Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution

Jeramiah J. Smith; Shigehiro Kuraku; Carson Holt; Tatjana Sauka-Spengler; Ning Jiang; Michael S. Campbell; Mark D. Yandell; Tereza Manousaki; Axel Meyer; Ona E. Bloom; Jennifer R. Morgan; Joseph D. Buxbaum; Ravi Sachidanandam; Carrie Sims; Alexander S. Garruss; Malcolm Cook; Robb Krumlauf; Leanne M. Wiedemann; Stacia A. Sower; Wayne A. Decatur; Jeffrey A. Hall; Chris T. Amemiya; Nil R. Saha; Katherine M. Buckley; Jonathan P. Rast; Sabyasachi Das; Masayuki Hirano; Nathanael McCurley; Peng Guo; Nicolas Rohner; Clifford J. Tabin; Paul Piccinelli; Greg Elgar; Magali Ruffier; Bronwen L. Aken; Stephen M.J. Searle; Matthieu Muffato; Miguel Pignatelli; Javier Herrero; Matthew Jones; C. Titus Brown; Yu Wen Chung-Davidson; Kaben G. Nanlohy; Scot V. Libants; Chu Yin Yeh; David W. McCauley; James A. Langeland; Zeev Pancer; Bernd Fritzsch; Pieter J. De Jong; Baoli Zhu; Lucinda L. Fulton; Brenda Theising; Paul Flicek; Marianne E. Bronner; Wesley C. Warren; Sandra W. Clifton; Richard K. Wilson; Weiming Li

doi:10.1038/ng.2568

Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution

Jeramiah J. Smith, Shigehiro Kuraku, Carson Holt, Tatjana Sauka-Spengler, Ning Jiang, Michael S. Campbell, Mark D. Yandell, Tereza Manousaki, Axel Meyer, Ona E. Bloom, Jennifer R. Morgan, Joseph D. Buxbaum, Ravi Sachidanandam, Carrie Sims, Alexander S. Garruss, Malcolm Cook, Robb Krumlauf, Leanne M. Wiedemann, Stacia A. Sower, Wayne A. DecaturJeffrey A. Hall, Chris T. Amemiya, Nil R. Saha, Katherine M. Buckley, Jonathan P. Rast, Sabyasachi Das, Masayuki Hirano, Nathanael McCurley, Peng Guo, Nicolas Rohner, Clifford J. Tabin, Paul Piccinelli, Greg Elgar, Magali Ruffier, Bronwen L. Aken, Stephen M.J. Searle, Matthieu Muffato, Miguel Pignatelli, Javier Herrero, Matthew Jones, C. Titus Brown, Yu Wen Chung-Davidson, Kaben G. Nanlohy, Scot V. Libants, Chu Yin Yeh, David W. McCauley, James A. Langeland, Zeev Pancer, Bernd Fritzsch, Pieter J. De Jong, Baoli Zhu, Lucinda L. Fulton, Brenda Theising, Paul Flicek, Marianne E. Bronner, Wesley C. Warren, Sandra W. Clifton, Richard K. Wilson, Weiming Li

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

510 Scopus citations

Abstract

Lampreys are representatives of an ancient vertebrate lineage that diverged from our own ∼500 million years ago. By virtue of this deeply shared ancestry, the sea lamprey (P. marinus) genome is uniquely poised to provide insight into the ancestry of vertebrate genomes and the underlying principles of vertebrate biology. Here, we present the first lamprey whole-genome sequence and assembly. We note challenges faced owing to its high content of repetitive elements and GC bases, as well as the absence of broad-scale sequence information from closely related species. Analyses of the assembly indicate that two whole-genome duplications likely occurred before the divergence of ancestral lamprey and gnathostome lineages. Moreover, the results help define key evolutionary events within vertebrate lineages, including the origin of myelin-associated proteins and the development of appendages. The lamprey genome provides an important resource for reconstructing vertebrate origins and the evolutionary events that have shaped the genomes of extant organisms.

Original language	English
Pages (from-to)	415-421
Number of pages	7
Journal	Nature Genetics
Volume	45
Issue number	4
DOIs	https://doi.org/10.1038/ng.2568
State	Published - Apr 2013

Bibliographical note

Funding Information:
We thank the Genome Institute, Washington University School of Medicine, Production Sequencing group for all sample procurement and genome sequencing work, the Michigan State University Genomic Core for transcriptome sequencing and the US Geological Survey, Lake Huron Biological Station for providing lamprey samples for sequencing. We thank F. Antonacci and E.E. Eichler (University of Washington) for performing FISH and providing access to computational facilities, respectively. We thank M. Robinson for bioinformatic analysis of immune system–related genes and conversion of GFF files for BAC end mapping. A portion of this research was conducted at the Marine Biological Laboratory (Woods Hole, Massachusetts). We acknowledge the support of the Stowers Institute for Medical Research (SIMR) and technical support from the SIMR Molecular Biology Core, particularly K. Staehling, A. Perera and K. Delventhal for BAC screening and sequencing. We acknowledge the Center for High-Performance Computing at the University of Utah for the allocation of computational resources toward gene annotation. We recognize all the important work that could not be cited owing to space limitations. The lamprey genome project was funded by the National Human Genome Research Institute (U54HG003079 (R.K.W.)). Additional support was provided by grants from the US National Institutes of Health (R24GM83982 (W.L.)) and the Great Lakes Fisheries commission (W.L.). Partial funding was provided by several additional sources, including grants from the US National Institutes of Health (F32GM087919 and T32HG00035 (J.J.S.); DE017911 (M.E.B.); R03NS078519 (O.E.B.); R01HG004694 (M.D.Y.); GM079492, GM090049 and RR014085 (C.T.A.); and R37HD032443 (C.J.T.)), the National Science Foundation (MCB-0719558 (C.T.A.); IOS-0849569 (S.A.S.); IBN-0208138 (L. Holland); and IOS-1126998 (M.D.Y.)), the New Hampshire Agricultural Experiment Station (Scientific Contribution Number 2471 (S.A.S.)), the Charles Evans Research Award (O.E.B., J.D.B. and J.R.M.), the Wellcome Trust (WT095908 (P.F.) and WT098051), the Canadian Institutes of Health Research (MOP74667 (J.P.R.)) and the Natural Sciences and Engineering Research Council of Canada (312221 (J.P.R.)).

Funding

We thank the Genome Institute, Washington University School of Medicine, Production Sequencing group for all sample procurement and genome sequencing work, the Michigan State University Genomic Core for transcriptome sequencing and the US Geological Survey, Lake Huron Biological Station for providing lamprey samples for sequencing. We thank F. Antonacci and E.E. Eichler (University of Washington) for performing FISH and providing access to computational facilities, respectively. We thank M. Robinson for bioinformatic analysis of immune system–related genes and conversion of GFF files for BAC end mapping. A portion of this research was conducted at the Marine Biological Laboratory (Woods Hole, Massachusetts). We acknowledge the support of the Stowers Institute for Medical Research (SIMR) and technical support from the SIMR Molecular Biology Core, particularly K. Staehling, A. Perera and K. Delventhal for BAC screening and sequencing. We acknowledge the Center for High-Performance Computing at the University of Utah for the allocation of computational resources toward gene annotation. We recognize all the important work that could not be cited owing to space limitations. The lamprey genome project was funded by the National Human Genome Research Institute (U54HG003079 (R.K.W.)). Additional support was provided by grants from the US National Institutes of Health (R24GM83982 (W.L.)) and the Great Lakes Fisheries commission (W.L.). Partial funding was provided by several additional sources, including grants from the US National Institutes of Health (F32GM087919 and T32HG00035 (J.J.S.); DE017911 (M.E.B.); R03NS078519 (O.E.B.); R01HG004694 (M.D.Y.); GM079492, GM090049 and RR014085 (C.T.A.); and R37HD032443 (C.J.T.)), the National Science Foundation (MCB-0719558 (C.T.A.); IOS-0849569 (S.A.S.); IBN-0208138 (L. Holland); and IOS-1126998 (M.D.Y.)), the New Hampshire Agricultural Experiment Station (Scientific Contribution Number 2471 (S.A.S.)), the Charles Evans Research Award (O.E.B., J.D.B. and J.R.M.), the Wellcome Trust (WT095908 (P.F.) and WT098051), the Canadian Institutes of Health Research (MOP74667 (J.P.R.)) and the Natural Sciences and Engineering Research Council of Canada (312221 (J.P.R.)).

Funders	Funder number
New Hampshire Agricultural Experiment Station
National Science Foundation Arctic Social Science Program	IBN-0208138, MCB-0719558, IOS-1126998, IOS-0849569
National Science Foundation Arctic Social Science Program
National Institutes of Health (NIH)	R24GM83982
National Institutes of Health (NIH)
National Human Genome Research Institute	T32HG000035, R01HG004694, U54HG003079
National Human Genome Research Institute
Great Lakes Fishery Commission	GM090049, R03NS078519, DE017911, R37HD032443, RR014085, T32HG00035, GM079492, F32GM087919
Great Lakes Fishery Commission
Stowers Institute for Medical Research
Wellcome Trust	WT095908, WT098051
Wellcome Trust
Canadian Institutes of Health Research	MOP74667
Canadian Institutes of Health Research
Natural Sciences and Engineering Research Council of Canada	312221
Natural Sciences and Engineering Research Council of Canada

ASJC Scopus subject areas

Genetics

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10.1038/ng.2568

Cite this

Smith, J. J., Kuraku, S., Holt, C., Sauka-Spengler, T., Jiang, N., Campbell, M. S., Yandell, M. D., Manousaki, T., Meyer, A., Bloom, O. E., Morgan, J. R., Buxbaum, J. D., Sachidanandam, R., Sims, C., Garruss, A. S., Cook, M., Krumlauf, R., Wiedemann, L. M., Sower, S. A., ... Li, W. (2013). Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nature Genetics, 45(4), 415-421. https://doi.org/10.1038/ng.2568

@article{2df6aba26f554ef0bfe29cc579208d05,

title = "Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution",

abstract = "Lampreys are representatives of an ancient vertebrate lineage that diverged from our own ∼500 million years ago. By virtue of this deeply shared ancestry, the sea lamprey (P. marinus) genome is uniquely poised to provide insight into the ancestry of vertebrate genomes and the underlying principles of vertebrate biology. Here, we present the first lamprey whole-genome sequence and assembly. We note challenges faced owing to its high content of repetitive elements and GC bases, as well as the absence of broad-scale sequence information from closely related species. Analyses of the assembly indicate that two whole-genome duplications likely occurred before the divergence of ancestral lamprey and gnathostome lineages. Moreover, the results help define key evolutionary events within vertebrate lineages, including the origin of myelin-associated proteins and the development of appendages. The lamprey genome provides an important resource for reconstructing vertebrate origins and the evolutionary events that have shaped the genomes of extant organisms.",

author = "Smith, {Jeramiah J.} and Shigehiro Kuraku and Carson Holt and Tatjana Sauka-Spengler and Ning Jiang and Campbell, {Michael S.} and Yandell, {Mark D.} and Tereza Manousaki and Axel Meyer and Bloom, {Ona E.} and Morgan, {Jennifer R.} and Buxbaum, {Joseph D.} and Ravi Sachidanandam and Carrie Sims and Garruss, {Alexander S.} and Malcolm Cook and Robb Krumlauf and Wiedemann, {Leanne M.} and Sower, {Stacia A.} and Decatur, {Wayne A.} and Hall, {Jeffrey A.} and Amemiya, {Chris T.} and Saha, {Nil R.} and Buckley, {Katherine M.} and Rast, {Jonathan P.} and Sabyasachi Das and Masayuki Hirano and Nathanael McCurley and Peng Guo and Nicolas Rohner and Tabin, {Clifford J.} and Paul Piccinelli and Greg Elgar and Magali Ruffier and Aken, {Bronwen L.} and Searle, {Stephen M.J.} and Matthieu Muffato and Miguel Pignatelli and Javier Herrero and Matthew Jones and Brown, {C. Titus} and Chung-Davidson, {Yu Wen} and Nanlohy, {Kaben G.} and Libants, {Scot V.} and Yeh, {Chu Yin} and McCauley, {David W.} and Langeland, {James A.} and Zeev Pancer and Bernd Fritzsch and {De Jong}, {Pieter J.} and Baoli Zhu and Fulton, {Lucinda L.} and Brenda Theising and Paul Flicek and Bronner, {Marianne E.} and Warren, {Wesley C.} and Clifton, {Sandra W.} and Wilson, {Richard K.} and Weiming Li",

note = "Funding Information: We thank the Genome Institute, Washington University School of Medicine, Production Sequencing group for all sample procurement and genome sequencing work, the Michigan State University Genomic Core for transcriptome sequencing and the US Geological Survey, Lake Huron Biological Station for providing lamprey samples for sequencing. We thank F. Antonacci and E.E. Eichler (University of Washington) for performing FISH and providing access to computational facilities, respectively. We thank M. Robinson for bioinformatic analysis of immune system–related genes and conversion of GFF files for BAC end mapping. A portion of this research was conducted at the Marine Biological Laboratory (Woods Hole, Massachusetts). We acknowledge the support of the Stowers Institute for Medical Research (SIMR) and technical support from the SIMR Molecular Biology Core, particularly K. Staehling, A. Perera and K. Delventhal for BAC screening and sequencing. We acknowledge the Center for High-Performance Computing at the University of Utah for the allocation of computational resources toward gene annotation. We recognize all the important work that could not be cited owing to space limitations. The lamprey genome project was funded by the National Human Genome Research Institute (U54HG003079 (R.K.W.)). Additional support was provided by grants from the US National Institutes of Health (R24GM83982 (W.L.)) and the Great Lakes Fisheries commission (W.L.). Partial funding was provided by several additional sources, including grants from the US National Institutes of Health (F32GM087919 and T32HG00035 (J.J.S.); DE017911 (M.E.B.); R03NS078519 (O.E.B.); R01HG004694 (M.D.Y.); GM079492, GM090049 and RR014085 (C.T.A.); and R37HD032443 (C.J.T.)), the National Science Foundation (MCB-0719558 (C.T.A.); IOS-0849569 (S.A.S.); IBN-0208138 (L. Holland); and IOS-1126998 (M.D.Y.)), the New Hampshire Agricultural Experiment Station (Scientific Contribution Number 2471 (S.A.S.)), the Charles Evans Research Award (O.E.B., J.D.B. and J.R.M.), the Wellcome Trust (WT095908 (P.F.) and WT098051), the Canadian Institutes of Health Research (MOP74667 (J.P.R.)) and the Natural Sciences and Engineering Research Council of Canada (312221 (J.P.R.)).",

year = "2013",

month = apr,

doi = "10.1038/ng.2568",

language = "English",

volume = "45",

pages = "415--421",

number = "4",

}

Smith, JJ, Kuraku, S, Holt, C, Sauka-Spengler, T, Jiang, N, Campbell, MS, Yandell, MD, Manousaki, T, Meyer, A, Bloom, OE, Morgan, JR, Buxbaum, JD, Sachidanandam, R, Sims, C, Garruss, AS, Cook, M, Krumlauf, R, Wiedemann, LM, Sower, SA, Decatur, WA, Hall, JA, Amemiya, CT, Saha, NR, Buckley, KM, Rast, JP, Das, S, Hirano, M, McCurley, N, Guo, P, Rohner, N, Tabin, CJ, Piccinelli, P, Elgar, G, Ruffier, M, Aken, BL, Searle, SMJ, Muffato, M, Pignatelli, M, Herrero, J, Jones, M, Brown, CT, Chung-Davidson, YW, Nanlohy, KG, Libants, SV, Yeh, CY, McCauley, DW, Langeland, JA, Pancer, Z, Fritzsch, B, De Jong, PJ, Zhu, B, Fulton, LL, Theising, B, Flicek, P, Bronner, ME, Warren, WC, Clifton, SW, Wilson, RK & Li, W 2013, 'Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution', Nature Genetics, vol. 45, no. 4, pp. 415-421. https://doi.org/10.1038/ng.2568

TY - JOUR

T1 - Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution

AU - Smith, Jeramiah J.

AU - Kuraku, Shigehiro

AU - Holt, Carson

AU - Sauka-Spengler, Tatjana

AU - Jiang, Ning

AU - Campbell, Michael S.

AU - Yandell, Mark D.

AU - Manousaki, Tereza

AU - Meyer, Axel

AU - Bloom, Ona E.

AU - Morgan, Jennifer R.

AU - Buxbaum, Joseph D.

AU - Sachidanandam, Ravi

AU - Sims, Carrie

AU - Garruss, Alexander S.

AU - Cook, Malcolm

AU - Krumlauf, Robb

AU - Wiedemann, Leanne M.

AU - Sower, Stacia A.

AU - Decatur, Wayne A.

AU - Hall, Jeffrey A.

AU - Amemiya, Chris T.

AU - Saha, Nil R.

AU - Buckley, Katherine M.

AU - Rast, Jonathan P.

AU - Das, Sabyasachi

AU - Hirano, Masayuki

AU - McCurley, Nathanael

AU - Guo, Peng

AU - Rohner, Nicolas

AU - Tabin, Clifford J.

AU - Piccinelli, Paul

AU - Elgar, Greg

AU - Ruffier, Magali

AU - Aken, Bronwen L.

AU - Searle, Stephen M.J.

AU - Muffato, Matthieu

AU - Pignatelli, Miguel

AU - Herrero, Javier

AU - Jones, Matthew

AU - Brown, C. Titus

AU - Chung-Davidson, Yu Wen

AU - Nanlohy, Kaben G.

AU - Libants, Scot V.

AU - Yeh, Chu Yin

AU - McCauley, David W.

AU - Langeland, James A.

AU - Pancer, Zeev

AU - Fritzsch, Bernd

AU - De Jong, Pieter J.

AU - Zhu, Baoli

AU - Fulton, Lucinda L.

AU - Theising, Brenda

AU - Flicek, Paul

AU - Bronner, Marianne E.

AU - Warren, Wesley C.

AU - Clifton, Sandra W.

AU - Wilson, Richard K.

AU - Li, Weiming

N1 - Funding Information: We thank the Genome Institute, Washington University School of Medicine, Production Sequencing group for all sample procurement and genome sequencing work, the Michigan State University Genomic Core for transcriptome sequencing and the US Geological Survey, Lake Huron Biological Station for providing lamprey samples for sequencing. We thank F. Antonacci and E.E. Eichler (University of Washington) for performing FISH and providing access to computational facilities, respectively. We thank M. Robinson for bioinformatic analysis of immune system–related genes and conversion of GFF files for BAC end mapping. A portion of this research was conducted at the Marine Biological Laboratory (Woods Hole, Massachusetts). We acknowledge the support of the Stowers Institute for Medical Research (SIMR) and technical support from the SIMR Molecular Biology Core, particularly K. Staehling, A. Perera and K. Delventhal for BAC screening and sequencing. We acknowledge the Center for High-Performance Computing at the University of Utah for the allocation of computational resources toward gene annotation. We recognize all the important work that could not be cited owing to space limitations. The lamprey genome project was funded by the National Human Genome Research Institute (U54HG003079 (R.K.W.)). Additional support was provided by grants from the US National Institutes of Health (R24GM83982 (W.L.)) and the Great Lakes Fisheries commission (W.L.). Partial funding was provided by several additional sources, including grants from the US National Institutes of Health (F32GM087919 and T32HG00035 (J.J.S.); DE017911 (M.E.B.); R03NS078519 (O.E.B.); R01HG004694 (M.D.Y.); GM079492, GM090049 and RR014085 (C.T.A.); and R37HD032443 (C.J.T.)), the National Science Foundation (MCB-0719558 (C.T.A.); IOS-0849569 (S.A.S.); IBN-0208138 (L. Holland); and IOS-1126998 (M.D.Y.)), the New Hampshire Agricultural Experiment Station (Scientific Contribution Number 2471 (S.A.S.)), the Charles Evans Research Award (O.E.B., J.D.B. and J.R.M.), the Wellcome Trust (WT095908 (P.F.) and WT098051), the Canadian Institutes of Health Research (MOP74667 (J.P.R.)) and the Natural Sciences and Engineering Research Council of Canada (312221 (J.P.R.)).

PY - 2013/4

Y1 - 2013/4

N2 - Lampreys are representatives of an ancient vertebrate lineage that diverged from our own ∼500 million years ago. By virtue of this deeply shared ancestry, the sea lamprey (P. marinus) genome is uniquely poised to provide insight into the ancestry of vertebrate genomes and the underlying principles of vertebrate biology. Here, we present the first lamprey whole-genome sequence and assembly. We note challenges faced owing to its high content of repetitive elements and GC bases, as well as the absence of broad-scale sequence information from closely related species. Analyses of the assembly indicate that two whole-genome duplications likely occurred before the divergence of ancestral lamprey and gnathostome lineages. Moreover, the results help define key evolutionary events within vertebrate lineages, including the origin of myelin-associated proteins and the development of appendages. The lamprey genome provides an important resource for reconstructing vertebrate origins and the evolutionary events that have shaped the genomes of extant organisms.

AB - Lampreys are representatives of an ancient vertebrate lineage that diverged from our own ∼500 million years ago. By virtue of this deeply shared ancestry, the sea lamprey (P. marinus) genome is uniquely poised to provide insight into the ancestry of vertebrate genomes and the underlying principles of vertebrate biology. Here, we present the first lamprey whole-genome sequence and assembly. We note challenges faced owing to its high content of repetitive elements and GC bases, as well as the absence of broad-scale sequence information from closely related species. Analyses of the assembly indicate that two whole-genome duplications likely occurred before the divergence of ancestral lamprey and gnathostome lineages. Moreover, the results help define key evolutionary events within vertebrate lineages, including the origin of myelin-associated proteins and the development of appendages. The lamprey genome provides an important resource for reconstructing vertebrate origins and the evolutionary events that have shaped the genomes of extant organisms.

UR - http://www.scopus.com/inward/record.url?scp=84875692135&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84875692135&partnerID=8YFLogxK

U2 - 10.1038/ng.2568

DO - 10.1038/ng.2568

M3 - Article

C2 - 23435085

AN - SCOPUS:84875692135

SN - 1061-4036

VL - 45

SP - 415

EP - 421

JO - Nature Genetics

JF - Nature Genetics

IS - 4

ER -

Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution

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