The structure, function and evolution of a complete human chromosome 8

The complete assembly of each human chromosome is essential for understanding human biology and evolution 1 , 2 . Here we use complementary long-read sequencing technologies to complete the linear assembly of human chromosome 8. Our assembly resolves the sequence of five previously long-standing gap...

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Veröffentlicht in:	Nature (London) Jg. 593; H. 7857; S. 101 - 107
Hauptverfasser:	Logsdon, Glennis A., Vollger, Mitchell R., Hsieh, PingHsun, Mao, Yafei, Liskovykh, Mikhail A., Koren, Sergey, Nurk, Sergey, Mercuri, Ludovica, Dishuck, Philip C., Rhie, Arang, de Lima, Leonardo G., Dvorkina, Tatiana, Porubsky, David, Harvey, William T., Mikheenko, Alla, Bzikadze, Andrey V., Kremitzki, Milinn, Graves-Lindsay, Tina A., Jain, Chirag, Hoekzema, Kendra, Murali, Shwetha C., Munson, Katherine M., Baker, Carl, Sorensen, Melanie, Lewis, Alexandra M., Surti, Urvashi, Gerton, Jennifer L., Larionov, Vladimir, Ventura, Mario, Miga, Karen H., Phillippy, Adam M., Eichler, Evan E.
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	London Nature Publishing Group UK 06.05.2021 Nature Publishing Group
Schlagworte:	13/106 14/19 14/32 14/63 38/1 45/15 45/22 45/23 45/29 45/90 631/181/2474 631/208/212 631/208/212/2304 631/337/103/90 Accuracy Animals Arrays Artificial chromosomes Assembly Cell Line Centromere - chemistry Centromere - genetics Centromere - metabolism Centromere protein A Chromosome 8 Chromosomes Chromosomes, Human, Pair 8 - chemistry Chromosomes, Human, Pair 8 - genetics Chromosomes, Human, Pair 8 - physiology Copy number Deoxyribonucleic acid Diploids DNA DNA Methylation DNA, Satellite - genetics Epigenesis, Genetic Evolution Evolution, Molecular Female Gene polymorphism Genes Genomes Genomics Haplotypes Health risks Humanities and Social Sciences Humans Macaca mulatta - genetics Male Minisatellite Repeats - genetics multidisciplinary Mutation Mutation rates Nucleosomes Nucleotide sequence Pan troglodytes - genetics Phylogeny Polymorphism Pongo abelii - genetics Satellite DNA Satellites Science Science (multidisciplinary) Structure-function relationships Telomere - chemistry Telomere - genetics Telomere - metabolism
ISSN:	0028-0836, 1476-4687, 1476-4687
Online-Zugang:	Volltext
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Abstract	The complete assembly of each human chromosome is essential for understanding human biology and evolution 1 , 2 . Here we use complementary long-read sequencing technologies to complete the linear assembly of human chromosome 8. Our assembly resolves the sequence of five previously long-standing gaps, including a 2.08-Mb centromeric α-satellite array, a 644-kb copy number polymorphism in the β-defensin gene cluster that is important for disease risk, and an 863-kb variable number tandem repeat at chromosome 8q21.2 that can function as a neocentromere. We show that the centromeric α-satellite array is generally methylated except for a 73-kb hypomethylated region of diverse higher-order α-satellites enriched with CENP-A nucleosomes, consistent with the location of the kinetochore. In addition, we confirm the overall organization and methylation pattern of the centromere in a diploid human genome. Using a dual long-read sequencing approach, we complete high-quality draft assemblies of the orthologous centromere from chromosome 8 in chimpanzee, orangutan and macaque to reconstruct its evolutionary history. Comparative and phylogenetic analyses show that the higher-order α-satellite structure evolved in the great ape ancestor with a layered symmetry, in which more ancient higher-order repeats locate peripherally to monomeric α-satellites. We estimate that the mutation rate of centromeric satellite DNA is accelerated by more than 2.2-fold compared to the unique portions of the genome, and this acceleration extends into the flanking sequence. The complete assembly of human chromosome 8 resolves previous gaps and reveals hidden complex forms of genetic variation, enabling functional and evolutionary characterization of primate centromeres.
AbstractList	The complete assembly of each human chromosome is essential for understanding human biology and evolution1,2. Here we use complementary long-read sequencing technologies to complete the linear assembly of human chromosome 8. Our assembly resolves the sequence of five previously long-standing gaps, including a 2.08-Mb centromeric α-satellite array, a 644-kb copy number polymorphism in the β-defensin gene cluster that is important for disease risk, and an 863-kb variable number tandem repeat at chromosome 8q21.2 that can function as a neocentromere. We show that the centromeric α-satellite array is generally methylated except for a 73-kb hypomethylated region of diverse higher-order α-satellites enriched with CENP-A nucleosomes, consistent with the location of the kinetochore. In addition, we confirm the overall organization and methylation pattern of the centromere in a diploid human genome. Using a dual long-read sequencing approach, we complete high-quality draft assemblies of the orthologous centromere from chromosome 8 in chimpanzee, orangutan and macaque to reconstruct its evolutionary history. Comparative and phylogenetic analyses show that the higher-order α-satellite structure evolved in the great ape ancestor with a layered symmetry, in which more ancient higher-order repeats locate peripherally to monomeric α-satellites. We estimate that the mutation rate of centromeric satellite DNA is accelerated by more than 2.2-fold compared to the unique portions of the genome, and this acceleration extends into the flanking sequence.The complete assembly of each human chromosome is essential for understanding human biology and evolution1,2. Here we use complementary long-read sequencing technologies to complete the linear assembly of human chromosome 8. Our assembly resolves the sequence of five previously long-standing gaps, including a 2.08-Mb centromeric α-satellite array, a 644-kb copy number polymorphism in the β-defensin gene cluster that is important for disease risk, and an 863-kb variable number tandem repeat at chromosome 8q21.2 that can function as a neocentromere. We show that the centromeric α-satellite array is generally methylated except for a 73-kb hypomethylated region of diverse higher-order α-satellites enriched with CENP-A nucleosomes, consistent with the location of the kinetochore. In addition, we confirm the overall organization and methylation pattern of the centromere in a diploid human genome. Using a dual long-read sequencing approach, we complete high-quality draft assemblies of the orthologous centromere from chromosome 8 in chimpanzee, orangutan and macaque to reconstruct its evolutionary history. Comparative and phylogenetic analyses show that the higher-order α-satellite structure evolved in the great ape ancestor with a layered symmetry, in which more ancient higher-order repeats locate peripherally to monomeric α-satellites. We estimate that the mutation rate of centromeric satellite DNA is accelerated by more than 2.2-fold compared to the unique portions of the genome, and this acceleration extends into the flanking sequence. The complete assembly of each human chromosome is essential for understanding human biology and evolution1,2. Here we use complementary long-read sequencing technologies to complete the linear assembly of human chromosome 8. Our assembly resolves the sequence of five previously long-standing gaps, including a 2.08-Mb centromeric α-satellite array, a 644-kb copy number polymorphism in the ß-defensin gene cluster that is important for disease risk, and an 863-kb variable number tandem repeat at chromosome 8q21.2 that can function as a neocentromere. We show that the centromeric α-satellite array is generally methylated except for a 73-kb hypomethylated region of diverse higher-order α-satellites enriched with CENP-A nucleosomes, consistent with the location of the kinetochore. In addition, we confirm the overall organization and methylation pattern of the centromere in a diploid human genome. Using a dual long-read sequencing approach, we complete high-quality draft assemblies ofthe orthologous centromere from chromosome 8 in chimpanzee, orangutan and macaque to reconstruct its evolutionary history. Comparative and phylogenetic analyses show that the higher-order α-satellite structure evolved in the great ape ancestor with a layered symmetry, in which more ancient higher-order repeats locate peripherally to monomeric α-satellites. We estimate that the mutation rate of centromeric satellite DNA is accelerated by more than 2.2-fold compared to the unique portions of the genome, and this acceleration extends into the flanking sequence. The complete assembly of each human chromosome is essential for understanding human biology and evolution 1,2 . Here we use complementary long-read sequencing technologies to complete the linear assembly of human chromosome 8. Our assembly resolves the sequence of five previously long-standing gaps, including a 2.08-Mb centromeric α-satellite array, a 644-kb copy number polymorphism in the β-defensin gene cluster that is important for disease risk, and an 863-kb variable number tandem repeat at chromosome 8q21.2 that can function as a neocentromere. We show that the centromeric α-satellite array is generally methylated except for a 73-kb hypomethylated region of diverse higher-order α-satellites enriched with CENP-A nucleosomes, consistent with the location of the kinetochore. In addition, we confirm the overall organization and methylation pattern of the centromere in a diploid human genome. Using a dual long-read sequencing approach, we complete high-quality draft assemblies of the orthologous centromere from chromosome 8 in chimpanzee, orangutan and macaque to reconstruct its evolutionary history. Comparative and phylogenetic analyses show that the higher-order α-satellite structure evolved in the great ape ancestor with a layered symmetry, in which more ancient higher-order repeats locate peripherally to monomeric α-satellites. We estimate that the mutation rate of centromeric satellite DNA is accelerated by more than 2.2-fold compared to the unique portions of the genome, and this acceleration extends into the flanking sequence. The complete assembly of each human chromosome is essential for understanding human biology and evolution 1 , 2 . Here we use complementary long-read sequencing technologies to complete the linear assembly of human chromosome 8. Our assembly resolves the sequence of five previously long-standing gaps, including a 2.08-Mb centromeric α-satellite array, a 644-kb copy number polymorphism in the β-defensin gene cluster that is important for disease risk, and an 863-kb variable number tandem repeat at chromosome 8q21.2 that can function as a neocentromere. We show that the centromeric α-satellite array is generally methylated except for a 73-kb hypomethylated region of diverse higher-order α-satellites enriched with CENP-A nucleosomes, consistent with the location of the kinetochore. In addition, we confirm the overall organization and methylation pattern of the centromere in a diploid human genome. Using a dual long-read sequencing approach, we complete high-quality draft assemblies of the orthologous centromere from chromosome 8 in chimpanzee, orangutan and macaque to reconstruct its evolutionary history. Comparative and phylogenetic analyses show that the higher-order α-satellite structure evolved in the great ape ancestor with a layered symmetry, in which more ancient higher-order repeats locate peripherally to monomeric α-satellites. We estimate that the mutation rate of centromeric satellite DNA is accelerated by more than 2.2-fold compared to the unique portions of the genome, and this acceleration extends into the flanking sequence. The complete assembly of human chromosome 8 resolves previous gaps and reveals hidden complex forms of genetic variation, enabling functional and evolutionary characterization of primate centromeres. The complete assembly of each human chromosome is essential for understanding human biology and evolution1,2. Here we use complementary long-read sequencing technologies to complete the linear assembly of human chromosome 8. Our assembly resolves the sequence of five previously long-standing gaps, including a 2.08-Mb centromeric α-satellite array, a 644-kb copy number polymorphism in the β-defensin gene cluster that is important for disease risk, and an 863-kb variable number tandem repeat at chromosome 8q21.2 that can function as a neocentromere. We show that the centromeric α-satellite array is generally methylated except for a 73-kb hypomethylated region of diverse higher-order α-satellites enriched with CENP-A nucleosomes, consistent with the location of the kinetochore. In addition, we confirm the overall organization and methylation pattern of the centromere in a diploid human genome. Using a dual long-read sequencing approach, we complete high-quality draft assemblies of the orthologous centromere from chromosome 8 in chimpanzee, orangutan and macaque to reconstruct its evolutionary history. Comparative and phylogenetic analyses show that the higher-order α-satellite structure evolved in the great ape ancestor with a layered symmetry, in which more ancient higher-order repeats locate peripherally to monomeric α-satellites. We estimate that the mutation rate of centromeric satellite DNA is accelerated by more than 2.2-fold compared to the unique portions of the genome, and this acceleration extends into the flanking sequence. The complete assembly of human chromosome 8 resolves previous gaps and reveals hidden complex forms of genetic variation, enabling functional and evolutionary characterization of primate centromeres. The complete assembly of each human chromosome is essential for understanding human biology and evolution . Here we use complementary long-read sequencing technologies to complete the linear assembly of human chromosome 8. Our assembly resolves the sequence of five previously long-standing gaps, including a 2.08-Mb centromeric α-satellite array, a 644-kb copy number polymorphism in the β-defensin gene cluster that is important for disease risk, and an 863-kb variable number tandem repeat at chromosome 8q21.2 that can function as a neocentromere. We show that the centromeric α-satellite array is generally methylated except for a 73-kb hypomethylated region of diverse higher-order α-satellites enriched with CENP-A nucleosomes, consistent with the location of the kinetochore. In addition, we confirm the overall organization and methylation pattern of the centromere in a diploid human genome. Using a dual long-read sequencing approach, we complete high-quality draft assemblies of the orthologous centromere from chromosome 8 in chimpanzee, orangutan and macaque to reconstruct its evolutionary history. Comparative and phylogenetic analyses show that the higher-order α-satellite structure evolved in the great ape ancestor with a layered symmetry, in which more ancient higher-order repeats locate peripherally to monomeric α-satellites. We estimate that the mutation rate of centromeric satellite DNA is accelerated by more than 2.2-fold compared to the unique portions of the genome, and this acceleration extends into the flanking sequence.
Author	Sorensen, Melanie Mikheenko, Alla Jain, Chirag Miga, Karen H. Lewis, Alexandra M. Vollger, Mitchell R. Harvey, William T. Hsieh, PingHsun Koren, Sergey Hoekzema, Kendra Munson, Katherine M. Surti, Urvashi Phillippy, Adam M. de Lima, Leonardo G. Eichler, Evan E. Bzikadze, Andrey V. Porubsky, David Liskovykh, Mikhail A. Graves-Lindsay, Tina A. Dvorkina, Tatiana Rhie, Arang Murali, Shwetha C. Logsdon, Glennis A. Nurk, Sergey Mao, Yafei Kremitzki, Milinn Baker, Carl Ventura, Mario Mercuri, Ludovica Gerton, Jennifer L. Dishuck, Philip C. Larionov, Vladimir
Author_xml	– sequence: 1 givenname: Glennis A. orcidid: 0000-0003-2396-0656 surname: Logsdon fullname: Logsdon, Glennis A. organization: Department of Genome Sciences, University of Washington School of Medicine – sequence: 2 givenname: Mitchell R. orcidid: 0000-0002-8651-1615 surname: Vollger fullname: Vollger, Mitchell R. organization: Department of Genome Sciences, University of Washington School of Medicine – sequence: 3 givenname: PingHsun surname: Hsieh fullname: Hsieh, PingHsun organization: Department of Genome Sciences, University of Washington School of Medicine – sequence: 4 givenname: Yafei orcidid: 0000-0002-9648-4278 surname: Mao fullname: Mao, Yafei organization: Department of Genome Sciences, University of Washington School of Medicine – sequence: 5 givenname: Mikhail A. surname: Liskovykh fullname: Liskovykh, Mikhail A. organization: Developmental Therapeutics Branch, National Cancer Institute – sequence: 6 givenname: Sergey orcidid: 0000-0002-1472-8962 surname: Koren fullname: Koren, Sergey organization: Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health – sequence: 7 givenname: Sergey surname: Nurk fullname: Nurk, Sergey organization: Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health – sequence: 8 givenname: Ludovica orcidid: 0000-0002-3688-4501 surname: Mercuri fullname: Mercuri, Ludovica organization: Department of Biology, University of Bari, Aldo Moro – sequence: 9 givenname: Philip C. orcidid: 0000-0003-2223-9787 surname: Dishuck fullname: Dishuck, Philip C. organization: Department of Genome Sciences, University of Washington School of Medicine – sequence: 10 givenname: Arang orcidid: 0000-0002-9809-8127 surname: Rhie fullname: Rhie, Arang organization: Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health – sequence: 11 givenname: Leonardo G. orcidid: 0000-0001-6340-6065 surname: de Lima fullname: de Lima, Leonardo G. organization: Stowers Institute for Medical Research – sequence: 12 givenname: Tatiana surname: Dvorkina fullname: Dvorkina, Tatiana organization: Center for Algorithmic Biotechnology, Institute of Translational Biomedicine, Saint Petersburg State University – sequence: 13 givenname: David orcidid: 0000-0001-8414-8966 surname: Porubsky fullname: Porubsky, David organization: Department of Genome Sciences, University of Washington School of Medicine – sequence: 14 givenname: William T. surname: Harvey fullname: Harvey, William T. organization: Department of Genome Sciences, University of Washington School of Medicine – sequence: 15 givenname: Alla surname: Mikheenko fullname: Mikheenko, Alla organization: Center for Algorithmic Biotechnology, Institute of Translational Biomedicine, Saint Petersburg State University – sequence: 16 givenname: Andrey V. surname: Bzikadze fullname: Bzikadze, Andrey V. organization: Graduate Program in Bioinformatics and Systems Biology, University of California, San Diego – sequence: 17 givenname: Milinn surname: Kremitzki fullname: Kremitzki, Milinn organization: McDonnell Genome Institute, Department of Genetics, Washington University School of Medicine – sequence: 18 givenname: Tina A. surname: Graves-Lindsay fullname: Graves-Lindsay, Tina A. organization: McDonnell Genome Institute, Department of Genetics, Washington University School of Medicine – sequence: 19 givenname: Chirag surname: Jain fullname: Jain, Chirag organization: Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health – sequence: 20 givenname: Kendra surname: Hoekzema fullname: Hoekzema, Kendra organization: Department of Genome Sciences, University of Washington School of Medicine – sequence: 21 givenname: Shwetha C. surname: Murali fullname: Murali, Shwetha C. organization: Department of Genome Sciences, University of Washington School of Medicine, Howard Hughes Medical Institute, University of Washington – sequence: 22 givenname: Katherine M. orcidid: 0000-0001-8413-6498 surname: Munson fullname: Munson, Katherine M. organization: Department of Genome Sciences, University of Washington School of Medicine – sequence: 23 givenname: Carl surname: Baker fullname: Baker, Carl organization: Department of Genome Sciences, University of Washington School of Medicine – sequence: 24 givenname: Melanie surname: Sorensen fullname: Sorensen, Melanie organization: Department of Genome Sciences, University of Washington School of Medicine – sequence: 25 givenname: Alexandra M. surname: Lewis fullname: Lewis, Alexandra M. organization: Department of Genome Sciences, University of Washington School of Medicine – sequence: 26 givenname: Urvashi surname: Surti fullname: Surti, Urvashi organization: Department of Pathology, University of Pittsburgh – sequence: 27 givenname: Jennifer L. orcidid: 0000-0003-0743-3637 surname: Gerton fullname: Gerton, Jennifer L. organization: Stowers Institute for Medical Research – sequence: 28 givenname: Vladimir surname: Larionov fullname: Larionov, Vladimir organization: Developmental Therapeutics Branch, National Cancer Institute – sequence: 29 givenname: Mario orcidid: 0000-0001-7762-8777 surname: Ventura fullname: Ventura, Mario organization: Department of Biology, University of Bari, Aldo Moro – sequence: 30 givenname: Karen H. orcidid: 0000-0002-3670-4507 surname: Miga fullname: Miga, Karen H. organization: Center for Biomolecular Science and Engineering, University of California, Santa Cruz – sequence: 31 givenname: Adam M. orcidid: 0000-0003-2983-8934 surname: Phillippy fullname: Phillippy, Adam M. organization: Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health – sequence: 32 givenname: Evan E. orcidid: 0000-0002-8246-4014 surname: Eichler fullname: Eichler, Evan E. email: eee@gs.washington.edu organization: Department of Genome Sciences, University of Washington School of Medicine, Howard Hughes Medical Institute, University of Washington
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/33828295$$D View this record in MEDLINE/PubMed
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Snippet	The complete assembly of each human chromosome is essential for understanding human biology and evolution 1 , 2 . Here we use complementary long-read... The complete assembly of each human chromosome is essential for understanding human biology and evolution 1,2 . Here we use complementary long-read sequencing... The complete assembly of each human chromosome is essential for understanding human biology and evolution . Here we use complementary long-read sequencing... The complete assembly of each human chromosome is essential for understanding human biology and evolution1,2. Here we use complementary long-read sequencing...
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SubjectTerms	13/106 14/19 14/32 14/63 38/1 45/15 45/22 45/23 45/29 45/90 631/181/2474 631/208/212 631/208/212/2304 631/337/103/90 Accuracy Animals Arrays Artificial chromosomes Assembly Cell Line Centromere - chemistry Centromere - genetics Centromere - metabolism Centromere protein A Chromosome 8 Chromosomes Chromosomes, Human, Pair 8 - chemistry Chromosomes, Human, Pair 8 - genetics Chromosomes, Human, Pair 8 - physiology Copy number Deoxyribonucleic acid Diploids DNA DNA Methylation DNA, Satellite - genetics Epigenesis, Genetic Evolution Evolution, Molecular Female Gene polymorphism Genes Genomes Genomics Haplotypes Health risks Humanities and Social Sciences Humans Macaca mulatta - genetics Male Minisatellite Repeats - genetics multidisciplinary Mutation Mutation rates Nucleosomes Nucleotide sequence Pan troglodytes - genetics Phylogeny Polymorphism Pongo abelii - genetics Satellite DNA Satellites Science Science (multidisciplinary) Structure-function relationships Telomere - chemistry Telomere - genetics Telomere - metabolism
Title	The structure, function and evolution of a complete human chromosome 8
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