The sea cucumber genome provides insights into morphological evolution and visceral regeneration.

Apart from sharing common ancestry with chordates, sea cucumbers exhibit a unique morphology and exceptional regenerative capacity. Here we present the complete genome sequence of an economically important sea cucumber, A. japonicus, generated using Illumina and PacBio platforms, to achieve an assem...

Full description

Bibliographic Details
Main Authors: Xiaojun Zhang, Lina Sun, Jianbo Yuan, Yamin Sun, Yi Gao, Libin Zhang, Shihao Li, Hui Dai, Jean-François Hamel, Chengzhang Liu, Yang Yu, Shilin Liu, Wenchao Lin, Kaimin Guo, Songjun Jin, Peng Xu, Kenneth B Storey, Pin Huan, Tao Zhang, Yi Zhou, Jiquan Zhang, Chenggang Lin, Xiaoni Li, Lili Xing, Da Huo, Mingzhe Sun, Lei Wang, Annie Mercier, Fuhua Li, Hongsheng Yang, Jianhai Xiang
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-10-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.2003790
_version_ 1819124387589128192
author Xiaojun Zhang
Lina Sun
Jianbo Yuan
Yamin Sun
Yi Gao
Libin Zhang
Shihao Li
Hui Dai
Jean-François Hamel
Chengzhang Liu
Yang Yu
Shilin Liu
Wenchao Lin
Kaimin Guo
Songjun Jin
Peng Xu
Kenneth B Storey
Pin Huan
Tao Zhang
Yi Zhou
Jiquan Zhang
Chenggang Lin
Xiaoni Li
Lili Xing
Da Huo
Mingzhe Sun
Lei Wang
Annie Mercier
Fuhua Li
Hongsheng Yang
Jianhai Xiang
author_facet Xiaojun Zhang
Lina Sun
Jianbo Yuan
Yamin Sun
Yi Gao
Libin Zhang
Shihao Li
Hui Dai
Jean-François Hamel
Chengzhang Liu
Yang Yu
Shilin Liu
Wenchao Lin
Kaimin Guo
Songjun Jin
Peng Xu
Kenneth B Storey
Pin Huan
Tao Zhang
Yi Zhou
Jiquan Zhang
Chenggang Lin
Xiaoni Li
Lili Xing
Da Huo
Mingzhe Sun
Lei Wang
Annie Mercier
Fuhua Li
Hongsheng Yang
Jianhai Xiang
author_sort Xiaojun Zhang
collection DOAJ
description Apart from sharing common ancestry with chordates, sea cucumbers exhibit a unique morphology and exceptional regenerative capacity. Here we present the complete genome sequence of an economically important sea cucumber, A. japonicus, generated using Illumina and PacBio platforms, to achieve an assembly of approximately 805 Mb (contig N50 of 190 Kb and scaffold N50 of 486 Kb), with 30,350 protein-coding genes and high continuity. We used this resource to explore key genetic mechanisms behind the unique biological characters of sea cucumbers. Phylogenetic and comparative genomic analyses revealed the presence of marker genes associated with notochord and gill slits, suggesting that these chordate features were present in ancestral echinoderms. The unique shape and weak mineralization of the sea cucumber adult body were also preliminarily explained by the contraction of biomineralization genes. Genome, transcriptome, and proteome analyses of organ regrowth after induced evisceration provided insight into the molecular underpinnings of visceral regeneration, including a specific tandem-duplicated prostatic secretory protein of 94 amino acids (PSP94)-like gene family and a significantly expanded fibrinogen-related protein (FREP) gene family. This high-quality genome resource will provide a useful framework for future research into biological processes and evolution in deuterostomes, including remarkable regenerative abilities that could have medical applications. Moreover, the multiomics data will be of prime value for commercial sea cucumber breeding programs.
first_indexed 2024-12-22T07:23:26Z
format Article
id doaj.art-48a1eec76ee24f74bc33889df620b1a8
institution Directory Open Access Journal
issn 1544-9173
1545-7885
language English
last_indexed 2024-12-22T07:23:26Z
publishDate 2017-10-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Biology
spelling doaj.art-48a1eec76ee24f74bc33889df620b1a82022-12-21T18:34:13ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852017-10-011510e200379010.1371/journal.pbio.2003790The sea cucumber genome provides insights into morphological evolution and visceral regeneration.Xiaojun ZhangLina SunJianbo YuanYamin SunYi GaoLibin ZhangShihao LiHui DaiJean-François HamelChengzhang LiuYang YuShilin LiuWenchao LinKaimin GuoSongjun JinPeng XuKenneth B StoreyPin HuanTao ZhangYi ZhouJiquan ZhangChenggang LinXiaoni LiLili XingDa HuoMingzhe SunLei WangAnnie MercierFuhua LiHongsheng YangJianhai XiangApart from sharing common ancestry with chordates, sea cucumbers exhibit a unique morphology and exceptional regenerative capacity. Here we present the complete genome sequence of an economically important sea cucumber, A. japonicus, generated using Illumina and PacBio platforms, to achieve an assembly of approximately 805 Mb (contig N50 of 190 Kb and scaffold N50 of 486 Kb), with 30,350 protein-coding genes and high continuity. We used this resource to explore key genetic mechanisms behind the unique biological characters of sea cucumbers. Phylogenetic and comparative genomic analyses revealed the presence of marker genes associated with notochord and gill slits, suggesting that these chordate features were present in ancestral echinoderms. The unique shape and weak mineralization of the sea cucumber adult body were also preliminarily explained by the contraction of biomineralization genes. Genome, transcriptome, and proteome analyses of organ regrowth after induced evisceration provided insight into the molecular underpinnings of visceral regeneration, including a specific tandem-duplicated prostatic secretory protein of 94 amino acids (PSP94)-like gene family and a significantly expanded fibrinogen-related protein (FREP) gene family. This high-quality genome resource will provide a useful framework for future research into biological processes and evolution in deuterostomes, including remarkable regenerative abilities that could have medical applications. Moreover, the multiomics data will be of prime value for commercial sea cucumber breeding programs.https://doi.org/10.1371/journal.pbio.2003790
spellingShingle Xiaojun Zhang
Lina Sun
Jianbo Yuan
Yamin Sun
Yi Gao
Libin Zhang
Shihao Li
Hui Dai
Jean-François Hamel
Chengzhang Liu
Yang Yu
Shilin Liu
Wenchao Lin
Kaimin Guo
Songjun Jin
Peng Xu
Kenneth B Storey
Pin Huan
Tao Zhang
Yi Zhou
Jiquan Zhang
Chenggang Lin
Xiaoni Li
Lili Xing
Da Huo
Mingzhe Sun
Lei Wang
Annie Mercier
Fuhua Li
Hongsheng Yang
Jianhai Xiang
The sea cucumber genome provides insights into morphological evolution and visceral regeneration.
PLoS Biology
title The sea cucumber genome provides insights into morphological evolution and visceral regeneration.
title_full The sea cucumber genome provides insights into morphological evolution and visceral regeneration.
title_fullStr The sea cucumber genome provides insights into morphological evolution and visceral regeneration.
title_full_unstemmed The sea cucumber genome provides insights into morphological evolution and visceral regeneration.
title_short The sea cucumber genome provides insights into morphological evolution and visceral regeneration.
title_sort sea cucumber genome provides insights into morphological evolution and visceral regeneration
url https://doi.org/10.1371/journal.pbio.2003790
work_keys_str_mv AT xiaojunzhang theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT linasun theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT jianboyuan theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT yaminsun theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT yigao theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT libinzhang theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT shihaoli theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT huidai theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT jeanfrancoishamel theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT chengzhangliu theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT yangyu theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT shilinliu theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT wenchaolin theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT kaiminguo theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT songjunjin theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT pengxu theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT kennethbstorey theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT pinhuan theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT taozhang theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT yizhou theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT jiquanzhang theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT chengganglin theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT xiaonili theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT lilixing theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT dahuo theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT mingzhesun theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT leiwang theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT anniemercier theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT fuhuali theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT hongshengyang theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT jianhaixiang theseacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT xiaojunzhang seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT linasun seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT jianboyuan seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT yaminsun seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT yigao seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT libinzhang seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT shihaoli seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT huidai seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT jeanfrancoishamel seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT chengzhangliu seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT yangyu seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT shilinliu seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT wenchaolin seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT kaiminguo seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT songjunjin seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT pengxu seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT kennethbstorey seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT pinhuan seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT taozhang seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT yizhou seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT jiquanzhang seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT chengganglin seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT xiaonili seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT lilixing seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT dahuo seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT mingzhesun seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT leiwang seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT anniemercier seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT fuhuali seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT hongshengyang seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration
AT jianhaixiang seacucumbergenomeprovidesinsightsintomorphologicalevolutionandvisceralregeneration