Transcriptome analysis for identifying possible causes of post-reproductive death of Sepia esculenta based on brain tissue

  • Jinyong Zhang
  • Muchun He
  • Zilong Xiang
  • Shufang LiuEmail author
  • ZhiMeng ZhuangEmail author
Research Article



The subpeduncle lobe/olfactory lobe–optic gland axis is called the endocrine regulation center of cephalopods. However, little is known about the mechanism of the subpeduncle lobe/olfactory lobe-optic gland axis regulate the sexual maturation and post-reproductive death of Sepia esculenta Hoyle.


The primary objective of this study was to provide basic information for revealing the mechanism of the subpeduncle lobe/olfactory lobe–optic axis regulating the rapid post-reproductive death of S. esculenta.


In this paper, Illumina sequencing based transcriptome analysis was performed on the brain tissue of female S. esculenta in the three key developmental stages: growth stage (BG), spawning stage (BS), and post-reproductive death stage (BA).


A total of 66.19 Gb Illumina sequencing data were obtained. A comparative analysis of the three stages showed 2609, 3333, and 170 differentially expressed genes (DEGs) in BG-vs-BA, BG-vs-BA, and BS-vs-BA, respectively. The Gene Ontology (GO) enrichment analysis of DEGs revealed that the regulation of cyclin-dependent protein serine/threonine kinase activity, oxidative phosphorylation, and respiratory chain were significantly enriched. The significant enrichment analysis of the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway identified pathways associated with the regulation of death, such as the mammalian target of rapamycin (mTOR) signaling pathway, AMPK signaling pathway, oxidative phosphorylation, and cell cycle.


The post-reproductive death of S. esculenta was found to be a complex energy steady-state regulation network system. The mTOR acted as an energy receptor and had a key role in regulating energy homeostasis.


DEGs Golden cuttlefish Rapid post-reproductive death Sepia esculenta Subpeduncle lobe/olfactory lobe Transcriptome 



This work was supported by the National Natural Science Foundation of China (31672645), and the basic scientific research service fee of the Central Scientific Research Institute (20603022016001) and Taishan Scholar Project, Shandong Province (2015-2019).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

13258_2019_811_MOESM1_ESM.docx (17 kb)
Supplementary material 1 (DOCX 16 KB)
13258_2019_811_MOESM2_ESM.opj (45 kb)
Supplementary material 2 (OPJ 44 KB)
13258_2019_811_MOESM3_ESM.opj (44 kb)
Supplementary material 3 (OPJ 43 KB)
13258_2019_811_MOESM4_ESM.opj (44 kb)
Supplementary material 4 (OPJ 44 KB)
13258_2019_811_MOESM5_ESM.opj (44 kb)
Supplementary material 5 (OPJ 43 KB)
13258_2019_811_MOESM6_ESM.opj (44 kb)
Supplementary material 6 (OPJ 44 KB)
13258_2019_811_MOESM7_ESM.opj (44 kb)
Supplementary material 7 (OPJ 44 KB)
13258_2019_811_MOESM8_ESM.opj (44 kb)
Supplementary material 8 (OPJ 44 KB)
13258_2019_811_MOESM9_ESM.opj (44 kb)
Supplementary material 9 (OPJ 43 KB)
13258_2019_811_MOESM10_ESM.opj (44 kb)
Supplementary material 10 (OPJ 44 KB)
13258_2019_811_MOESM11_ESM.opj (44 kb)
Supplementary material 11 (OPJ 44 KB)


  1. Albertin CB, Simakov O, Mitros T, Wang ZY, Pungor JR, Edsinger-Gonzales E, Brenner S, Ragsdale CW, Rokhsar DS (2015) The octopus genome and the evolution of cephalopod neural and morphological novelties. Nature 524:220–224CrossRefGoogle Scholar
  2. Bian L, Liu CL, Chen SQ, Zhao FZ, Ge JL, Tan J (2018) Transcriptome analysis of gene expression patterns during embryonic development in golden cuttlefish (Sepia esculenta). Genes Genom 40:253–263CrossRefGoogle Scholar
  3. Brown EJ, Albers MW, Shin TB, Ichikawa K, Keith CT (1994) A mammalian protein targeted by G1-arresting rapamycin–receptor complex. Nature 369(6483):756–758CrossRefGoogle Scholar
  4. Copes N, Edwards C, Chaput D, Saifee M, Barjuca I, Nelson D, Paraggio A, Saad P, Lipps D, Stevens SM Jr, Bradshaw PC (2015) Metabolome and proteome changes with aging in Caenorhabditis elegans. Exp Gerontol 72:67–84CrossRefGoogle Scholar
  5. Cota D, Proulx K, Blake Smith KA, Kozma Sara C, Thomas G, Woods SC, Seeley RJ (2006) Hypothalamic mTOR signaling regulates food intake. Science 312:927–930CrossRefGoogle Scholar
  6. Di Cristo C (2013) Nervous control of reproduction in Octopus vulgaris: a new model. Invert Neurosci 13:27–34CrossRefGoogle Scholar
  7. Di Cosmo A, Di Cristo C (1998) Neuropeptidergic control of the optic gland of Octopus vulgaris: FMRF-amide and GnRH immunoreactivity. J Comp Neurol 398(1):1–12CrossRefGoogle Scholar
  8. Diter F (1974) The subpeduncle lobe of the octopus brain: evidence for dual function. Brain Res 75:277–285CrossRefGoogle Scholar
  9. Fox TD (2016) Mitochondrial protein synthesis, import, and assembly. Genetics 192(4):1203–1234CrossRefGoogle Scholar
  10. Harel I, Benayoun BA, Machado B, Singh PP, Hu CK, Pech MF, Valenzano DR, Zhang E, Sharp SC, Artandi SE, Brunet A (2015) A platform for rapid exploration of aging and diseases in a naturally short-lived vertebrate. Cell 160(5):1013–1026CrossRefGoogle Scholar
  11. Hoving HJT, Lipinski MR, Videler JJ (2008) Reproductive system and the spermatophoric reaction of the mesopelagic squid Octopoteuthis sicula (Rüppell, 1844) (Cephalopoda: Octopoteuthidae) from southern African waters. Afr J Mar Sci 30:603–612CrossRefGoogle Scholar
  12. Howell JJ, Manning BD (2011) mTOR couples cellular nutrient sensing to organismal metabolic homeostasis. Trends Endocrinol Metab 22(3):94–102CrossRefGoogle Scholar
  13. Imamura K, Ogura T, Kishimoto A, Kaminishi M, Esumi H (2001) Cell cycle regulation via p53 phosphorylation by a 5′-AMP activated protein kinase activator, 5-aminoimidazole-4-carboxamide-1-beta-D-ribofuranoside, in a human hepatocellular carcinoma cell line. Biochem Biophys Res Commun 2:562–567CrossRefGoogle Scholar
  14. Jiang J, Feng L, Liu Y, Jiang WD, Hu K, Li SH, Zhou XQ (2013) Mechanistic target of rapamycin in common carp: cDNA cloning, characterization, and tissue expression. GENE 512(2):566–572CrossRefGoogle Scholar
  15. Jones OR, Scheuerlein A, Salguero-Gómez R, Camarda CG, Schaible R, Casper BB, Dahlgren JP, Ehrlén J, García MB, Menges ES, Quintana-Ascencio PF, Caswell H, Baudisch A, Vaupel JW (2014) Diversity of ageing across the tree of life. Nature 505:169–173CrossRefGoogle Scholar
  16. Jung H, Lyons RE, Dinh H, Hurwood DA, McWilliam S, Mather PB (2011) Transcriptomics of a giant freshwater prawn (Macrobrachium rosenbergii): de novo assembly,annotation and marker discovery. PLoS One 6(12):e27938CrossRefGoogle Scholar
  17. Kerscher O, Felberbaum R, Hochstrasser M (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22:159–180CrossRefGoogle Scholar
  18. King RW, Deshaies RJ, Peters JM, Kirschner MW (1996) How proteolysis drives the cell cycle. Science 274(5293):1652–1659CrossRefGoogle Scholar
  19. Komander D, Rape M (2012) The ubiquitin code. Annu Rev Biochem 81:203–229CrossRefGoogle Scholar
  20. Kumar L, Futschik ME (2007) Mfuzz: a software package for soft clustering of microarray data. Bioinformation 2(1):5–7CrossRefGoogle Scholar
  21. Künstner A, Wolf JBW, Backstrom N, Whitney O, Balakrishnan CN, Day L, Edwards SV, Janes DE, Schlinger BA, Wilson RK, Jarvis ED, Warren WC, Ellegren H (2010) Comparative genomics based on massive parallel transcriptome sequencing reveals patterns of substitution and selection across 10 bird species. Mol Ecol 19(Suppl 1):266–276CrossRefGoogle Scholar
  22. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359CrossRefGoogle Scholar
  23. Laplante M, Sabatini DM (2009) mTOR signaling at a glance. J Cell Sci 122(Pt 20):3589–3594CrossRefGoogle Scholar
  24. Laplante M, Sabatini DM (2012) mTOR Signaling. Csh Perspect Biol 4(2):1Google Scholar
  25. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. Google Scholar
  26. Liang Y, Bao WL, Bao CC, Miao XF, Hao HF, Li SY, Wang ZG, Liu DJ (2012) Molecular characterization and functional analysis of Cashmere goat mammalian target of rapamycin. DNA Cell Biol 31(5):839–844CrossRefGoogle Scholar
  27. Liu CL, Zhao FZ, Yan JP, Liu CS, Liu SW, Chen SQ (2016) Transcriptome sequencing and de novo assembly of golden cuttlefish Sepia esculenta Hoyle. Int J Mol Sci 17:1749CrossRefGoogle Scholar
  28. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ∆∆Ct method. Methods 25(4):402–408CrossRefGoogle Scholar
  29. Lu ZM, Liu W, Liu LQ, Shi HL, Ping HL, Wang TM, Chi CF, Wu CW, Chen CH, Shen KN (2016) De novo assembly and comparison of the ovarian transcriptomes of the common Chinese cuttlefish (Sepiella japonica) with different gonadal development. Genom Data 7(C):155–158CrossRefGoogle Scholar
  30. Lynch CJ, Patson BJ, Anthony J, Vaval A, Jefferson LS, Vary TC (2002) Leucine is a direct-acting nutrient signal that regulates protein synthesis in adipose tissue. Am J Physiol Endocrinol Metab 283(3):E503–E513CrossRefGoogle Scholar
  31. Messenger JB (1979) The nervous system of Loligo. IV. The peduncle and olfactory lobes. Philos Trans R Soc Lond B Biol Sci 285:275–308CrossRefGoogle Scholar
  32. Meter MV, Gorbunova V, Seluanov A (2016) Comparative biology of aging: insights from long-lived rodent species. Handbook of the Biology of Aging (8 Edition) 305–324 Academic Press: CambridgeCrossRefGoogle Scholar
  33. Minakata H, Shigeno S, Kano N, Haraguchi S, Osugi T, Tsutsui K (2009) Octopus gonadotrophin-releasing hormone: a multifunctional peptide in the endocrine and nervous systems of the cephalopod. J Neuroendocrinol 21:322–326CrossRefGoogle Scholar
  34. Morrison CD, Xi XC, White CL, Ye JP, Martin RJ (2007) Amino acids inhibit Agrp gene expression via an mTOR-dependent mechanism. Am J Physiol Endocrinol Metab 293(1):E165–E171CrossRefGoogle Scholar
  35. Nesis KN (1987) Cephalopods of the world. Neptune City: T. F. H. Publications 1–15Google Scholar
  36. Park DC, Yeo SG (2013) Aging. Korean J Audiol 17(2):39–44CrossRefGoogle Scholar
  37. Rocha F, Guerra A, Gonzalez AF (2001) A review of reproductive strategies in cephalopods. Biol Rev 76:291–304CrossRefGoogle Scholar
  38. Rodhouse PG (1998) Physiological progenesis in cephalopod mollusks. Biol Bull 195:17–20CrossRefGoogle Scholar
  39. Ropelle ER, Pauli JR, Fernandes MF, Rocco SA, Marin RM, Morari J, Souza KK, Dias MM, Gomes-Marcondes MC, Gontijo JA, Franchini KG, Velloso LA, Saad MJ, Carvalheira JB (2008) A central role for neuronal AMP-activated protein kinase (AMPK) and mammalian target of rapamycin (mTOR) in high-protein diet-induced weight loss. Diabetes 57(3):594–605CrossRefGoogle Scholar
  40. Storey JD (2003) The positive false discovery rate: a Bayesian interpretation and the q-value. Ann Stat 31:2013–2035CrossRefGoogle Scholar
  41. Teaniniuraitemoana V, Huvet A, Levy P, Klopp C, Lhuillier E, Gaertner-Mazouni N, Gueguen Y, Le Moullac G (2014) Gonad transcriptome analysis of pearl oyster Pinctada margaritifera: identification of potential sex differentiation and sex determining genes. BMC Genom 15(1):491CrossRefGoogle Scholar
  42. Tian K, Lou FR, Gao TX, Zhou YD, Miao ZQ, Han ZQ (2018) De novo assembly and annotation of the whole transcriptome of Sepiella maindroni. Mar Genom 38:13–16CrossRefGoogle Scholar
  43. Wan LY, Su W, Li B, Lei Y, Yan LY, Kang YP, Huan DX, Chen YN, Jiang HF, Liao BS (2018) Molecular analysis of formation of drought tolerance traits in peanut. Chin J Oil Crop Sci 40(3):335–343 (Chinese with English abstract)Google Scholar
  44. Wang LK, Feng ZX, Wang X, Wang XW, Zhang XG (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–148CrossRefGoogle Scholar
  45. Wang L, Zhang XM, Ding PW, Liu TY, Chen SQ (2017) Reproductive behavior and mating strategy of Sepia esculenta. Acta Ecol Sin 1000-0933(6):1871–1880 (Chinese with English abstract)Google Scholar
  46. Wells MJ, Wells J (1959) Hormonal control of sexual maturity in octopus. J Exp Biol 36:1–33Google Scholar
  47. Xu GY, Li Y, An WJ, Li SD, Guan YF, Wang NP, Tang CS, Wang X, Zhu Y, Li XY, Mulholland MW, Zhang WZ (2009) Gastric mammalian target of rapamycin signaling regulates ghrelin production and food intake. Endocrinology 150(8):3637–3644CrossRefGoogle Scholar
  48. Yin YN, Liu CL, Hu P, Zhang JY, Liu SF, Zhuang ZM, Xue TM (2018) Histology of oogenesis and ovarian development in cultured Sepia esculenta. J Fish Sci China 25(3):503–511 (Chinese with English abstract)Google Scholar
  49. Young JZ (1971) The anatomy of the nervous system of Octopus vulgaris. Clarendon, OxfordGoogle Scholar
  50. Zhang X, Mao Y, Huang ZX, Qu M, Chen J, Ding SX, Hong JN, Sun TT (2012) Transcriptome analysis of the Octopus vulgaris central nervous system. PLoS One 7:e40320CrossRefGoogle Scholar
  51. Zhang JY, Liu CL, He MC, Xiang ZL, Yin YN, Liu SF, Zhuang ZM (2019) A full-length transcriptome of Sepia esculenta using a combination of single-molecule long-read (SMRT) and Illumina sequencing. Mar Genom 43:54–57CrossRefGoogle Scholar

Copyright information

© The Genetics Society of Korea 2019

Authors and Affiliations

  1. 1.Wuxi Fisheries CollegeNanjing Agricultural UniversityWuxiChina
  2. 2.Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery SciencesQingdaoChina
  3. 3.Function Laboratory for Marine Fisheries Science and Food Production ProcessesQingdao National Laboratory for Marine Science and TechnologyQingdaoChina
  4. 4.Ministry of Education Key Laboratory of Marine Genetics and Breeding, College of Marine Life SciencesOcean University of ChinaQingdaoChina
  5. 5.College of Fisheries and Life ScienceShanghai Ocean UniversityShanghaiChina

Personalised recommendations