Structurally divergent and recurrently mutated regions of primate genomes

Yafei Mao; William T. Harvey; David Porubsky; Katherine M. Munson; Kendra Hoekzema; Alexandra P. Lewis; Peter A. Audano; Allison Rozanski; Xiangyu Yang; Shilong Zhang; Dong Ahn Yoo; David S. Gordon; Tyler Fair; Xiaoxi Wei; Glennis A. Logsdon; Marina Haukness; Philip C. Dishuck; Hyeonsoo Jeong; Ricardo del Rosario; Vanessa L. Bauer; Will T. Fattor; Gregory K. Wilkerson; Yuxiang Mao; Yongyong Shi; Qiang Sun; Qing Lu; Benedict Paten; Trygve E. Bakken; Alex A. Pollen; Guoping Feng; Sara L. Sawyer; Wesley C. Warren; Lucia Carbone; Evan E. Eichler

doi:10.1016/j.cell.2024.01.052

Structurally divergent and recurrently mutated regions of primate genomes

Yafei Mao, William T. Harvey, David Porubsky, Katherine M. Munson, Kendra Hoekzema, Alexandra P. Lewis, Peter A. Audano, Allison Rozanski, Xiangyu Yang, Shilong Zhang, Dong Ahn Yoo, David S. Gordon, Tyler Fair, Xiaoxi Wei, Glennis A. Logsdon, Marina Haukness, Philip C. Dishuck, Hyeonsoo Jeong, Ricardo del Rosario, Vanessa L. BauerWill T. Fattor, Gregory K. Wilkerson, Yuxiang Mao, Yongyong Shi, Qiang Sun, Qing Lu, Benedict Paten, Trygve E. Bakken, Alex A. Pollen, Guoping Feng, Sara L. Sawyer, Wesley C. Warren, Lucia Carbone, Evan E. Eichler

Research output: Contribution to journal › Article › peer-review

1 Scopus citations

Abstract

We sequenced and assembled using multiple long-read sequencing technologies the genomes of chimpanzee, bonobo, gorilla, orangutan, gibbon, macaque, owl monkey, and marmoset. We identified 1,338,997 lineage-specific fixed structural variants (SVs) disrupting 1,561 protein-coding genes and 136,932 regulatory elements, including the most complete set of human-specific fixed differences. We estimate that 819.47 Mbp or ∼27% of the genome has been affected by SVs across primate evolution. We identify 1,607 structurally divergent regions wherein recurrent structural variation contributes to creating SV hotspots where genes are recurrently lost (e.g., CARD, C4, and OLAH gene families) and additional lineage-specific genes are generated (e.g., CKAP2, VPS36, ACBD7, and NEK5 paralogs), becoming targets of rapid chromosomal diversification and positive selection (e.g., RGPD gene family). High-fidelity long-read sequencing has made these dynamic regions of the genome accessible for sequence-level analyses within and between primate species.

Original language	English (US)
Pages (from-to)	1547-1562.e13
Journal	Cell
Volume	187
Issue number	6
DOIs	https://doi.org/10.1016/j.cell.2024.01.052
State	Published - Mar 14 2024

Keywords

adaptive evolution
comparative genomics
duplicated genes
evolutionary medicine
human diseases
long-read sequencing
NPHP1 and Joubert syndrome
primate evolution
RGPD gene family

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.cell.2024.01.052

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Mao, Y., Harvey, W. T., Porubsky, D., Munson, K. M., Hoekzema, K., Lewis, A. P., Audano, P. A., Rozanski, A., Yang, X., Zhang, S., Yoo, D. A., Gordon, D. S., Fair, T., Wei, X., Logsdon, G. A., Haukness, M., Dishuck, P. C., Jeong, H., del Rosario, R., ... Eichler, E. E. (2024). Structurally divergent and recurrently mutated regions of primate genomes. Cell, 187(6), 1547-1562.e13. https://doi.org/10.1016/j.cell.2024.01.052

Mao, Y, Harvey, WT, Porubsky, D, Munson, KM, Hoekzema, K, Lewis, AP, Audano, PA, Rozanski, A, Yang, X, Zhang, S, Yoo, DA, Gordon, DS, Fair, T, Wei, X, Logsdon, GA, Haukness, M, Dishuck, PC, Jeong, H, del Rosario, R, Bauer, VL, Fattor, WT, Wilkerson, GK, Mao, Y, Shi, Y, Sun, Q, Lu, Q, Paten, B, Bakken, TE, Pollen, AA, Feng, G, Sawyer, SL, Warren, WC, Carbone, L & Eichler, EE 2024, 'Structurally divergent and recurrently mutated regions of primate genomes', Cell, vol. 187, no. 6, pp. 1547-1562.e13. https://doi.org/10.1016/j.cell.2024.01.052

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title = "Structurally divergent and recurrently mutated regions of primate genomes",

abstract = "We sequenced and assembled using multiple long-read sequencing technologies the genomes of chimpanzee, bonobo, gorilla, orangutan, gibbon, macaque, owl monkey, and marmoset. We identified 1,338,997 lineage-specific fixed structural variants (SVs) disrupting 1,561 protein-coding genes and 136,932 regulatory elements, including the most complete set of human-specific fixed differences. We estimate that 819.47 Mbp or ∼27% of the genome has been affected by SVs across primate evolution. We identify 1,607 structurally divergent regions wherein recurrent structural variation contributes to creating SV hotspots where genes are recurrently lost (e.g., CARD, C4, and OLAH gene families) and additional lineage-specific genes are generated (e.g., CKAP2, VPS36, ACBD7, and NEK5 paralogs), becoming targets of rapid chromosomal diversification and positive selection (e.g., RGPD gene family). High-fidelity long-read sequencing has made these dynamic regions of the genome accessible for sequence-level analyses within and between primate species.",

keywords = "adaptive evolution, comparative genomics, duplicated genes, evolutionary medicine, human diseases, long-read sequencing, NPHP1 and Joubert syndrome, primate evolution, RGPD gene family",

author = "Yafei Mao and Harvey, {William T.} and David Porubsky and Munson, {Katherine M.} and Kendra Hoekzema and Lewis, {Alexandra P.} and Audano, {Peter A.} and Allison Rozanski and Xiangyu Yang and Shilong Zhang and Yoo, {Dong Ahn} and Gordon, {David S.} and Tyler Fair and Xiaoxi Wei and Logsdon, {Glennis A.} and Marina Haukness and Dishuck, {Philip C.} and Hyeonsoo Jeong and {del Rosario}, Ricardo and Bauer, {Vanessa L.} and Fattor, {Will T.} and Wilkerson, {Gregory K.} and Yuxiang Mao and Yongyong Shi and Qiang Sun and Qing Lu and Benedict Paten and Bakken, {Trygve E.} and Pollen, {Alex A.} and Guoping Feng and Sawyer, {Sara L.} and Warren, {Wesley C.} and Lucia Carbone and Eichler, {Evan E.}",

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doi = "10.1016/j.cell.2024.01.052",

language = "English (US)",

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T1 - Structurally divergent and recurrently mutated regions of primate genomes

AU - Mao, Yafei

AU - Harvey, William T.

AU - Porubsky, David

AU - Munson, Katherine M.

AU - Hoekzema, Kendra

AU - Lewis, Alexandra P.

AU - Audano, Peter A.

AU - Rozanski, Allison

AU - Yang, Xiangyu

AU - Zhang, Shilong

AU - Yoo, Dong Ahn

AU - Gordon, David S.

AU - Fair, Tyler

AU - Wei, Xiaoxi

AU - Logsdon, Glennis A.

AU - Haukness, Marina

AU - Dishuck, Philip C.

AU - Jeong, Hyeonsoo

AU - del Rosario, Ricardo

AU - Bauer, Vanessa L.

AU - Fattor, Will T.

AU - Wilkerson, Gregory K.

AU - Mao, Yuxiang

AU - Shi, Yongyong

AU - Sun, Qiang

AU - Lu, Qing

AU - Paten, Benedict

AU - Bakken, Trygve E.

AU - Pollen, Alex A.

AU - Feng, Guoping

AU - Sawyer, Sara L.

AU - Warren, Wesley C.

AU - Carbone, Lucia

AU - Eichler, Evan E.

PY - 2024/3/14

Y1 - 2024/3/14

N2 - We sequenced and assembled using multiple long-read sequencing technologies the genomes of chimpanzee, bonobo, gorilla, orangutan, gibbon, macaque, owl monkey, and marmoset. We identified 1,338,997 lineage-specific fixed structural variants (SVs) disrupting 1,561 protein-coding genes and 136,932 regulatory elements, including the most complete set of human-specific fixed differences. We estimate that 819.47 Mbp or ∼27% of the genome has been affected by SVs across primate evolution. We identify 1,607 structurally divergent regions wherein recurrent structural variation contributes to creating SV hotspots where genes are recurrently lost (e.g., CARD, C4, and OLAH gene families) and additional lineage-specific genes are generated (e.g., CKAP2, VPS36, ACBD7, and NEK5 paralogs), becoming targets of rapid chromosomal diversification and positive selection (e.g., RGPD gene family). High-fidelity long-read sequencing has made these dynamic regions of the genome accessible for sequence-level analyses within and between primate species.

AB - We sequenced and assembled using multiple long-read sequencing technologies the genomes of chimpanzee, bonobo, gorilla, orangutan, gibbon, macaque, owl monkey, and marmoset. We identified 1,338,997 lineage-specific fixed structural variants (SVs) disrupting 1,561 protein-coding genes and 136,932 regulatory elements, including the most complete set of human-specific fixed differences. We estimate that 819.47 Mbp or ∼27% of the genome has been affected by SVs across primate evolution. We identify 1,607 structurally divergent regions wherein recurrent structural variation contributes to creating SV hotspots where genes are recurrently lost (e.g., CARD, C4, and OLAH gene families) and additional lineage-specific genes are generated (e.g., CKAP2, VPS36, ACBD7, and NEK5 paralogs), becoming targets of rapid chromosomal diversification and positive selection (e.g., RGPD gene family). High-fidelity long-read sequencing has made these dynamic regions of the genome accessible for sequence-level analyses within and between primate species.

KW - adaptive evolution

KW - comparative genomics

KW - duplicated genes

KW - evolutionary medicine

KW - human diseases

KW - long-read sequencing

KW - NPHP1 and Joubert syndrome

KW - primate evolution

KW - RGPD gene family

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U2 - 10.1016/j.cell.2024.01.052

DO - 10.1016/j.cell.2024.01.052

M3 - Article

C2 - 38428424

AN - SCOPUS:85187211353

SN - 0092-8674

VL - 187

SP - 1547-1562.e13

JO - Cell

JF - Cell

IS - 6

ER -

Structurally divergent and recurrently mutated regions of primate genomes

Abstract

Keywords

ASJC Scopus subject areas

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