Skip to main content
SpringerLink
Log in

Muscle transcriptome resource for growth, lipid metabolism and immune system in Hilsa shad, Tenualosa ilisha

  • Research Article
  • Published:
Genes & Genomics Aims and scope Submit manuscript

Abstract

The information on the genes involved in muscle growth, lipid metabolism and immune systems would help to understand the mechanisms during the spawning migration in Hilsa shad, which in turn would be useful in its future domestication process. The primary objective of this study was to generate the transcriptome profile of its muscle through RNA seq. The total RNA was isolated and library was prepared from muscle tissue of Tenualosa ilisha, which was collected from Padma River at Farakka, India. The prepared library was then sequenced by Illumina HiSeq platform, HiSeq 2000, using paired-end strategy. A total of 8.68 GB of pair-end reads of muscle transcriptome was generated, and 43,384,267 pair-end reads were assembled into 3,04,233 contigs, of which 23.99% of assembled contigs has length ≥ 150 bp. The total GO terms were categorised into cellular component, molecular function and biological process through PANTHER database. Fifty-three genes related to muscle growth were identified and genes in different pathways were: 75 in PI3/AKT, 46 in mTOR, 76 in MAPK signalling, 24 in Janus kinase–signal transducer and activator of transcription, 45 in AMPK and 27 in cGMP pathways. This study also mined the genes involved in lipid metabolism, in which glycerophospholipid metabolism contained highest number of genes (32) and four were found to be involved in fatty acid biosynthesis. There were 58 immune related genes found, in which 31 were under innate and 27 under adaptive immunity. The present study included a large genomic resource of T. ilisha muscle generated through RNAseq, which revealed the essential dataset for our understanding of regulatory processes, specifically during the seasonal spawning migration. As Hilsa is a slow growing fish, the genes identified for muscle growth provided the basic information to study myogenesis. In addition, genes identified for lipid metabolism and immune system would provide resources for lipid synthesis and understanding of Hilsa defense mechanisms, respectively.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alam AK, Mohanty BP, Hoq ME, Thilshed S (2012) Nutritional values, consumption and utilization of Hilsa Tenualosa ilisha (Hamilton 1822). In: Proceedings of the Regional Workshop on Hilsa: potential for aquaculture.

  • Bassel-Duby R, Olson EN (2006) Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem 7:75:19–37

    Article  CAS  Google Scholar 

  • Betancor MB, Ortega A, de la Gándara F, Tocher DR, Mourente G (2017) Lipid metabolism-related gene expression pattern of Atlantic bluefin tuna (Thunnus thynnus L.) larvae fed on live prey. Fish Physiol Biochem 43(2):493–516

    Article  CAS  PubMed  Google Scholar 

  • Bhuiyan AI, Momen M (2012) Studies on the protozoan parasites of Hilsa Shad, Tenualosa Ilisha in Bangladesh. Bangladesh J Zool 40(1):33–41

    Article  Google Scholar 

  • Bower NI. Taylor RG. Johnston IA (2009) Phasing of muscle gene expression with fasting-induced recovery growth in Atlantic salmon. Front Zool 6(1):18

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Buckingham M, Rigby PW (2014) Gene regulatory networks and transcriptional mechanisms that control myogenesis. Dev Cell 28(3):225–238

    Article  CAS  PubMed  Google Scholar 

  • Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinform 10(1):421

    Article  CAS  Google Scholar 

  • Chatterjee A, Roy D, Patnaik E, Nongthomba U (2016) Muscles provide protection during microbial infection by activating innate immune response pathways in Drosophila and zebrafish. Dis Models Mech 9(6):697–705

    Article  CAS  Google Scholar 

  • Cuesta A, Vargas-Chacoff L, García-López A, Arjona FJ, Martínez-Rodríguez G, Meseguer J, Mancera JM, Esteban MA (2007) Effect of sex-steroid hormones, testosterone and estradiol, on humoral immune parameters of gilthead seabream. Fish Shellfish Immunol 23(3):693–700

    Article  CAS  PubMed  Google Scholar 

  • de Paula TG, Zanella BT, de Almeida Fantinatti BE, de Moraes LN, da Silva Duran BO, de Oliveira CB, Salomão RA, da Silva RN, Padovani CR, Mareco EA, Carvalho RF (2017) Food restriction increase the expression of mTORC1 complex genes in the skeletal muscle of juvenile pacu (Piaractus mesopotamicus). PLoS ONE 12(5):e0177679

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dewan BK, Mia MS, Yeasmin F, Sarker SC, Siddiky MN, Kamal M (2015) Studies on the proximate composition of Hilsa of different size groups at Chandpur region. Int J Nat Soc Sci 2(5):52–55

    Google Scholar 

  • Di Donato V, Auer TO, Duroure K, Del Bene F (2013) Characterization of the calcium binding protein family in zebrafish. PLoS ONE 8(1):e53299

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dinarello CA (2010) Anti-inflammatory agents: present and future. Cell 140(6):935–950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Divya BK, Yadav P, Masih P, Singh RK, Mohindra V (2017) In silico characterization of myogenic factor 6 transcript of Hilsa, Tenualosa ilisha and putative role of its SNPs with differential growth. Meta Gene 13:140–148

    Article  Google Scholar 

  • Fuentes EN, Valdés JA, Molina A, Björnsson BT (2013) Regulation of skeletal muscle growth in fish by the growth hormone–insulin-like growth factor system. Gen Com Endocrinol 192:136–148

    Article  CAS  Google Scholar 

  • Geisler HW, Shi H, Gerrard DE (2013) MAPK pathway in skeletal muscle diseases. J Vet Sci Anim Husb 1(1):1

    Google Scholar 

  • Ghobeishavi A, Mousavi SM, Yavari V, Kochanian P, Zakeri M (2016) The innate immunity changes of the female anadromous hilsa shad, Tenulaosa ilisha, during spawning and post spawning season. Iran J Fish Sci 15(4):1526–1539

    Google Scholar 

  • Gurmaches SJ, Garcia CL, Gutierrez J, Navarro I (2012) Adiponectin effects and gene expression in rainbow trout: an in vivo and in vitro approach. J Exp Biol 215(8):1373–1383

    Article  CAS  Google Scholar 

  • Hablützel PI, Brown M, Friberg IM, Jackson JA (2016) Changing expression of vertebrate immunity genes in an anthropogenic environment: a controlled experiment. BMC Evolut Biol 16(1):175

    Article  Google Scholar 

  • Hamilton F (1822) An account of the fishes found in the river Ganges and its branches. Constable and company, Edinburgh

    Book  Google Scholar 

  • Hardie DG. Schaffer BE, Brunet A (2016) AMPK: an energy-sensing pathway with multiple inputs and outputs. Trends Cell Biol 26(3):190–201

    Article  CAS  PubMed  Google Scholar 

  • Harris J, Bird DJ (2000) Modulation of the fish immune system by hormones. Vet Immunol Immunopathol 77(3):163–176

    Article  CAS  PubMed  Google Scholar 

  • Hossain M, Adhikary RK, Mahbu KR, Begum M, Islam MR (2012) Effect of 10% concentrations of salt, garlic and coriander on the quality of smoked hilsa Fish (Tenualosa ilisha). Am J Food Technol 7:501–505

    Article  CAS  Google Scholar 

  • Huang Y, Chain FJ, Panchal M, Eizaguirre C, Kalbe M, Lenz TL, Samonte IE, Stoll M, Bornberg-Bauer E, Reusch TB, Milinski M (2016) Transcriptome profiling of immune tissues reveals habitat-specific gene expression between lake and river sticklebacks. Mol Ecol 25(4):943–958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin J, Médale F, Kamalam BS, Aguirre P, Véron V, Panserat S (2014) Comparison of glucose and lipid metabolic gene expressions between fat and lean lines of rainbow trout after a glucose load. PLoS ONE 9(8):e105548

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Johnston IA. Bower NI. Macqueen DJ (2011) Growth and the regulation of myotomal muscle mass in teleost fish. J Exp Biol 214(10):1617–1628

    Article  CAS  PubMed  Google Scholar 

  • Joshi NA, Fass JN (2011) Sickle: a sliding-window, adaptive, quality-based trimming tool for FastQ files (Version 1.33) [Software]. Available at https://github.com/najoshi/sickle

  • Kamalam BS, Medale F, Kaushik S, Polakof S, Skiba-Cassy S, Panserat S (2012) Regulation of metabolism by dietary carbohydrates in two lines of rainbow trout divergently selected for muscle fat content. J Exp Biol 215(15):2567–2578

    Article  CAS  PubMed  Google Scholar 

  • Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28(1):27–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim YH, Chung JI, Woo HG, Jung YS, Lee SH, Moon CH, Suh-Kim H, Baik EJ (2010) Differential regulation of proliferation and differentiation in neural precursor cells by the Jak pathway. Stem Cells 28(10):1816–1828

    Article  CAS  PubMed  Google Scholar 

  • Klopfleisch R, Gruber AD (2012) Transcriptome and proteome research in veterinary science: what is possible and what questions can be asked? Sci World J. https://doi.org/10.1100/2012/254962

    Article  Google Scholar 

  • Lass A, Zimmermann R, Haemmerle G, Riederer M, Schoiswohl G, Schweiger M, Kienesberger P, Strauss JG, Gorkiewicz G, Zechner R (2006) Adipose triglyceride lipase-mediated lipolysis of cellular fat stores is activated by CGI-58 and defective in Chanarin-Dorfman Syndrome. Cell Metab 3(5):309–319

    Article  CAS  PubMed  Google Scholar 

  • Le Grand F, Jones AE, Seale V, Scimè A, Rudnicki MA (2009) Wnt7a activates the planar cell polarity pathway to drive the symmetric expansion of satellite stem cells. Cell Stem Cell 4(6):535–547

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leonard JBK, McCormick SD (1999) The effect of migration distance and timing on metabolic enzyme activity in an anadromous clupeid, the American shad (Alosa sapidissima). Fish Physiol Biochem 20(2):163–179

    Article  CAS  Google Scholar 

  • Liang XF, Ogata HY, Oku H (2002) Effect of dietary fatty acids on lipoprotein lipase gene expression in the liver and visceral adipose tissue of fed and starved red sea bream Pagrus major. Comp Biochem Physiol A: Mol Integr Physiol 132(4):913–919

    Article  Google Scholar 

  • Lin KW, Li J, Finn PW (2011) Emerging pathways in asthma: Innate and adaptive interactions. Biochim Biophy Acta (BBA)-Gen Subj 1810(11):1052–1058

    Article  CAS  Google Scholar 

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17(1):10

    Article  Google Scholar 

  • Martin SA, Douglas A, Houlihan DF, Secombes CJ (2010) Starvation alters the liver transcriptome of the innate immune response in Atlantic salmon (Salmo salar). BMC Genom 11(1):418

    Article  CAS  Google Scholar 

  • Mi H, Poudel S, Muruganujan A, Casagrande JT, Thomas PD (2015) PANTHER version 10: expanded protein families and functions, and analysis tools. Nucleic Acids Res 44(D1):D336–D342

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mohanty BP, Ganguly S, Mahanty A, Sankar TV, Anandan R, Chakraborty K, Paul BN, Sarma D, Syama Dayal J, Venkateshwarlu G, Mathew S (2016) DHA and EPA content and fatty acid profile of 39 food fishes from India. BioMed Res Int. https://doi.org/10.1155/2016/4027437

    Article  PubMed  PubMed Central  Google Scholar 

  • Montfort J, Le Cam A, Gabillard JC, Rescan PY (2016) Gene expression profiling of trout regenerating muscle reveals common transcriptional signatures with hyperplastic growth zones of the post-embryonic myotome. BMC Genom 17(1):810

    Article  CAS  Google Scholar 

  • Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 1(suppl_2):W182–W185 35(

    Article  Google Scholar 

  • Musumeci G, Imbesi R, Szychlinska MA, Castrogiovanni P (2015) Apoptosis and skeletal muscle in aging. Open J Apoptosis 22(02):41

    Article  CAS  Google Scholar 

  • Ozsolak F, Milos PM (2011) RNA sequencing: advances, challenges and opportunities. Nat Rev Genet 12(2):87

    Article  CAS  PubMed  Google Scholar 

  • Pal D, Khozin-Goldberg I, Cohen Z, Boussiba S (2011) The effect of light, salinity, and nitrogen availability on lipid production by Nannochloropsis sp. Appl Microbiol Biotechnol 90(4):1429–1441

    Article  CAS  PubMed  Google Scholar 

  • Papatheodorou I, Oellrich A, Smedley D (2015) Linking gene expression to phenotypes via pathway information. J Biomed Semant 6(1):17

    Article  Google Scholar 

  • Pressley ME, Phelan PE, Witten PE, Mellon MT, Kim CH (2005) Pathogenesis and inflammatory response to Edwardsiella tarda infection in the zebrafish. Dev Comp Immunol 29(6):501–513

    Article  CAS  PubMed  Google Scholar 

  • Ralston A, Shaw K (2008) Gene expression regulates cell differentiation. Nat Educ 1(1):127

    Google Scholar 

  • Rannikko K. Ortutay C, Vihinen M (2007) Immunity genes and their orthologs: a multi-species database. Int Immunol 19(12):1361–1370

    Article  CAS  PubMed  Google Scholar 

  • Rao BM, Murthy LN, Mathew S, Asha KK, Sankar TV, Prasad MM (2012) Changes in the nutritional profile of Godavari hilsa shad, Tenualosa ilisha (Hamilton, 1822) during its anadromous migration from Bay of Bengal to the River Godavari. Indian J Fish 55:125–132

    Google Scholar 

  • Rauta PR, Nayak B, Das S (2012) Immune system and immune responses in fish and their role in comparative immunity study: a model for higher organisms. Immunol Lett 148(1):23–33

    Article  CAS  PubMed  Google Scholar 

  • Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD, Glass DJ (2001) Mediation of IGF-1-induced skeletal myotube hypertrophy by PI (3) K/Akt/mTOR and PI (3) K/Akt/GSK3 pathways. Nat Cell Biol 3(11)1009–1013

    Article  CAS  PubMed  Google Scholar 

  • Saito H, Kurogi H, Chow S, Mochioka N (2015) Variation of lipids and fatty acids of the Japanese freshwater Eel, Anguilla japonica, during Spawning Migration. J Oleo Sci 64(6):603–616

    Article  CAS  PubMed  Google Scholar 

  • Salem M, Manor ML, Aussanasuwannakul A, Kenney PB, Weber GM, Yao J (2013) Effect of sexual maturation on muscle gene expression of rainbow trout: RNA-Seq approach. Physiol Rep 1(5):e00120

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schiaffino S, Dyar KA, Ciciliot S, Blaauw B, Sandri M (2013) Mechanisms regulating skeletal muscle growth and atrophy. FEBS J 280(17):4294–4314

    Article  CAS  PubMed  Google Scholar 

  • Secombes CJ, Wang T, Bird S (2011) The interleukins of fish. Dev Comp Immunol 35(12):1336–1345

    Article  CAS  PubMed  Google Scholar 

  • Shamsuzzaman MM, Mazumder SK, Siddique MA, Miah MN (2012) Microbial quality of hilsa shad (Tenualosa ilisha) at different stages of processing. J Bangladesh Agric Univ 9(2):339–344

    Article  Google Scholar 

  • Singh A, Sood N, Chauhan UK, Mohindra V (2012) EST-based identification of immune-relevant genes from spleen of Indian catfish, Clarias batrachus (Linnaeus, 1758). Gene 502(1):53–59

    Article  CAS  PubMed  Google Scholar 

  • Swierzko AS, Szala A, Sawicki S, Szemraj J, Sniadecki M, Sokolowska A, Kaluzynski A, Wydra D, Cedzynski M (2014) Mannose-Binding Lectin (MBL) and MBL-associated serine protease-2 (MASP-2) in women with malignant and benign ovarian tumours. Cancer Immunol Immunother 63(11):1129–1140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terova G, Rimoldi S, Chini V, Gornati R, Bernardini G, Saroglia M (2007) Cloning and expression analysis of insulin-like growth factor I and II in liver and muscle of sea bass (Dicentrarchus labrax, L.) during long-term fasting and refeeding. J Fish Biol 70(sb):219–233

    Article  CAS  Google Scholar 

  • The Gene Ontology Consortium (2000) Nature America Inc., http://genetics.nature.com

  • Thorpe C, Kim JJ (1995) Structure and mechanism of action of the acyl-CoA dehydrogenases. FASEB J 9(9):718–725

    Article  CAS  PubMed  Google Scholar 

  • Wang X, da Mota SR, Liu R, Moore CE, Xie J, Lanucara F, Agarwala U, dit Ruys SP, Vertommen D, Rider MH, Eyers CE (2014) Eukaryotic elongation factor 2 kinase activity is controlled by multiple inputs from oncogenic signaling. Mol Cell Biol 34(22):4088–4103

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu K, Huang C, Shi X, Chen F, Xu YH, Pan YX, Luo Z, Liu X (2016) Role and mechanism of the AMPK pathway in waterborne Zn exposure influencing the hepatic energy metabolism of Synechogobius hasta. Sci Rep 6:38716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu FF, Zhang YB, Liu TK, Liu Y, Sun F, Jiang J, Gui JF (2010) Fish virus-induced interferon exerts antiviral function through Stat1 pathway. Mol Immunol 47(14):2330–2341

    Article  CAS  PubMed  Google Scholar 

  • Zapata A, Amemiya CT (2000) Phylogeny of lower vertebrates and their immunological structures. In Pasquier LD, Litman GW (eds) Origin and evolution of the vertebrate immune system, Springer, Berlin, pp 67–107

    Chapter  Google Scholar 

  • Zeng L, Liu B, Wu CW, Lei JL, Xu MY, Zhu AY, Zhang JS, Hong WS (2016) Molecular characterization and expression analysis of AMPK α subunit isoform genes from Scophthalmus maximus responding to salinity stress. Fish Physiol Biochem 42(6):1595–1607

    Article  CAS  PubMed  Google Scholar 

  • Zou G, Zhu Y, Liang H, Li Z (2015) Association of pituitary adenylate cyclase-activating polypeptide and myogenic factor 6 genes with growth traits in Nile tilapia (Oreochromis niloticus). Aquac Int 23(5):1217–1225

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was undertaken under ICAR-National Agricultural Science Fund (NASF) sponsored consortium project code: CN No. 6932 (Reg.No. WQ-3023) and financial support by ICAR-NASF is duly acknowledged. The authors thankfully acknowledge the research facilities extended by Director, ICAR-NBFGR for this work.

Author information

Author notes

  1. J. K. Jena

    Present address: Division of Fisheries Science, Indian Council of Agricultural Research (ICAR), Krishi Anusandhan Bhawan - II, New Delhi, 110 012, India

Authors and Affiliations

  1. ICAR- National Bureau of Fish Genetic Resources (NBFGR), Canal Ring Road, P. O. Dilkusha, Lucknow, Uttar Pradesh, 226002, India

    B. K. Divya, Vindhya Mohindra, Rajeev K. Singh, Prabhaker Yadav, Prachi Masih & J. K. Jena

Authors
  1. B. K. Divya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vindhya Mohindra
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rajeev K. Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Prabhaker Yadav
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Prachi Masih
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. K. Jena
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vindhya Mohindra.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1005 KB)

Supplementary material 2 (DOCX 44 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Divya, B.K., Mohindra, V., Singh, R.K. et al. Muscle transcriptome resource for growth, lipid metabolism and immune system in Hilsa shad, Tenualosa ilisha. Genes Genom 41, 1–15 (2019). https://doi.org/10.1007/s13258-018-0732-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-018-0732-y

Keywords

Search

Navigation