibility and modifications, is important for understanding and effectively utilizing the increased amount of genome sequences reported. However, while such annotation has been well explored in a diverse set of tissues and cell types in human and model organisms, relatively little data are available for livestock genomes, hindering our understanding of complex trait variation, domestication, and adaptive evolution. Here, we present the first complete global landscape of regulatory elements in cattle and explore the dynamics of chromatin states in rumen epithelial cells induced by the rumen developmental regulator—butyrate. Results We established the first global map of regulatory elements (15 chromatin states) and defined their coordinated activities in cattle, through genome-wide profiling for six histone modifications, RNA polymerase II, CTCF-binding sites, DNA accessibility, DNA methylation, and transcriptome in rumen epithelial primary cells (REPC), rumen tissues, and Madin-Darby bovine kidney epithelial cells (MDBK). We demonstrated that each chromatin state exhibited specific enrichment for sequence ontology, transcription, methylation, trait-associated variants, gene expression-associated variants, selection signatures, and evolutionarily conserved elements, implying distinct biological functions. After butyrate treatments, we observed that the weak enhancers and flanking active transcriptional start sites (TSS) were the most dynamic chromatin states, occurred concomitantly with significant alterations in gene expression and DNA methylation, which was significantly associated with heifer conception rate and stature economic traits. Conclusion Our results demonstrate the crucial role of functional genome annotation for understanding genome regulation, complex trait variation, and adaptive evolution in livestock. Using butyrate to induce the dynamics of the epigenomic landscape, we were able to establish the correlation among nutritional elements, chromatin states, gene activities, and phenotypic outcomes. |
| first_indexed | 2024-12-24T00:12:47Z |
| format | Article |
| id | doaj.art-9a83f8325feb47549d4e381f93e5700c |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-12-24T00:12:47Z |
| publishDate | 2019-08-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-9a83f8325feb47549d4e381f93e5700c2022-12-21T17:24:51ZengBMCBMC Biology1741-70072019-08-0117111610.1186/s12915-019-0687-8Functional annotation of the cattle genome through systematic discovery and characterization of chromatin states and butyrate-induced variationsLingzhao Fang0Shuli Liu1Mei Liu2Xiaolong Kang3Shudai Lin4Bingjie Li5Erin E. Connor6Ransom L. Baldwin7Albert Tenesa8Li Ma9George E. Liu10Cong-jun Li11Animal Genomics and Improvement Laboratory, BARC, Agricultural Research Service, USDAAnimal Genomics and Improvement Laboratory, BARC, Agricultural Research Service, USDAAnimal Genomics and Improvement Laboratory, BARC, Agricultural Research Service, USDAAnimal Genomics and Improvement Laboratory, BARC, Agricultural Research Service, USDAAnimal Genomics and Improvement Laboratory, BARC, Agricultural Research Service, USDAAnimal Genomics and Improvement Laboratory, BARC, Agricultural Research Service, USDAAnimal Genomics and Improvement Laboratory, BARC, Agricultural Research Service, USDAAnimal Genomics and Improvement Laboratory, BARC, Agricultural Research Service, USDAThe Roslin Institute, University of EdinburghDepartment of Animal and Avian Sciences, University of MarylandAnimal Genomics and Improvement Laboratory, BARC, Agricultural Research Service, USDAAnimal Genomics and Improvement Laboratory, BARC, Agricultural Research Service, USDAAbstract Background The functional annotation of genomes, including chromatin accessibility and modifications, is important for understanding and effectively utilizing the increased amount of genome sequences reported. However, while such annotation has been well explored in a diverse set of tissues and cell types in human and model organisms, relatively little data are available for livestock genomes, hindering our understanding of complex trait variation, domestication, and adaptive evolution. Here, we present the first complete global landscape of regulatory elements in cattle and explore the dynamics of chromatin states in rumen epithelial cells induced by the rumen developmental regulator—butyrate. Results We established the first global map of regulatory elements (15 chromatin states) and defined their coordinated activities in cattle, through genome-wide profiling for six histone modifications, RNA polymerase II, CTCF-binding sites, DNA accessibility, DNA methylation, and transcriptome in rumen epithelial primary cells (REPC), rumen tissues, and Madin-Darby bovine kidney epithelial cells (MDBK). We demonstrated that each chromatin state exhibited specific enrichment for sequence ontology, transcription, methylation, trait-associated variants, gene expression-associated variants, selection signatures, and evolutionarily conserved elements, implying distinct biological functions. After butyrate treatments, we observed that the weak enhancers and flanking active transcriptional start sites (TSS) were the most dynamic chromatin states, occurred concomitantly with significant alterations in gene expression and DNA methylation, which was significantly associated with heifer conception rate and stature economic traits. Conclusion Our results demonstrate the crucial role of functional genome annotation for understanding genome regulation, complex trait variation, and adaptive evolution in livestock. Using butyrate to induce the dynamics of the epigenomic landscape, we were able to establish the correlation among nutritional elements, chromatin states, gene activities, and phenotypic outcomes.http://link.springer.com/article/10.1186/s12915-019-0687-8Cattle genomeFunctional annotationChromatin statesButyrateRumen development |
| spellingShingle | Lingzhao Fang Shuli Liu Mei Liu Xiaolong Kang Shudai Lin Bingjie Li Erin E. Connor Ransom L. Baldwin Albert Tenesa Li Ma George E. Liu Cong-jun Li Functional annotation of the cattle genome through systematic discovery and characterization of chromatin states and butyrate-induced variations BMC Biology Cattle genome Functional annotation Chromatin states Butyrate Rumen development |
| title | Functional annotation of the cattle genome through systematic discovery and characterization of chromatin states and butyrate-induced variations |
| title_full | Functional annotation of the cattle genome through systematic discovery and characterization of chromatin states and butyrate-induced variations |
| title_fullStr | Functional annotation of the cattle genome through systematic discovery and characterization of chromatin states and butyrate-induced variations |
| title_full_unstemmed | Functional annotation of the cattle genome through systematic discovery and characterization of chromatin states and butyrate-induced variations |
| title_short | Functional annotation of the cattle genome through systematic discovery and characterization of chromatin states and butyrate-induced variations |
| title_sort | functional annotation of the cattle genome through systematic discovery and characterization of chromatin states and butyrate induced variations |
| topic | Cattle genome Functional annotation Chromatin states Butyrate Rumen development |
| url | http://link.springer.com/article/10.1186/s12915-019-0687-8 |
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