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

PLoS Biol. 2017 Oct 12;15(10):e2003790. doi: 10.1371/journal.pbio.2003790. eCollection 2017 Oct.

Abstract

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.

MeSH terms

  • Animals
  • Biological Evolution*
  • Bone and Bones / anatomy & histology
  • Calcification, Physiologic / genetics
  • Conserved Sequence / genetics
  • Genes, Homeobox
  • Genome*
  • Multigene Family
  • Nervous System / metabolism
  • Phylogeny
  • Regeneration / genetics*
  • Sea Cucumbers / anatomy & histology*
  • Sea Cucumbers / genetics*
  • Sea Cucumbers / physiology
  • Viscera / physiology*

Grant support

The National High-Technology Research and Development Program of China http://program.most.gov.cn/ (grant number 2012AA10A404, 2012AA092205). Received by JX and XZ. Strategic Priority Research Program of the Chinese Academy of Sciences http://www.cas.cn/xxgkml/zgkxyyb/kxyj/xdzx/ (grant number XDA11020703, XDA11020704). Received by LZ, CLin, and HY. National Natural Science Foundation of China http://www.nsfc.gov.cn/ (grant number U1406404, 31272397). Received by HY and SJ. The Scientific and Technological Innovation Project of Qingdao National Laboratory for Marine Science and Technology http://www.qnlm.ac/index (grant number 2015ASKJ02-03). Received by JX. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.