Marine Biotechnology

, Volume 18, Issue 4, pp 485–499 | Cite as

Long Non-Coding RNAs (lncRNAs) of Sea Cucumber: Large-Scale Prediction, Expression Profiling, Non-Coding Network Construction, and lncRNA-microRNA-Gene Interaction Analysis of lncRNAs in Apostichopus japonicus and Holothuria glaberrima During LPS Challenge and Radial Organ Complex Regeneration

  • Chuang Mu
  • Ruijia WangEmail author
  • Tianqi Li
  • Yuqiang Li
  • Meilin Tian
  • Wenqian Jiao
  • Xiaoting Huang
  • Lingling Zhang
  • Xiaoli Hu
  • Shi Wang
  • Zhenmin BaoEmail author
Original Article


Long non-coding RNA (lncRNA) structurally resembles mRNA but cannot be translated into protein. Although the systematic identification and characterization of lncRNAs have been increasingly reported in model species, information concerning non-model species is still lacking. Here, we report the first systematic identification and characterization of lncRNAs in two sea cucumber species: (1) Apostichopus japonicus during lipopolysaccharide (LPS) challenge and in heathy tissues and (2) Holothuria glaberrima during radial organ complex regeneration, using RNA-seq datasets and bioinformatics analysis. We identified A. japonicus and H. glaberrima lncRNAs that were differentially expressed during LPS challenge and radial organ complex regeneration, respectively. Notably, the predicted lncRNA-microRNA-gene trinities revealed that, in addition to targeting protein-coding transcripts, miRNAs might also target lncRNAs, thereby participating in a potential novel layer of regulatory interactions among non-coding RNA classes in echinoderms. Furthermore, the constructed coding-non-coding network implied the potential involvement of lncRNA-gene interactions during the regulation of several important genes (e.g., Toll-like receptor 1 [TLR1] and transglutaminase-1 [TGM1]) in response to LPS challenge and radial organ complex regeneration in sea cucumbers. Overall, this pioneer systematic identification, annotation, and characterization of lncRNAs in echinoderm pave the way for similar studies and future genetic, genomic, and evolutionary research in non-model species.


Long non-coding RNA (lncRNA) RNA-seq Sea cucumber Innate immune response Tissue regeneration 



This work was supported by the National Natural Science Foundation of China (31502165) and Shandong Provincial Natural Science Foundation, China (ZR2015CQ001). The authors wish to thank Dr. Yan Sun, and Xue Li, Jing Wang, Xiaogang Xun and Liheng Zhang for their assistance in bioinformatics analysis.

Compliance with ethical standards

Conflict of Interests

No conflicts of interest are declared.

Supplementary material

10126_2016_9711_Fig6_ESM.jpg (82 kb)
Supplementary Fig. 1

Details of the correlation coefficients in the correlation matrices of A. japonicus and H. glaberrima. Details of correlation coefficients and p values in the correlation matrices of A. japonicus and H. glaberrima. (a) Distribution of correlation coefficients in the correlation matrix of A. japonicas; (b) correlation coefficients and p values in the correlation matrix of A. japonicas; (c) distribution of correlation coefficients in the correlation matrix of H. glaberrima; (d) correlation coefficients and p values in the correlation matrix of H. glaberrima. The plots were generated using correlation coefficients, p values, and the frequency (counts) of lncRNA/gene pairs in each interval. Blue dots correspond to highly significantly correlated lncRNAs/genes pairs (|correlation coefficient| >0.95 and a two-tailed p value <0.05); green dots correspond to significantly correlated lncRNAs/genes pairs (|correlation coefficient| >0.75 and a two-tailed p value <0.05); red dots correspond to other lncRNAs/genes pairs (|correlation coefficient| <0.75 or p value >0.05) (JPG 82 kb)

10126_2016_9711_MOESM1_ESM.tif (1.3 mb)
High resolution image (TIF 1319 kb)
10126_2016_9711_Fig7_ESM.jpg (68 kb)
Supplementary Fig. 2

The molecular function and cellular component enrichment networks of A. japonicus and H. glaberrima. The coding-non-coding enrichment network corresponding to the ontologies of molecular function and cellular component for A.japonicus and H. glaberrima. (a) The cellular component network of A.japonicus; (b) the molecular function network of A.japonicus; (c) the cellular component network of H. glaberrima; (d) the molecular function network of H. glaberrima (JPG 67 kb)

10126_2016_9711_MOESM2_ESM.tif (6.6 mb)
High resolution image (TIF 6711 kb)
10126_2016_9711_Fig8_ESM.jpg (66 kb)
Supplementary Fig. 3

Clusters of biological process networks in A. japonicus and H. glaberrima. Clusters of biological process networks for the two species, including the three clusters in biological process network of A. japonicus (a, b, and c) and the three clusters in biological process network of H. glaberrima (d, e, and f) (JPG 65 kb)

10126_2016_9711_MOESM3_ESM.tif (5.9 mb)
High resolution image (TIF 6029 kb)
10126_2016_9711_Fig9_ESM.jpg (104 kb)
Supplementary Fig. 4

A summary of the GO enrichment analysis of the microRNA-targeted genes in A. japonicus and H. glaberrima. The GO enrichment analysis of the microRNA-targeted genes in (a) A. japonicus and (b) H. glaberrima. The x-axis corresponds to the GO terms of the three ontological categories, and the y-axis corresponds to the percentage of gene sequences (JPG 104 kb)

10126_2016_9711_MOESM4_ESM.tif (2.9 mb)
High resolution image (TIF 2931 kb)
10126_2016_9711_MOESM5_ESM.xlsx (814 kb)
Supplementary Table 1 List of lncRNAs in A. japonicus and H. glaberrima (XLSX 814 kb)
10126_2016_9711_MOESM6_ESM.xlsx (10 kb)
Supplementary Table 2 Summary of lncRNA hits in other species (XLSX 10 kb)
10126_2016_9711_MOESM7_ESM.xlsx (14 kb)
Supplementary Table 3 Summary of reciprocal blast results for lncRNAs in A. japonicus and H. glaberrima (XLSX 13 kb)
10126_2016_9711_MOESM8_ESM.xlsx (214 kb)
Supplementary Table 4 Differentially expressed genes and lncRNAs in A. japonicus and H. glaberrima (XLSX 214 kb)
10126_2016_9711_MOESM9_ESM.xlsx (33 kb)
Supplementary Table 5 Details of significantly enriched GO terms in the coding-non-coding enrichment networks of A. japonicus and H. glaberrima (XLSX 33 kb)
10126_2016_9711_MOESM10_ESM.xlsx (238 kb)
Supplementary Table 6 The lncRNA-microRNA-gene trinities in A. japonicus and H. glaberrima (XLSX 238 kb)
10126_2016_9711_MOESM11_ESM.docx (845 kb)
ESM 1 (DOCX 844 kb)
10126_2016_9711_MOESM12_ESM.docx (864 kb)
ESM 2 (DOCX 864 kb)
10126_2016_9711_MOESM13_ESM.docx (58 kb)
ESM 3 (DOCX 58 kb)


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Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Chuang Mu
    • 1
  • Ruijia Wang
    • 1
    Email author
  • Tianqi Li
    • 1
  • Yuqiang Li
    • 1
  • Meilin Tian
    • 1
  • Wenqian Jiao
    • 1
  • Xiaoting Huang
    • 1
  • Lingling Zhang
    • 1
  • Xiaoli Hu
    • 1
  • Shi Wang
    • 1
  • Zhenmin Bao
    • 1
    Email author
  1. 1.Ministry of Education Key Laboratory of Marine Genetics and Breeding, College of Marine Life SciencesOcean University of ChinaQingdaoChina

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