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Genomic insights of body plan transitions from bilateral to pentameral symmetry in Echinoderms

Li, Yongxin and Omori, Akihito and Flores, Rachel L. and Satterfield, Sheri and Nguyen, Christine and Ota, Tatsuya and Tsurugaya, Toko and Ikuta, Tetsuro and Ikeo, Kazuho and Kikuchi, Mani and Leong, Jason C. K. and Reich, Adrian and Hao, Meng and Wan, Wenting and Dong, Yang and Ren, Yaondong and Zhang, Si and Zeng, Tao and Uesaka, Masahiro and Uchida, Yui and Li, Xueyan and Shibata, Tomoko F. and Bino, Takahiro and Ogawa, Kota and Shigenobu, Shuji and Kondo, Mariko and Wang, Fayou and Chen, Luonan and Wessel, Gary and Saiga, Hidetoshi and Cameron, R. Andrew and Livingston, Brian and Bradham, Cynthia and Wang, Wen and Irie, Naoki (2020) Genomic insights of body plan transitions from bilateral to pentameral symmetry in Echinoderms. Communications Biology, 3 . Art. No. 371. ISSN 2399-3642. PMCID PMC7351957. https://resolver.caltech.edu/CaltechAUTHORS:20200720-120711537

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Abstract

Echinoderms are an exceptional group of bilaterians that develop pentameral adult symmetry from a bilaterally symmetric larva. However, the genetic basis in evolution and development of this unique transformation remains to be clarified. Here we report newly sequenced genomes, developmental transcriptomes, and proteomes of diverse echinoderms including the green sea urchin (L. variegatus), a sea cucumber (A. japonicus), and with particular emphasis on a sister group of the earliest-diverged echinoderms, the feather star (A. japonica). We learned that the last common ancestor of echinoderms retained a well-organized Hox cluster reminiscent of the hemichordate, and had gene sets involved in endoskeleton development. Further, unlike in other animal groups, the most conserved developmental stages were not at the body plan establishing phase, and genes normally involved in bilaterality appear to function in pentameric axis development. These results enhance our understanding of the divergence of protostomes and deuterostomes almost 500 Mya.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s42003-020-1091-1DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7351957PubMed CentralArticle
https://doi.org/10.5061/dryad.rbnzs7h7nRelated ItemDRYAD database
ORCID:
AuthorORCID
Omori, Akihito0000-0003-0571-6553
Ota, Tatsuya0000-0002-1115-5169
Reich, Adrian0000-0002-1680-8659
Dong, Yang0000-0001-6212-3055
Zeng, Tao0000-0002-0295-3994
Li, Xueyan0000-0003-0457-7846
Shigenobu, Shuji0000-0003-4640-2323
Kondo, Mariko0000-0002-8072-2729
Chen, Luonan0000-0002-3960-0068
Cameron, R. Andrew0000-0003-3947-6041
Wang, Wen0000-0002-7801-2066
Irie, Naoki0000-0002-6720-381X
Additional Information:© The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 18 October 2019; Accepted 19 June 2020; Published 10 July 2020. This work was supported by the National Natural Science Foundation of China (No. 31561143016; No. 31621062 and Strategic International Collaborative Research Program (SICORP) of JST. We thank Flore Castellan for help drawing animals and embryos. GMW gratefully acknowledges support in part from NIH 9RO1GM125071. Data availability: Genomic sequence data and assembled genomes for the following species are available through the NCBI database at the indicated BioProject accession IDs: Brittle star genome (PRJNA182997), feather star genome (PRJNA553656), and green sea urchin genome (PRJNA553643). RNAseq data are available for the following species at the indicated BioProject accession IDs: green sea urchin RNAseq data (PRJNA554218), feather star RNAseq data (PRJNA553591), and Japanese sea cucumber RNAseq data (PRJNA553613). Cloned sequences of Hox genes of the feather star (hox1 LC462021, hox2 LC462022, hox4 LC462023, hox5 LC462024, hox7 LC462025, hox8 LC462026, hox9/10 LC462027, hox11/13a LC462028, hox11/13c LC462029) are also available through the NCBI database at the indicated nucleotide accession IDs. Assembled genomes and gene sets can also be accessed through the DRYAD database60 at https://doi.org/10.5061/dryad.rbnzs7h7n. Proteomic data are available via the ProteomeXchange with identifier PXD019526. Source data for Figs. 2a and 3b can be found in Supplementary Data 1 and Supplementary Data 2. Code availability: No custom or proprietary software was used in the analysis. Versions and parameters for each software package used are described in the reporting summary and elsewhere in the “Methods.” Author Contributions: The study was conceived by N.I., W.Wang, M.Kondo, Y.L., B.L., and C.B. The echinoderm DNA and RNA samples were collected and sequenced by A.C., A.O., A.R., C.B., K.O., M.Kikuchi, M.Kondo, M.U., N.I., R.F., T.B., Y.U., W.Wan, and W.Wang. Genomes were assembled and annotated by G.W., Y.L., M.H., W.Wang, X.L., and Y.R. Bioinformatics analyses were performed by C.B., C.N., F.W., G.W., J.L., S.Satterfield, L.C., N.I., R.F., S.Shigenobu, S.Z., T.Z., Y.D., and Y.L. Hox cluster analysis were performed by H.S., K.I., T.O., T.S., T.T., T.I., and M.Kondo. Proteome analyses were done by B.L., C.N., R.F., and S.Satterfield. WISH analyses were performed by A.O., M.Kondo., and M.Kikuchi. The manuscript was written by A.C., A.O., B.L., C.B., G.W., H.S., N.I., T.O., T.I., W.Wang, and Y.L. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
National Natural Science Foundation of China31561143016
National Natural Science Foundation of China31621062
Japan Science and Technology Agency (JST)UNSPECIFIED
NIH9RO1GM125071
Subject Keywords:Evolutionary developmental biology; Evolutionary genetics
PubMed Central ID:PMC7351957
Record Number:CaltechAUTHORS:20200720-120711537
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200720-120711537
Official Citation:Li, Y., Omori, A., Flores, R.L. et al. Genomic insights of body plan transitions from bilateral to pentameral symmetry in Echinoderms. Commun Biol 3, 371 (2020). https://doi.org/10.1038/s42003-020-1091-1
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:104447
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:20 Jul 2020 21:07
Last Modified:20 Jul 2020 21:07

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