Analysis of the Sea Urchin Genome Highlights Contrasting Trends of Genomic and Regulatory Evolution in Deuterostomes

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 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.

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References

Madgwick A, Magri M, Dantec C, Gailly D, Fiuza U, Guignard L . Evolution of embryonic cis-regulatory landscapes between divergent Phallusia and Ciona ascidians. Dev Biol. 2019; 448(2):71-87. DOI: 10.1016/j.ydbio.2019.01.003. View

Baughman K, McDougall C, Cummins S, Hall M, Degnan B, Satoh N . Genomic organization of Hox and ParaHox clusters in the echinoderm, Acanthaster planci. Genesis. 2014; 52(12):952-8. DOI: 10.1002/dvg.22840. View

Wu J, Huang B, Chen H, Yin Q, Liu Y, Xiang Y . The landscape of accessible chromatin in mammalian preimplantation embryos. Nature. 2016; 534(7609):652-7. DOI: 10.1038/nature18606. View

Kouzarides T . Chromatin modifications and their function. Cell. 2007; 128(4):693-705. DOI: 10.1016/j.cell.2007.02.005. View

Liu Y, Schmidt B, Maskell D . MSAProbs: multiple sequence alignment based on pair hidden Markov models and partition function posterior probabilities. Bioinformatics. 2010; 26(16):1958-64. DOI: 10.1093/bioinformatics/btq338. View

Gildor T, Ben-Tabou de-Leon S . Comparative Study of Regulatory Circuits in Two Sea Urchin Species Reveals Tight Control of Timing and High Conservation of Expression Dynamics. PLoS Genet. 2015; 11(7):e1005435. PMC: 4521883. DOI: 10.1371/journal.pgen.1005435. View

Pongor L, Gross J, Vera Alvarez R, Murai J, Jang S, Zhang H . BAMscale: quantification of next-generation sequencing peaks and generation of scaled coverage tracks. Epigenetics Chromatin. 2020; 13(1):21. PMC: 7175505. DOI: 10.1186/s13072-020-00343-x. View

Putnam N, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A . Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science. 2007; 317(5834):86-94. DOI: 10.1126/science.1139158. View

Huang S, Kang M, Xu A . HaploMerger2: rebuilding both haploid sub-assemblies from high-heterozygosity diploid genome assembly. Bioinformatics. 2017; 33(16):2577-2579. PMC: 5870766. DOI: 10.1093/bioinformatics/btx220. View

10.

Stanke M, Keller O, Gunduz I, Hayes A, Waack S, Morgenstern B . AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 2006; 34(Web Server issue):W435-9. PMC: 1538822. DOI: 10.1093/nar/gkl200. View

11.

Nord A, Blow M, Attanasio C, Akiyama J, Holt A, Hosseini R . Rapid and pervasive changes in genome-wide enhancer usage during mammalian development. Cell. 2013; 155(7):1521-31. PMC: 3989111. DOI: 10.1016/j.cell.2013.11.033. View

12.

Yamazaki A, Morino Y, Urata M, Yamaguchi M, Minokawa T, Furukawa R . / homeobox genes and the evolution of the double-negative gate for endomesoderm specification in echinoderms. Development. 2020; 147(4). DOI: 10.1242/dev.182139. View

13.

Wood N, Mattiello T, Rowe M, Ward L, Perillo M, Arnone M . Neuropeptidergic Systems in Pluteus Larvae of the Sea Urchin : Neurochemical Complexity in a "Simple" Nervous System. Front Endocrinol (Lausanne). 2018; 9:628. PMC: 6209648. DOI: 10.3389/fendo.2018.00628. View

14.

Barsi J, Tu Q, Calestani C, Davidson E . Genome-wide assessment of differential effector gene use in embryogenesis. Development. 2015; 142(22):3892-901. PMC: 4712884. DOI: 10.1242/dev.127746. View

15.

Revilla-I-Domingo R, Oliveri P, Davidson E . A missing link in the sea urchin embryo gene regulatory network: hesC and the double-negative specification of micromeres. Proc Natl Acad Sci U S A. 2007; 104(30):12383-8. PMC: 1941478. DOI: 10.1073/pnas.0705324104. View

16.

Simakov O, Kawashima T, Marletaz F, Jenkins J, Koyanagi R, Mitros T . Hemichordate genomes and deuterostome origins. Nature. 2015; 527(7579):459-65. PMC: 4729200. DOI: 10.1038/nature16150. View

17.

McClay D . Evolutionary crossroads in developmental biology: sea urchins. Development. 2011; 138(13):2639-48. PMC: 3109595. DOI: 10.1242/dev.048967. View

18.

Martinez P, RAST J, Davidson E . Organization of an echinoderm Hox gene cluster. Proc Natl Acad Sci U S A. 1999; 96(4):1469-74. PMC: 15486. DOI: 10.1073/pnas.96.4.1469. View

19.

Gerstein M, Rozowsky J, Yan K, Wang D, Cheng C, Brown J . Comparative analysis of the transcriptome across distant species. Nature. 2014; 512(7515):445-8. PMC: 4155737. DOI: 10.1038/nature13424. View

20.

Ramirez F, Ryan D, Gruning B, Bhardwaj V, Kilpert F, Richter A . deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 2016; 44(W1):W160-5. PMC: 4987876. DOI: 10.1093/nar/gkw257. View