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

Research output: Contribution to journalArticlepeer-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 languageEnglish
Article number100295
JournalCell Genomics
Volume3
Issue number4
DOIs
StatePublished - 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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