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PMID: 33789087 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Expectations and blind spots for structural variation detection from long-read assemblies and short-read genome sequencing technologies.

American journal of human genetics ·Vol. 108 ·No. 5 ·2021-00-06 ·Pages 919-928

Zhao X, Collins RL, Lee WP, Weber AM, Jun Y, Zhu Q, Weisburd B, Huang Y, Audano PA, Wang H, Walker M, Lowther C, Fu J, Human Genome Structural Variation Consortium, Gerstein MB, Devine SE, Marschall T, Korbel JO, Eichler EE, Chaisson MJP, Lee C, Mills RE, Brand H, Talkowski ME

Abstract

Virtually all genome sequencing efforts in national biobanks, complex and Mendelian disease programs, and medical genetic initiatives are reliant upon short-read whole-genome sequencing (srWGS), which presents challenges for the detection of structural variants (SVs) relative to emerging long-read WGS (lrWGS) technologies. Given this ubiquity of srWGS in large-scale genomics initiatives, we sought to establish expectations for routine SV detection from this data type by comparison with lrWGS assembly, as well as to quantify the genomic properties and added value of SVs uniquely accessible to each technology. Analyses from the Human Genome Structural Variation Consortium (HGSVC) of three families captured ~11,000 SVs per genome from srWGS and ~25,000 SVs per genome from lrWGS assembly. Detection power and precision for SV discovery varied dramatically by genomic context and variant class: 9.7% of the current GRCh38 reference is defined by segmental duplication (SD) and simple repeat (SR), yet 91.4% of deletions that were specifically discovered by lrWGS localized to these regions. Across the remaining 90.3% of reference sequence, we observed extremely high (93.8%) concordance between technologies for deletions in these datasets. In contrast, lrWGS was superior for detection of insertions across all genomic contexts. Given that non-SD/SR sequences encompass 95.9% of currently annotated disease-associated exons, improved sensitivity from lrWGS to discover novel pathogenic deletions in these currently interpretable genomic regions is likely to be incremental. However, these analyses highlight the considerable added value of assembly-based lrWGS to create new catalogs of insertions and transposable elements, as well as disease-associated repeat expansions in genomic sequences that were previously recalcitrant to routine assessment.

Keywords
copy number variation genome assembly long-read technology segmental duplication simple repeats structural variation whole-genome sequencing
MeSH Terms
DNA Copy Number Variations Exons/genetics Genome, Human/genetics Genomic Structural Variation Genomics/methods Goals Humans Research Design Segmental Duplications, Genomic Sequence Alignment Whole Genome Sequencing/methods,standards
Authors & Affiliations
24 authors, click to expand affiliations / ORCID
Zhao Xuefang
Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA 02114, USA; Program in Medical and Population Genetics and Stanley Center for Psychiatric Disorders, Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA.
Collins Ryan L
Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA 02114, USA; Program in Medical and Population Genetics and Stanley Center for Psychiatric Disorders, Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Division of Medical Sciences, Harvard Medical School, Boston, MA 02115, USA.
Lee Wan-Ping
The Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA.
Weber Alexandra M
Department of Computational Medicine and Bioinformatics, University of Michigan Medical School, 100 Washtenaw Avenue, Ann Arbor, MI 48109, USA; Department of Human Genetics, University of Michigan Medical School, 1241 East Catherine Street, Ann Arbor, MI 48109, USA.
Jun Yukyung
The Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA.
Zhu Qihui
The Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA.
Weisburd Ben
Program in Medical and Population Genetics and Stanley Center for Psychiatric Disorders, Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, MA 02142, USA.
Huang Yongqing
Data Sciences Platform, Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, MA 02142, USA.
Audano Peter A
Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA 98195, USA.
Wang Harold
Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA 02114, USA; Program in Medical and Population Genetics and Stanley Center for Psychiatric Disorders, Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, MA 02142, USA.
Walker Mark
Program in Medical and Population Genetics and Stanley Center for Psychiatric Disorders, Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA.
Lowther Chelsea
Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA 02114, USA; Program in Medical and Population Genetics and Stanley Center for Psychiatric Disorders, Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA.
Fu Jack
Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA 02114, USA; Program in Medical and Population Genetics and Stanley Center for Psychiatric Disorders, Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA.
Human Genome Structural Variation Consortium
Gerstein Mark B
Yale University Medical School, Computational Biology and Bioinformatics Program, New Haven, CT 06520, USA.
Devine Scott E
Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD 21201, USA.
Marschall Tobias
Institute for Medical Biometry and Bioinformatics, Medical Faculty, Heinrich Heine University, 40225 Düsseldorf, Germany.
Korbel Jan O
European Molecular Biology Laboratory, Genome Biology Unit, 69117 Heidelberg, Germany; European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
Eichler Evan E
Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA 98195, USA; Howard Hughes Medical Institute, University of Washington, Seattle, WA 98195, USA.
Chaisson Mark J P
Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA 98195, USA; Department of Quantitative and Computational Biology, University of Southern California, Los Angeles, CA 90089, USA.
Lee Charles
The Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA; Department of Graduate Studies - Life Sciences, Ewha Womans University, 52, Ewhayeodae-gil, Seodaemun-gu, Seoul 03760, South Korea; Precision Medicine Center, The First Affiliated Hospital of Xi'an Jiaotong University, 277 West Yanta Road, Xi'an 710061, Shaanxi, People's Republic of China.
Mills Ryan E
Department of Computational Medicine and Bioinformatics, University of Michigan Medical School, 100 Washtenaw Avenue, Ann Arbor, MI 48109, USA; Department of Human Genetics, University of Michigan Medical School, 1241 East Catherine Street, Ann Arbor, MI 48109, USA.
Brand Harrison
Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA 02114, USA; Program in Medical and Population Genetics and Stanley Center for Psychiatric Disorders, Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA.
Talkowski Michael E
Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA 02114, USA; Program in Medical and Population Genetics and Stanley Center for Psychiatric Disorders, Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA; Division of Medical Sciences, Harvard Medical School, Boston, MA 02115, USA. Electronic address: [email protected].
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Article Info
Journal
American journal of human genetics
Abbr.
Am J Hum Genet
ISSN
1537-6605
Published
2021-00-06
Epub
2021-00-30
Pages
919-928
Language
English
Region
United States
NLM ID
0370475
PMCID
PMC8206509
Subset
IM
Grants
NHGRI NIH HHS · R01 HG002898 · United States
NIMH NIH HHS · R01 MH115957 · United States
NICHD NIH HHS · R03 HD099547 · United States
NHGRI NIH HHS · UM1 HG008895 · United States
NHGRI NIH HHS · F31 HG010569 · United States
NIDCR NIH HHS · R00 DE026824 · United States
NICHD NIH HHS · R01 HD091797 · United States
NHGRI NIH HHS · T32 HG002295 · United States
NHGRI NIH HHS · R01 HG010169 · United States
NICHD NIH HHS · R01 HD081256 · United States
NHGRI NIH HHS · U24 HG007497 · United States
NICHD NIH HHS · R01 HD096326 · United States
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