The sea lamprey germline genome provides insights into programmed genome rearrangement and vertebrate evolution

Jeramiah J. Smith; Nataliya Timoshevskaya; Chengxi Ye; Carson Holt; Melissa C. Keinath; Hugo J. Parker; Malcolm E. Cook; Jon E. Hess; Shawn R. Narum; Francesco Lamanna; Henrik Kaessmann; Vladimir A. Timoshevskiy; Courtney K.M. Waterbury; Cody Saraceno; Leanne M. Wiedemann; Sofia M.C. Robb; Carl Baker; Evan E. Eichler; Dorit Hockman; Tatjana Sauka-Spengler; Mark Yandell; Robb Krumlauf; Greg Elgar; Chris T. Amemiya

doi:10.1038/s41588-017-0036-1

The sea lamprey germline genome provides insights into programmed genome rearrangement and vertebrate evolution

Jeramiah J. Smith, Nataliya Timoshevskaya, Chengxi Ye, Carson Holt, Melissa C. Keinath, Hugo J. Parker, Malcolm E. Cook, Jon E. Hess, Shawn R. Narum, Francesco Lamanna, Henrik Kaessmann, Vladimir A. Timoshevskiy, Courtney K.M. Waterbury, Cody Saraceno, Leanne M. Wiedemann, Sofia M.C. Robb, Carl Baker, Evan E. Eichler, Dorit Hockman, Tatjana Sauka-SpenglerMark Yandell, Robb Krumlauf, Greg Elgar, Chris T. Amemiya

Biology

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

186 Scopus citations

Abstract

The sea lamprey (Petromyzon marinus) serves as a comparative model for reconstructing vertebrate evolution. To enable more informed analyses, we developed a new assembly of the lamprey germline genome that integrates several complementary data sets. Analysis of this highly contiguous (chromosome-scale) assembly shows that both chromosomal and whole-genome duplications have played significant roles in the evolution of ancestral vertebrate and lamprey genomes, including chromosomes that carry the six lamprey HOX clusters. The assembly also contains several hundred genes that are reproducibly eliminated from somatic cells during early development in lamprey. Comparative analyses show that gnathostome (mouse) homologs of these genes are frequently marked by polycomb repressive complexes (PRCs) in embryonic stem cells, suggesting overlaps in the regulatory logic of somatic DNA elimination and bivalent states that are regulated by early embryonic PRCs. This new assembly will enhance diverse studies that are informed by lampreys' unique biology and evolutionary/comparative perspective.

Original language	English
Pages (from-to)	270-277
Number of pages	8
Journal	Nature Genetics
Volume	50
Issue number	2
DOIs	https://doi.org/10.1038/s41588-017-0036-1
State	Published - Feb 1 2018

Bibliographical note

Funding Information:
Research reported in this publication was supported by the National Institute of General Medical Sciences of the US National Institutes of Health under award number R01GM104123 to J.J.S., the Stowers Institute under award number SIMR-1001 to H.J.P., M.E.C., L.M.W., S.M.C.R. and R.K., and the Bonneville Power Administration to J.E.H. and S.R.N. E.E.E. is an investigator of the Howard Hughes Medical Institute. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Support and resources from the Center for High Performance Computing at the University of Utah are gratefully acknowledged. Additional computational support was provided by The University of Kentucky High Performance Computing complex.

Publisher Copyright:
© 2018 The Author(s).

ASJC Scopus subject areas

Genetics

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10.1038/s41588-017-0036-1

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Smith, J. J., Timoshevskaya, N., Ye, C., Holt, C., Keinath, M. C., Parker, H. J., Cook, M. E., Hess, J. E., Narum, S. R., Lamanna, F., Kaessmann, H., Timoshevskiy, V. A., Waterbury, C. K. M., Saraceno, C., Wiedemann, L. M., Robb, S. M. C., Baker, C., Eichler, E. E., Hockman, D., ... Amemiya, C. T. (2018). The sea lamprey germline genome provides insights into programmed genome rearrangement and vertebrate evolution. Nature Genetics, 50(2), 270-277. https://doi.org/10.1038/s41588-017-0036-1

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title = "The sea lamprey germline genome provides insights into programmed genome rearrangement and vertebrate evolution",

abstract = "The sea lamprey (Petromyzon marinus) serves as a comparative model for reconstructing vertebrate evolution. To enable more informed analyses, we developed a new assembly of the lamprey germline genome that integrates several complementary data sets. Analysis of this highly contiguous (chromosome-scale) assembly shows that both chromosomal and whole-genome duplications have played significant roles in the evolution of ancestral vertebrate and lamprey genomes, including chromosomes that carry the six lamprey HOX clusters. The assembly also contains several hundred genes that are reproducibly eliminated from somatic cells during early development in lamprey. Comparative analyses show that gnathostome (mouse) homologs of these genes are frequently marked by polycomb repressive complexes (PRCs) in embryonic stem cells, suggesting overlaps in the regulatory logic of somatic DNA elimination and bivalent states that are regulated by early embryonic PRCs. This new assembly will enhance diverse studies that are informed by lampreys' unique biology and evolutionary/comparative perspective.",

author = "Smith, {Jeramiah J.} and Nataliya Timoshevskaya and Chengxi Ye and Carson Holt and Keinath, {Melissa C.} and Parker, {Hugo J.} and Cook, {Malcolm E.} and Hess, {Jon E.} and Narum, {Shawn R.} and Francesco Lamanna and Henrik Kaessmann and Timoshevskiy, {Vladimir A.} and Waterbury, {Courtney K.M.} and Cody Saraceno and Wiedemann, {Leanne M.} and Robb, {Sofia M.C.} and Carl Baker and Eichler, {Evan E.} and Dorit Hockman and Tatjana Sauka-Spengler and Mark Yandell and Robb Krumlauf and Greg Elgar and Amemiya, {Chris T.}",

note = "Funding Information: Research reported in this publication was supported by the National Institute of General Medical Sciences of the US National Institutes of Health under award number R01GM104123 to J.J.S., the Stowers Institute under award number SIMR-1001 to H.J.P., M.E.C., L.M.W., S.M.C.R. and R.K., and the Bonneville Power Administration to J.E.H. and S.R.N. E.E.E. is an investigator of the Howard Hughes Medical Institute. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Support and resources from the Center for High Performance Computing at the University of Utah are gratefully acknowledged. Additional computational support was provided by The University of Kentucky High Performance Computing complex. Publisher Copyright: {\textcopyright} 2018 The Author(s).",

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doi = "10.1038/s41588-017-0036-1",

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Smith, JJ, Timoshevskaya, N, Ye, C, Holt, C, Keinath, MC, Parker, HJ, Cook, ME, Hess, JE, Narum, SR, Lamanna, F, Kaessmann, H, Timoshevskiy, VA, Waterbury, CKM, Saraceno, C, Wiedemann, LM, Robb, SMC, Baker, C, Eichler, EE, Hockman, D, Sauka-Spengler, T, Yandell, M, Krumlauf, R, Elgar, G & Amemiya, CT 2018, 'The sea lamprey germline genome provides insights into programmed genome rearrangement and vertebrate evolution', Nature Genetics, vol. 50, no. 2, pp. 270-277. https://doi.org/10.1038/s41588-017-0036-1

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T1 - The sea lamprey germline genome provides insights into programmed genome rearrangement and vertebrate evolution

AU - Smith, Jeramiah J.

AU - Timoshevskaya, Nataliya

AU - Ye, Chengxi

AU - Holt, Carson

AU - Keinath, Melissa C.

AU - Parker, Hugo J.

AU - Cook, Malcolm E.

AU - Hess, Jon E.

AU - Narum, Shawn R.

AU - Lamanna, Francesco

AU - Kaessmann, Henrik

AU - Timoshevskiy, Vladimir A.

AU - Waterbury, Courtney K.M.

AU - Saraceno, Cody

AU - Wiedemann, Leanne M.

AU - Robb, Sofia M.C.

AU - Baker, Carl

AU - Eichler, Evan E.

AU - Hockman, Dorit

AU - Sauka-Spengler, Tatjana

AU - Yandell, Mark

AU - Krumlauf, Robb

AU - Elgar, Greg

AU - Amemiya, Chris T.

N1 - Funding Information: Research reported in this publication was supported by the National Institute of General Medical Sciences of the US National Institutes of Health under award number R01GM104123 to J.J.S., the Stowers Institute under award number SIMR-1001 to H.J.P., M.E.C., L.M.W., S.M.C.R. and R.K., and the Bonneville Power Administration to J.E.H. and S.R.N. E.E.E. is an investigator of the Howard Hughes Medical Institute. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Support and resources from the Center for High Performance Computing at the University of Utah are gratefully acknowledged. Additional computational support was provided by The University of Kentucky High Performance Computing complex. Publisher Copyright: © 2018 The Author(s).

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N2 - The sea lamprey (Petromyzon marinus) serves as a comparative model for reconstructing vertebrate evolution. To enable more informed analyses, we developed a new assembly of the lamprey germline genome that integrates several complementary data sets. Analysis of this highly contiguous (chromosome-scale) assembly shows that both chromosomal and whole-genome duplications have played significant roles in the evolution of ancestral vertebrate and lamprey genomes, including chromosomes that carry the six lamprey HOX clusters. The assembly also contains several hundred genes that are reproducibly eliminated from somatic cells during early development in lamprey. Comparative analyses show that gnathostome (mouse) homologs of these genes are frequently marked by polycomb repressive complexes (PRCs) in embryonic stem cells, suggesting overlaps in the regulatory logic of somatic DNA elimination and bivalent states that are regulated by early embryonic PRCs. This new assembly will enhance diverse studies that are informed by lampreys' unique biology and evolutionary/comparative perspective.

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The sea lamprey germline genome provides insights into programmed genome rearrangement and vertebrate evolution

Abstract

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ASJC Scopus subject areas

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