Analysis of the P. lividus sea urchin genome highlights contrasting trends of genomic and regulatory evolution in deuterostomes

Ferdinand Marlétaz; Arnaud Couloux; Julie Poulain; Karine Labadie; Corinne Da Silva; Sophie Mangenot; Benjamin Noel; Albert J. Poustka; Philippe Dru; Cinta Pegueroles; Marco Borra; Elijah K. Lowe; Guy Lhomond; Lydia Besnardeau; Stéphanie Le Gras; Tao Ye; Daria Gavriouchkina; Roberta Russo; Caterina Costa; Francesca Zito; Letizia Anello; Aldo Nicosia; Maria Antonietta Ragusa; Marta Pascual; M. Dolores Molina; Aline Chessel; Marta Di Carlo; Xavier Turon; Richard R. Copley; Jean Yves Exposito; Pedro Martinez; Vincenzo Cavalieri; Smadar Ben Tabou de Leon; Jenifer Croce; Paola Oliveri; Valeria Matranga; Maria Di Bernardo; Julia Morales; Patrick Cormier; Anne Marie Geneviève; Jean Marc Aury; Valérie Barbe; Patrick Wincker; Maria Ina Arnone; Christian Gache; Thierry Lepage

doi:10.1016/j.xgen.2023.100295

Analysis of the P. lividus sea urchin genome highlights contrasting trends of genomic and regulatory evolution in deuterostomes

Ferdinand Marlétaz, Arnaud Couloux, Julie Poulain, Karine Labadie, Corinne Da Silva, Sophie Mangenot, Benjamin Noel, Albert J. Poustka, Philippe Dru, Cinta Pegueroles, Marco Borra, Elijah K. Lowe, Guy Lhomond, Lydia Besnardeau, Stéphanie Le Gras, Tao Ye, Daria Gavriouchkina, Roberta Russo, Caterina Costa, Francesca ZitoLetizia Anello, Aldo Nicosia, Maria Antonietta Ragusa, Marta Pascual, M. Dolores Molina, Aline Chessel, Marta Di Carlo, Xavier Turon, Richard R. Copley, Jean Yves Exposito, Pedro Martinez, Vincenzo Cavalieri, Smadar Ben Tabou de Leon, Jenifer Croce, Paola Oliveri, Valeria Matranga, Maria Di Bernardo, Julia Morales, Patrick Cormier, Anne Marie Geneviève, Jean Marc Aury, Valérie Barbe, Patrick Wincker, Maria Ina Arnone, Christian Gache, Thierry Lepage

Department of Marine Biology

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

Abstract

Sea urchins are emblematic models in developmental biology and display several characteristics that set them apart from other deuterostomes. To uncover the genomic cues that may underlie these specificities, we generated a chromosome-scale genome assembly for the sea urchin Paracentrotus lividus and an extensive gene expression and epigenetic profiles of its embryonic development. We found that, unlike vertebrates, sea urchins retained ancestral chromosomal linkages but underwent very fast intrachromosomal gene order mixing. We identified a burst of gene duplication in the echinoid lineage and showed that some of these expanded genes have been recruited in novel structures (water vascular system, Aristotle's lantern, and skeletogenic micromere lineage). Finally, we identified gene-regulatory modules conserved between sea urchins and chordates. Our results suggest that gene-regulatory networks controlling development can be conserved despite extensive gene order rearrangement.

Original language	English
Article number	100295
Journal	Cell Genomics
Volume	3
Issue number	4
DOIs	https://doi.org/10.1016/j.xgen.2023.100295
State	Published - 12 Apr 2023

Bibliographical note

Funding Information:
F.M. is supported by a Royal Society University research fellowship (URF\R1\191161) and a BBSRC research grant (BB/V01109X/). The authors acknowledge support from the Marine Genomics Network of Excellence (MGE), the European Marine Biological Resource Centre (EMBRC), and the Coordinated Research Infrastructures Building Enduring Life-science (CORBEL). Proximity ligation Chicago and HiC were supported by Dovetail Genomics (Cantata Bio). Pacbio sequencing was funded by a grant from the Agence Nationale de la Recherche (ANR) to T.L. (project ANR-14-CE11-0006-01) and by a grant from CORBEL to M.I.A. E.K.L. was supported by a fellowship from EMBRC. We thank Hiroshi Wada and Atsuko Yamazaki for providing the pmar sequences of Eucidaris tribuloides. C.P. and X.T. are funded by the grant PID2020-118550RB (MarGeCh), funded by MCIN/AEI/10.13039/501100011033 (Spanish Government). We thank Alexandre de Mendoza for insightful comments. We also thank Carla Falugi, Sonia Manzo, and Maeve S. Kelly for support in the early phases of the project. C.G. initiated the project. M.I.A. prepared the genomic DNA. A.C. J.M.A. V.B. and P.W. supervised the acquisition of genomic data. T.L. A.J.P. M.B. C.D.S. M.I.A. and P.D. generated and processed genomic and transcriptome resources. G.L. L.B. M.I.A. A.-M.G. S.M. and T.L. processed and sequenced BAC clones. J.P. K.L. C.D.S. S.M. B.N. A.C. J.M.A. and V.B. generated sequencing libraries and processed the sequencing data. F.M. A.C. and J.M.A. assembled the genome. P.C. J.M. M.I.A. S.B.T.d.L. P.O. and T.L. collected samples for transcriptome analysis. P.D. E.K.L. F.M. and C.D.S. assembled the transcriptomes. C.P. M.P. and X.T. identified lncRNAs from transcriptomes. R.R. C.C. F.Z. A.N. M.A.R. C.F. S.M. M.D.C. R.R.C. J.Y.E. P.M. V.C. J.C. and M.D.B. contributed to the analyses of the genome sequence and to preparation of experimental materials. A.C. M.D.M. and T.L. identified, cloned, and performed the functional analysis of the pop genes. F.M. did the phylogenetic analysis of the pop genes. T.L. prepared and quality-checked the ATAC-seq and Cut&Tag libraries. S.L.G. T.Y. F.M. and D.G. processed and analyzed the ATAC-seq and Cut&Tag data. F.M. generated a chromosome scale assembly and performed integrative bioinformatics analyses. C.G. and T.L. supervised and coordinated the project. F.M. and T.L. wrote the paper. All authors commented and approved the manuscript. The authors declare no competing interests.

Funding Information:
F.M. is supported by a Royal Society University research fellowship ( URF\R1\191161 ) and a BBSRC research grant ( BB/V01109X/ ). The authors acknowledge support from the Marine Genomics Network of Excellence (MGE), the European Marine Biological Resource Centre (EMBRC), and the Coordinated Research Infrastructures Building Enduring Life-science ( CORBEL ). Proximity ligation Chicago and HiC were supported by Dovetail Genomics (Cantata Bio). Pacbio sequencing was funded by a grant from the Agence Nationale de la Recherche (ANR) to T.L. (project ANR-14-CE11-0006-01 ) and by a grant from CORBEL to M.I.A. E.K.L. was supported by a fellowship from EMBRC . We thank Hiroshi Wada and Atsuko Yamazaki for providing the pmar sequences of Eucidaris tribuloides. C.P. and X.T. are funded by the grant PID2020-118550RB (MarGeCh), funded by MCIN/AEI/10.13039/501100011033 (Spanish Government). We thank Alexandre de Mendoza for insightful comments. We also thank Carla Falugi, Sonia Manzo, and Maeve S. Kelly for support in the early phases of the project.

Publisher Copyright:
© 2023 The Author(s)

ASJC Scopus subject areas

Genetics
Biochemistry, Genetics and Molecular Biology (miscellaneous)

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10.1016/j.xgen.2023.100295

Cite this

Marlétaz, F., Couloux, A., Poulain, J., Labadie, K., Da Silva, C., Mangenot, S., Noel, B., Poustka, A. J., Dru, P., Pegueroles, C., Borra, M., Lowe, E. K., Lhomond, G., Besnardeau, L., Le Gras, S., Ye, T., Gavriouchkina, D., Russo, R., Costa, C., ... Lepage, T. (2023). Analysis of the P. lividus sea urchin genome highlights contrasting trends of genomic and regulatory evolution in deuterostomes. Cell Genomics, 3(4), [100295]. https://doi.org/10.1016/j.xgen.2023.100295

@article{584fad338f1b4cce830a57d2450c615f,

title = "Analysis of the P. lividus sea urchin genome highlights contrasting trends of genomic and regulatory evolution in deuterostomes",

abstract = "Sea urchins are emblematic models in developmental biology and display several characteristics that set them apart from other deuterostomes. To uncover the genomic cues that may underlie these specificities, we generated a chromosome-scale genome assembly for the sea urchin Paracentrotus lividus and an extensive gene expression and epigenetic profiles of its embryonic development. We found that, unlike vertebrates, sea urchins retained ancestral chromosomal linkages but underwent very fast intrachromosomal gene order mixing. We identified a burst of gene duplication in the echinoid lineage and showed that some of these expanded genes have been recruited in novel structures (water vascular system, Aristotle's lantern, and skeletogenic micromere lineage). Finally, we identified gene-regulatory modules conserved between sea urchins and chordates. Our results suggest that gene-regulatory networks controlling development can be conserved despite extensive gene order rearrangement.",

author = "Ferdinand Marl{\'e}taz and Arnaud Couloux and Julie Poulain and Karine Labadie and {Da Silva}, Corinne and Sophie Mangenot and Benjamin Noel and Poustka, {Albert J.} and Philippe Dru and Cinta Pegueroles and Marco Borra and Lowe, {Elijah K.} and Guy Lhomond and Lydia Besnardeau and {Le Gras}, St{\'e}phanie and Tao Ye and Daria Gavriouchkina and Roberta Russo and Caterina Costa and Francesca Zito and Letizia Anello and Aldo Nicosia and Ragusa, {Maria Antonietta} and Marta Pascual and Molina, {M. Dolores} and Aline Chessel and {Di Carlo}, Marta and Xavier Turon and Copley, {Richard R.} and Exposito, {Jean Yves} and Pedro Martinez and Vincenzo Cavalieri and {Ben Tabou de Leon}, Smadar and Jenifer Croce and Paola Oliveri and Valeria Matranga and {Di Bernardo}, Maria and Julia Morales and Patrick Cormier and Genevi{\`e}ve, {Anne Marie} and Aury, {Jean Marc} and Val{\'e}rie Barbe and Patrick Wincker and Arnone, {Maria Ina} and Christian Gache and Thierry Lepage",

note = "Funding Information: F.M. is supported by a Royal Society University research fellowship (URF\R1\191161) and a BBSRC research grant (BB/V01109X/). The authors acknowledge support from the Marine Genomics Network of Excellence (MGE), the European Marine Biological Resource Centre (EMBRC), and the Coordinated Research Infrastructures Building Enduring Life-science (CORBEL). Proximity ligation Chicago and HiC were supported by Dovetail Genomics (Cantata Bio). Pacbio sequencing was funded by a grant from the Agence Nationale de la Recherche (ANR) to T.L. (project ANR-14-CE11-0006-01) and by a grant from CORBEL to M.I.A. E.K.L. was supported by a fellowship from EMBRC. We thank Hiroshi Wada and Atsuko Yamazaki for providing the pmar sequences of Eucidaris tribuloides. C.P. and X.T. are funded by the grant PID2020-118550RB (MarGeCh), funded by MCIN/AEI/10.13039/501100011033 (Spanish Government). We thank Alexandre de Mendoza for insightful comments. We also thank Carla Falugi, Sonia Manzo, and Maeve S. Kelly for support in the early phases of the project. C.G. initiated the project. M.I.A. prepared the genomic DNA. A.C. J.M.A. V.B. and P.W. supervised the acquisition of genomic data. T.L. A.J.P. M.B. C.D.S. M.I.A. and P.D. generated and processed genomic and transcriptome resources. G.L. L.B. M.I.A. A.-M.G. S.M. and T.L. processed and sequenced BAC clones. J.P. K.L. C.D.S. S.M. B.N. A.C. J.M.A. and V.B. generated sequencing libraries and processed the sequencing data. F.M. A.C. and J.M.A. assembled the genome. P.C. J.M. M.I.A. S.B.T.d.L. P.O. and T.L. collected samples for transcriptome analysis. P.D. E.K.L. F.M. and C.D.S. assembled the transcriptomes. C.P. M.P. and X.T. identified lncRNAs from transcriptomes. R.R. C.C. F.Z. A.N. M.A.R. C.F. S.M. M.D.C. R.R.C. J.Y.E. P.M. V.C. J.C. and M.D.B. contributed to the analyses of the genome sequence and to preparation of experimental materials. A.C. M.D.M. and T.L. identified, cloned, and performed the functional analysis of the pop genes. F.M. did the phylogenetic analysis of the pop genes. T.L. prepared and quality-checked the ATAC-seq and Cut&Tag libraries. S.L.G. T.Y. F.M. and D.G. processed and analyzed the ATAC-seq and Cut&Tag data. F.M. generated a chromosome scale assembly and performed integrative bioinformatics analyses. C.G. and T.L. supervised and coordinated the project. F.M. and T.L. wrote the paper. All authors commented and approved the manuscript. The authors declare no competing interests. Funding Information: F.M. is supported by a Royal Society University research fellowship ( URF\R1\191161 ) and a BBSRC research grant ( BB/V01109X/ ). The authors acknowledge support from the Marine Genomics Network of Excellence (MGE), the European Marine Biological Resource Centre (EMBRC), and the Coordinated Research Infrastructures Building Enduring Life-science ( CORBEL ). Proximity ligation Chicago and HiC were supported by Dovetail Genomics (Cantata Bio). Pacbio sequencing was funded by a grant from the Agence Nationale de la Recherche (ANR) to T.L. (project ANR-14-CE11-0006-01 ) and by a grant from CORBEL to M.I.A. E.K.L. was supported by a fellowship from EMBRC . We thank Hiroshi Wada and Atsuko Yamazaki for providing the pmar sequences of Eucidaris tribuloides. C.P. and X.T. are funded by the grant PID2020-118550RB (MarGeCh), funded by MCIN/AEI/10.13039/501100011033 (Spanish Government). We thank Alexandre de Mendoza for insightful comments. We also thank Carla Falugi, Sonia Manzo, and Maeve S. Kelly for support in the early phases of the project. Publisher Copyright: {\textcopyright} 2023 The Author(s)",

year = "2023",

month = apr,

day = "12",

doi = "10.1016/j.xgen.2023.100295",

language = "English",

volume = "3",

journal = "Cell Genomics",

issn = "2666-979X",

publisher = "Cell Press",

number = "4",

}

Marlétaz, F, Couloux, A, Poulain, J, Labadie, K, Da Silva, C, Mangenot, S, Noel, B, Poustka, AJ, Dru, P, Pegueroles, C, Borra, M, Lowe, EK, Lhomond, G, Besnardeau, L, Le Gras, S, Ye, T, Gavriouchkina, D, Russo, R, Costa, C, Zito, F, Anello, L, Nicosia, A, Ragusa, MA, Pascual, M, Molina, MD, Chessel, A, Di Carlo, M, Turon, X, Copley, RR, Exposito, JY, Martinez, P, Cavalieri, V, Ben Tabou de Leon, S, Croce, J, Oliveri, P, Matranga, V, Di Bernardo, M, Morales, J, Cormier, P, Geneviève, AM, Aury, JM, Barbe, V, Wincker, P, Arnone, MI, Gache, C & Lepage, T 2023, 'Analysis of the P. lividus sea urchin genome highlights contrasting trends of genomic and regulatory evolution in deuterostomes', Cell Genomics, vol. 3, no. 4, 100295. https://doi.org/10.1016/j.xgen.2023.100295

TY - JOUR

T1 - Analysis of the P. lividus sea urchin genome highlights contrasting trends of genomic and regulatory evolution in deuterostomes

AU - Marlétaz, Ferdinand

AU - Couloux, Arnaud

AU - Poulain, Julie

AU - Labadie, Karine

AU - Da Silva, Corinne

AU - Mangenot, Sophie

AU - Noel, Benjamin

AU - Poustka, Albert J.

AU - Dru, Philippe

AU - Pegueroles, Cinta

AU - Borra, Marco

AU - Lowe, Elijah K.

AU - Lhomond, Guy

AU - Besnardeau, Lydia

AU - Le Gras, Stéphanie

AU - Ye, Tao

AU - Gavriouchkina, Daria

AU - Russo, Roberta

AU - Costa, Caterina

AU - Zito, Francesca

AU - Anello, Letizia

AU - Nicosia, Aldo

AU - Ragusa, Maria Antonietta

AU - Pascual, Marta

AU - Molina, M. Dolores

AU - Chessel, Aline

AU - Di Carlo, Marta

AU - Turon, Xavier

AU - Copley, Richard R.

AU - Exposito, Jean Yves

AU - Martinez, Pedro

AU - Cavalieri, Vincenzo

AU - Ben Tabou de Leon, Smadar

AU - Croce, Jenifer

AU - Oliveri, Paola

AU - Matranga, Valeria

AU - Di Bernardo, Maria

AU - Morales, Julia

AU - Cormier, Patrick

AU - Geneviève, Anne Marie

AU - Aury, Jean Marc

AU - Barbe, Valérie

AU - Wincker, Patrick

AU - Arnone, Maria Ina

AU - Gache, Christian

AU - Lepage, Thierry

N1 - Funding Information: F.M. is supported by a Royal Society University research fellowship (URF\R1\191161) and a BBSRC research grant (BB/V01109X/). The authors acknowledge support from the Marine Genomics Network of Excellence (MGE), the European Marine Biological Resource Centre (EMBRC), and the Coordinated Research Infrastructures Building Enduring Life-science (CORBEL). Proximity ligation Chicago and HiC were supported by Dovetail Genomics (Cantata Bio). Pacbio sequencing was funded by a grant from the Agence Nationale de la Recherche (ANR) to T.L. (project ANR-14-CE11-0006-01) and by a grant from CORBEL to M.I.A. E.K.L. was supported by a fellowship from EMBRC. We thank Hiroshi Wada and Atsuko Yamazaki for providing the pmar sequences of Eucidaris tribuloides. C.P. and X.T. are funded by the grant PID2020-118550RB (MarGeCh), funded by MCIN/AEI/10.13039/501100011033 (Spanish Government). We thank Alexandre de Mendoza for insightful comments. We also thank Carla Falugi, Sonia Manzo, and Maeve S. Kelly for support in the early phases of the project. C.G. initiated the project. M.I.A. prepared the genomic DNA. A.C. J.M.A. V.B. and P.W. supervised the acquisition of genomic data. T.L. A.J.P. M.B. C.D.S. M.I.A. and P.D. generated and processed genomic and transcriptome resources. G.L. L.B. M.I.A. A.-M.G. S.M. and T.L. processed and sequenced BAC clones. J.P. K.L. C.D.S. S.M. B.N. A.C. J.M.A. and V.B. generated sequencing libraries and processed the sequencing data. F.M. A.C. and J.M.A. assembled the genome. P.C. J.M. M.I.A. S.B.T.d.L. P.O. and T.L. collected samples for transcriptome analysis. P.D. E.K.L. F.M. and C.D.S. assembled the transcriptomes. C.P. M.P. and X.T. identified lncRNAs from transcriptomes. R.R. C.C. F.Z. A.N. M.A.R. C.F. S.M. M.D.C. R.R.C. J.Y.E. P.M. V.C. J.C. and M.D.B. contributed to the analyses of the genome sequence and to preparation of experimental materials. A.C. M.D.M. and T.L. identified, cloned, and performed the functional analysis of the pop genes. F.M. did the phylogenetic analysis of the pop genes. T.L. prepared and quality-checked the ATAC-seq and Cut&Tag libraries. S.L.G. T.Y. F.M. and D.G. processed and analyzed the ATAC-seq and Cut&Tag data. F.M. generated a chromosome scale assembly and performed integrative bioinformatics analyses. C.G. and T.L. supervised and coordinated the project. F.M. and T.L. wrote the paper. All authors commented and approved the manuscript. The authors declare no competing interests. Funding Information: F.M. is supported by a Royal Society University research fellowship ( URF\R1\191161 ) and a BBSRC research grant ( BB/V01109X/ ). The authors acknowledge support from the Marine Genomics Network of Excellence (MGE), the European Marine Biological Resource Centre (EMBRC), and the Coordinated Research Infrastructures Building Enduring Life-science ( CORBEL ). Proximity ligation Chicago and HiC were supported by Dovetail Genomics (Cantata Bio). Pacbio sequencing was funded by a grant from the Agence Nationale de la Recherche (ANR) to T.L. (project ANR-14-CE11-0006-01 ) and by a grant from CORBEL to M.I.A. E.K.L. was supported by a fellowship from EMBRC . We thank Hiroshi Wada and Atsuko Yamazaki for providing the pmar sequences of Eucidaris tribuloides. C.P. and X.T. are funded by the grant PID2020-118550RB (MarGeCh), funded by MCIN/AEI/10.13039/501100011033 (Spanish Government). We thank Alexandre de Mendoza for insightful comments. We also thank Carla Falugi, Sonia Manzo, and Maeve S. Kelly for support in the early phases of the project. Publisher Copyright: © 2023 The Author(s)

PY - 2023/4/12

Y1 - 2023/4/12

N2 - Sea urchins are emblematic models in developmental biology and display several characteristics that set them apart from other deuterostomes. To uncover the genomic cues that may underlie these specificities, we generated a chromosome-scale genome assembly for the sea urchin Paracentrotus lividus and an extensive gene expression and epigenetic profiles of its embryonic development. We found that, unlike vertebrates, sea urchins retained ancestral chromosomal linkages but underwent very fast intrachromosomal gene order mixing. We identified a burst of gene duplication in the echinoid lineage and showed that some of these expanded genes have been recruited in novel structures (water vascular system, Aristotle's lantern, and skeletogenic micromere lineage). Finally, we identified gene-regulatory modules conserved between sea urchins and chordates. Our results suggest that gene-regulatory networks controlling development can be conserved despite extensive gene order rearrangement.

AB - Sea urchins are emblematic models in developmental biology and display several characteristics that set them apart from other deuterostomes. To uncover the genomic cues that may underlie these specificities, we generated a chromosome-scale genome assembly for the sea urchin Paracentrotus lividus and an extensive gene expression and epigenetic profiles of its embryonic development. We found that, unlike vertebrates, sea urchins retained ancestral chromosomal linkages but underwent very fast intrachromosomal gene order mixing. We identified a burst of gene duplication in the echinoid lineage and showed that some of these expanded genes have been recruited in novel structures (water vascular system, Aristotle's lantern, and skeletogenic micromere lineage). Finally, we identified gene-regulatory modules conserved between sea urchins and chordates. Our results suggest that gene-regulatory networks controlling development can be conserved despite extensive gene order rearrangement.

UR - http://www.scopus.com/inward/record.url?scp=85152694377&partnerID=8YFLogxK

U2 - 10.1016/j.xgen.2023.100295

DO - 10.1016/j.xgen.2023.100295

M3 - Article

AN - SCOPUS:85152694377

SN - 2666-979X

VL - 3

JO - Cell Genomics

JF - Cell Genomics

IS - 4

M1 - 100295

ER -

Analysis of the P. lividus sea urchin genome highlights contrasting trends of genomic and regulatory evolution in deuterostomes

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