An improved germline genome assembly for the sea lamprey Petromyzon marinus illuminates the evolution of germline-specific chromosomes

Nataliya Timoshevskaya; Kaan Eşkut; Vladimir A. Timoshevskiy; Sofia M.C. Robb; Carson Holt; Jon E. Hess; Hugo J. Parker; Cindy F. Baker; Allison K. Miller; Cody Saraceno; Mark Yandell; Robb Krumlauf; Shawn R. Narum; Ralph T. Lampman; Neil J. Gemmell; Jacquelyn Mountcastle; Bettina Haase; Jennifer R. Balacco; Giulio Formenti; Sarah Pelan; Ying Sims; Kerstin Howe; Olivier Fedrigo; Erich D. Jarvis; Jeramiah J. Smith

doi:10.1016/j.celrep.2023.112263

An improved germline genome assembly for the sea lamprey Petromyzon marinus illuminates the evolution of germline-specific chromosomes

Nataliya Timoshevskaya, Kaan Eşkut, Vladimir A. Timoshevskiy, Sofia M.C. Robb, Carson Holt, Jon E. Hess, Hugo J. Parker, Cindy F. Baker, Allison K. Miller, Cody Saraceno, Mark Yandell, Robb Krumlauf, Shawn R. Narum, Ralph T. Lampman, Neil J. Gemmell, Jacquelyn Mountcastle, Bettina Haase, Jennifer R. Balacco, Giulio Formenti, Sarah PelanYing Sims, Kerstin Howe, Olivier Fedrigo, Erich D. Jarvis, Jeramiah J. Smith

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

3 Scopus citations

Abstract

Programmed DNA loss is a gene silencing mechanism that is employed by several vertebrate and nonvertebrate lineages, including all living jawless vertebrates and songbirds. Reconstructing the evolution of somatically eliminated (germline-specific) sequences in these species has proven challenging due to a high content of repeats and gene duplications in eliminated sequences and a corresponding lack of highly accurate and contiguous assemblies for these regions. Here, we present an improved assembly of the sea lamprey (Petromyzon marinus) genome that was generated using recently standardized methods that increase the contiguity and accuracy of vertebrate genome assemblies. This assembly resolves highly contiguous, somatically retained chromosomes and at least one germline-specific chromosome, permitting new analyses that reconstruct the timing, mode, and repercussions of recruitment of genes to the germline-specific fraction. These analyses reveal major roles of interchromosomal segmental duplication, intrachromosomal duplication, and positive selection for germline functions in the long-term evolution of germline-specific chromosomes.

Original language	English
Article number	112263
Journal	Cell Reports
Volume	42
Issue number	3
DOIs	https://doi.org/10.1016/j.celrep.2023.112263
State	Published - Mar 28 2023

Bibliographical note

Funding Information:
We thank Jane Kitson for facilitating discussions to ensure the appropriate representation of Maori iwi interests in relation to the collection and presentation of data from kanakana/piharau. The contents of this paper are solely the responsibility of the authors and do not necessarily represent the official views of NIH or NSF. Partial computational support was provided by The University of Kentucky High Performance Computing complex. The support and resources from the Center for High Performance Computing at the University of Utah are gratefully acknowledged. This work was funded by grants from the National Institutes of Health (NIH) ( R35GM130349 ) and the National Science Foundation (NSF) ( MCB1818012 ) to J.J.S., a grant from the Great Lakes Fishery Commission to J.J.S. and E.D.J., HHMI funds to E.D.J., and New Zealand Ministry of Business Innovation and Employment ( MBIE ) contract C01X1615 to C.F.B. A.K.M. and N.J.G. are supported by the University of Otago and a subcontract from C01X1615 .

Funding Information:
We thank Jane Kitson for facilitating discussions to ensure the appropriate representation of Maori iwi interests in relation to the collection and presentation of data from kanakana/piharau. The contents of this paper are solely the responsibility of the authors and do not necessarily represent the official views of NIH or NSF. Partial computational support was provided by The University of Kentucky High Performance Computing complex. The support and resources from the Center for High Performance Computing at the University of Utah are gratefully acknowledged. This work was funded by grants from the National Institutes of Health (NIH) (R35GM130349) and the National Science Foundation (NSF) (MCB1818012) to J.J.S. a grant from the Great Lakes Fishery Commission to J.J.S. and E.D.J. HHMI funds to E.D.J. and New Zealand Ministry of Business Innovation and Employment (MBIE) contract C01X1615 to C.F.B. A.K.M. and N.J.G. are supported by the University of Otago and a subcontract from C01X1615. Conceptualization, J.J.S. and E.D.J.; investigation, N.T. K.İ.E. V.A.T. S.M.C.R. C.H. J.E.H. H.J.P. C.F.B. A.K.M. C.S. S.R.N. R.T.L. J.M. B.H. J.R.B. G.F. S.P. Y.S. K.H. and O.F.; writing – original draft, J.J.S.; writing – review & editing, N.T. and E.D.J.; funding acquisition, J.J.S. E.D.J. and C.F.B.; resources, M.Y. N.J.G. and R.K.; supervision, J.J.S. and E.D.J. The authors declare no competing interests. One or more of the authors of this paper self-identifies as an underrepresented ethnic minority in their field of research or within their geographical location. One or more of the authors of this paper received support from a program designed to increase minority representation in their field of research. We avoided “helicopter science” practices by including the participating local contributors from the region where we conducted the research as authors on the paper.

Publisher Copyright:
© 2023 The Authors

Keywords

CP: Molecular biology
assembly
chromatin diminution
chromosome
evolution
genome
germline
lamprey
programmed DNA loss

ASJC Scopus subject areas

Biochemistry, Genetics and Molecular Biology (all)

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10.1016/j.celrep.2023.112263

Cite this

Timoshevskaya, N., Eşkut, K., Timoshevskiy, V. A., Robb, S. M. C., Holt, C., Hess, J. E., Parker, H. J., Baker, C. F., Miller, A. K., Saraceno, C., Yandell, M., Krumlauf, R., Narum, S. R., Lampman, R. T., Gemmell, N. J., Mountcastle, J., Haase, B., Balacco, J. R., Formenti, G., ... Smith, J. J. (2023). An improved germline genome assembly for the sea lamprey Petromyzon marinus illuminates the evolution of germline-specific chromosomes. Cell Reports, 42(3), Article 112263. https://doi.org/10.1016/j.celrep.2023.112263

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title = "An improved germline genome assembly for the sea lamprey Petromyzon marinus illuminates the evolution of germline-specific chromosomes",

abstract = "Programmed DNA loss is a gene silencing mechanism that is employed by several vertebrate and nonvertebrate lineages, including all living jawless vertebrates and songbirds. Reconstructing the evolution of somatically eliminated (germline-specific) sequences in these species has proven challenging due to a high content of repeats and gene duplications in eliminated sequences and a corresponding lack of highly accurate and contiguous assemblies for these regions. Here, we present an improved assembly of the sea lamprey (Petromyzon marinus) genome that was generated using recently standardized methods that increase the contiguity and accuracy of vertebrate genome assemblies. This assembly resolves highly contiguous, somatically retained chromosomes and at least one germline-specific chromosome, permitting new analyses that reconstruct the timing, mode, and repercussions of recruitment of genes to the germline-specific fraction. These analyses reveal major roles of interchromosomal segmental duplication, intrachromosomal duplication, and positive selection for germline functions in the long-term evolution of germline-specific chromosomes.",

keywords = "CP: Molecular biology, assembly, chromatin diminution, chromosome, evolution, genome, germline, lamprey, programmed DNA loss",

author = "Nataliya Timoshevskaya and Kaan E{\c s}kut and Timoshevskiy, {Vladimir A.} and Robb, {Sofia M.C.} and Carson Holt and Hess, {Jon E.} and Parker, {Hugo J.} and Baker, {Cindy F.} and Miller, {Allison K.} and Cody Saraceno and Mark Yandell and Robb Krumlauf and Narum, {Shawn R.} and Lampman, {Ralph T.} and Gemmell, {Neil J.} and Jacquelyn Mountcastle and Bettina Haase and Balacco, {Jennifer R.} and Giulio Formenti and Sarah Pelan and Ying Sims and Kerstin Howe and Olivier Fedrigo and Jarvis, {Erich D.} and Smith, {Jeramiah J.}",

note = "Funding Information: We thank Jane Kitson for facilitating discussions to ensure the appropriate representation of Maori iwi interests in relation to the collection and presentation of data from kanakana/piharau. The contents of this paper are solely the responsibility of the authors and do not necessarily represent the official views of NIH or NSF. Partial computational support was provided by The University of Kentucky High Performance Computing complex. The support and resources from the Center for High Performance Computing at the University of Utah are gratefully acknowledged. This work was funded by grants from the National Institutes of Health (NIH) ( R35GM130349 ) and the National Science Foundation (NSF) ( MCB1818012 ) to J.J.S., a grant from the Great Lakes Fishery Commission to J.J.S. and E.D.J., HHMI funds to E.D.J., and New Zealand Ministry of Business Innovation and Employment ( MBIE ) contract C01X1615 to C.F.B. A.K.M. and N.J.G. are supported by the University of Otago and a subcontract from C01X1615 . Funding Information: We thank Jane Kitson for facilitating discussions to ensure the appropriate representation of Maori iwi interests in relation to the collection and presentation of data from kanakana/piharau. The contents of this paper are solely the responsibility of the authors and do not necessarily represent the official views of NIH or NSF. Partial computational support was provided by The University of Kentucky High Performance Computing complex. The support and resources from the Center for High Performance Computing at the University of Utah are gratefully acknowledged. This work was funded by grants from the National Institutes of Health (NIH) (R35GM130349) and the National Science Foundation (NSF) (MCB1818012) to J.J.S. a grant from the Great Lakes Fishery Commission to J.J.S. and E.D.J. HHMI funds to E.D.J. and New Zealand Ministry of Business Innovation and Employment (MBIE) contract C01X1615 to C.F.B. A.K.M. and N.J.G. are supported by the University of Otago and a subcontract from C01X1615. Conceptualization, J.J.S. and E.D.J.; investigation, N.T. K.İ.E. V.A.T. S.M.C.R. C.H. J.E.H. H.J.P. C.F.B. A.K.M. C.S. S.R.N. R.T.L. J.M. B.H. J.R.B. G.F. S.P. Y.S. K.H. and O.F.; writing – original draft, J.J.S.; writing – review & editing, N.T. and E.D.J.; funding acquisition, J.J.S. E.D.J. and C.F.B.; resources, M.Y. N.J.G. and R.K.; supervision, J.J.S. and E.D.J. The authors declare no competing interests. One or more of the authors of this paper self-identifies as an underrepresented ethnic minority in their field of research or within their geographical location. One or more of the authors of this paper received support from a program designed to increase minority representation in their field of research. We avoided “helicopter science” practices by including the participating local contributors from the region where we conducted the research as authors on the paper. Publisher Copyright: {\textcopyright} 2023 The Authors",

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Timoshevskaya, N, Eşkut, K, Timoshevskiy, VA, Robb, SMC, Holt, C, Hess, JE, Parker, HJ, Baker, CF, Miller, AK, Saraceno, C, Yandell, M, Krumlauf, R, Narum, SR, Lampman, RT, Gemmell, NJ, Mountcastle, J, Haase, B, Balacco, JR, Formenti, G, Pelan, S, Sims, Y, Howe, K, Fedrigo, O, Jarvis, ED & Smith, JJ 2023, 'An improved germline genome assembly for the sea lamprey Petromyzon marinus illuminates the evolution of germline-specific chromosomes', Cell Reports, vol. 42, no. 3, 112263. https://doi.org/10.1016/j.celrep.2023.112263

TY - JOUR

T1 - An improved germline genome assembly for the sea lamprey Petromyzon marinus illuminates the evolution of germline-specific chromosomes

AU - Timoshevskaya, Nataliya

AU - Eşkut, Kaan

AU - Timoshevskiy, Vladimir A.

AU - Robb, Sofia M.C.

AU - Holt, Carson

AU - Hess, Jon E.

AU - Parker, Hugo J.

AU - Baker, Cindy F.

AU - Miller, Allison K.

AU - Saraceno, Cody

AU - Yandell, Mark

AU - Krumlauf, Robb

AU - Narum, Shawn R.

AU - Lampman, Ralph T.

AU - Gemmell, Neil J.

AU - Mountcastle, Jacquelyn

AU - Haase, Bettina

AU - Balacco, Jennifer R.

AU - Formenti, Giulio

AU - Pelan, Sarah

AU - Sims, Ying

AU - Howe, Kerstin

AU - Fedrigo, Olivier

AU - Jarvis, Erich D.

AU - Smith, Jeramiah J.

N1 - Funding Information: We thank Jane Kitson for facilitating discussions to ensure the appropriate representation of Maori iwi interests in relation to the collection and presentation of data from kanakana/piharau. The contents of this paper are solely the responsibility of the authors and do not necessarily represent the official views of NIH or NSF. Partial computational support was provided by The University of Kentucky High Performance Computing complex. The support and resources from the Center for High Performance Computing at the University of Utah are gratefully acknowledged. This work was funded by grants from the National Institutes of Health (NIH) ( R35GM130349 ) and the National Science Foundation (NSF) ( MCB1818012 ) to J.J.S., a grant from the Great Lakes Fishery Commission to J.J.S. and E.D.J., HHMI funds to E.D.J., and New Zealand Ministry of Business Innovation and Employment ( MBIE ) contract C01X1615 to C.F.B. A.K.M. and N.J.G. are supported by the University of Otago and a subcontract from C01X1615 . Funding Information: We thank Jane Kitson for facilitating discussions to ensure the appropriate representation of Maori iwi interests in relation to the collection and presentation of data from kanakana/piharau. The contents of this paper are solely the responsibility of the authors and do not necessarily represent the official views of NIH or NSF. Partial computational support was provided by The University of Kentucky High Performance Computing complex. The support and resources from the Center for High Performance Computing at the University of Utah are gratefully acknowledged. This work was funded by grants from the National Institutes of Health (NIH) (R35GM130349) and the National Science Foundation (NSF) (MCB1818012) to J.J.S. a grant from the Great Lakes Fishery Commission to J.J.S. and E.D.J. HHMI funds to E.D.J. and New Zealand Ministry of Business Innovation and Employment (MBIE) contract C01X1615 to C.F.B. A.K.M. and N.J.G. are supported by the University of Otago and a subcontract from C01X1615. Conceptualization, J.J.S. and E.D.J.; investigation, N.T. K.İ.E. V.A.T. S.M.C.R. C.H. J.E.H. H.J.P. C.F.B. A.K.M. C.S. S.R.N. R.T.L. J.M. B.H. J.R.B. G.F. S.P. Y.S. K.H. and O.F.; writing – original draft, J.J.S.; writing – review & editing, N.T. and E.D.J.; funding acquisition, J.J.S. E.D.J. and C.F.B.; resources, M.Y. N.J.G. and R.K.; supervision, J.J.S. and E.D.J. The authors declare no competing interests. One or more of the authors of this paper self-identifies as an underrepresented ethnic minority in their field of research or within their geographical location. One or more of the authors of this paper received support from a program designed to increase minority representation in their field of research. We avoided “helicopter science” practices by including the participating local contributors from the region where we conducted the research as authors on the paper. Publisher Copyright: © 2023 The Authors

PY - 2023/3/28

Y1 - 2023/3/28

N2 - Programmed DNA loss is a gene silencing mechanism that is employed by several vertebrate and nonvertebrate lineages, including all living jawless vertebrates and songbirds. Reconstructing the evolution of somatically eliminated (germline-specific) sequences in these species has proven challenging due to a high content of repeats and gene duplications in eliminated sequences and a corresponding lack of highly accurate and contiguous assemblies for these regions. Here, we present an improved assembly of the sea lamprey (Petromyzon marinus) genome that was generated using recently standardized methods that increase the contiguity and accuracy of vertebrate genome assemblies. This assembly resolves highly contiguous, somatically retained chromosomes and at least one germline-specific chromosome, permitting new analyses that reconstruct the timing, mode, and repercussions of recruitment of genes to the germline-specific fraction. These analyses reveal major roles of interchromosomal segmental duplication, intrachromosomal duplication, and positive selection for germline functions in the long-term evolution of germline-specific chromosomes.

AB - Programmed DNA loss is a gene silencing mechanism that is employed by several vertebrate and nonvertebrate lineages, including all living jawless vertebrates and songbirds. Reconstructing the evolution of somatically eliminated (germline-specific) sequences in these species has proven challenging due to a high content of repeats and gene duplications in eliminated sequences and a corresponding lack of highly accurate and contiguous assemblies for these regions. Here, we present an improved assembly of the sea lamprey (Petromyzon marinus) genome that was generated using recently standardized methods that increase the contiguity and accuracy of vertebrate genome assemblies. This assembly resolves highly contiguous, somatically retained chromosomes and at least one germline-specific chromosome, permitting new analyses that reconstruct the timing, mode, and repercussions of recruitment of genes to the germline-specific fraction. These analyses reveal major roles of interchromosomal segmental duplication, intrachromosomal duplication, and positive selection for germline functions in the long-term evolution of germline-specific chromosomes.

KW - CP: Molecular biology

KW - assembly

KW - chromatin diminution

KW - chromosome

KW - evolution

KW - genome

KW - germline

KW - lamprey

KW - programmed DNA loss

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U2 - 10.1016/j.celrep.2023.112263

DO - 10.1016/j.celrep.2023.112263

M3 - Article

C2 - 36930644

AN - SCOPUS:85150029905

SN - 2211-1247

VL - 42

JO - Cell Reports

JF - Cell Reports

IS - 3

M1 - 112263

ER -

An improved germline genome assembly for the sea lamprey Petromyzon marinus illuminates the evolution of germline-specific chromosomes

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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