Skip to main content

Advertisement

SpringerLink
Log in

Differential Growth-Related Gene Expression in Abalone (Haliotis midae)

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

The slow growth rate of Haliotis midae impedes the optimal commercial production of this most profitable South African aquaculture species. To date, no comprehensive effort has been made to identify genes associated with growth variation in farmed H. midae. The aim of this study was therefore to investigate growth variation in H. midae and to identify and quantify the expression of selected growth-related genes. Towards this aim, molecular methodologies and cell cultures were combined as a time-efficient and economical way of studying abalone transcriptomics and cell biology. Modern Illumina sequencing-by-synthesis technology and subsequent sequence annotation were used to elucidate differential gene expression between two sibling groups of abalone demonstrating significant growth variation. The expression of selected target genes involved in growth was subsequently analysed by quantitative real-time PCR (qPCR). Fast- and slow-growing abalone and in vitro primary haemocyte cultures treated with different growth-stimulating factors were used. The results obtained from transcriptome analysis and qPCR revealed significant differences in gene expression between large and small abalone, and between treated and untreated haemocyte cell cultures. Throughout in vivo and in vitro qPCR experiments, the up-regulation of genes involved in the insulin signalling pathway suggests that insulin may be involved in enhanced growth rate for various H. midae tissues.

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

Similar content being viewed by others

References

  • Adams PS (2006) Data analysis and reporting. In: Dorak MT (ed) Real-time PCR. Taylor and Francis Group, Abingdon, pp 39–62

    Google Scholar 

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29

    Article  PubMed  CAS  Google Scholar 

  • Baranski M, Loughnan S, Austin C, Robinson N (2006) Linkage maps of microsatellite DNA markers for the blacklip abalone Haliotis rubra. Anim Genet 37:563–570

    Article  PubMed  CAS  Google Scholar 

  • Baranski M, Rourke M, Loughnan S, Hayes B, Austin C, Robinson N (2008) Detection of QTL for growth rate in the blacklip abalone (Haliotis rubra Leach) using selective DNA pooling. Anim Genet 39:606–614

    Article  PubMed  CAS  Google Scholar 

  • Beaumont AR, Hoare K (2003) Biotechnology and genetics in fisheries and aquaculture, 1st edn. Blackwell Science, Kent, p 158

    Book  Google Scholar 

  • Bester AE, Slabbert R, D'Amato ME (2004) Isolation and characterization of microsatellite markers in the South African abalone (Haliotis midae). Mol Ecol Notes 4:618–619

    Article  CAS  Google Scholar 

  • Bester AE, Roodt-Wilding R, Whitaker HA (2008) Discovery and evaluation of single nucleotide polymorphisms (SNPs) for Haliotis midae: a targeted EST approach. Anim Genet 39:321–324

    Article  PubMed  CAS  Google Scholar 

  • Blaxter M (2010) MolluscDB: A web interface for the MolluscDB Partigene database. Homepage of the University of Edinburgh. http://xyala.cap.ed.ac.uk/NeglectedGenomes/MOLLUSCA/. Accessed 28 May 2010

  • Britz PJ, Lee B, Botes L (2009) AISA 2009 Aquaculture Benchmarking Survey: Primary Production and Markets. A report for the Aquaculture Institute of South Africa and Swisscontact, produced by Enviro-Fish Africa (Pty.) Ltd., 130 pp

  • Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

    Article  PubMed  CAS  Google Scholar 

  • Carninci P, Nakamura M, Sato K, Hayashizaki Y, Brownstein MJ (2002) Cytoplasmic RNA extraction from fresh and frozen mammalian tissues. Biotechniques 33:306–309

    PubMed  CAS  Google Scholar 

  • Chen SN, Wen CM (1999) Establishment of cell lines derived from oyster, Crassostrea gigas Thunberg and hard clam. Meretrix lusoria Röding. Methods Cell Sci 21:183–192

    Article  PubMed  CAS  Google Scholar 

  • Clark MS, Thorne MAS, Vieira FA, Cardoso JCR, Power DM, Peck LS (2010) Insights into shell deposition in the Antarctic bivalve Laternula elliptica: gene discovery in the mantle transcriptome using 454 pyrosequencing. BMC Genomics 11:362

    Article  PubMed  Google Scholar 

  • Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  PubMed  CAS  Google Scholar 

  • Corbett Research (2006) Rotor-Gene 6000 operator manual 1.7.87. Corbett Research, Australia

  • De Cássia Ruy P, Neto AZ, Ruiz JC, De Oliveira GC, Aguiar E, De Oliveira FS, Cipriano DAS (2010) Functional analysis of Biomphalaria glabrata ESTs. Homepage of Genomics and Computational Biology Group, Fiocruz. http://www.snaildb.org/. Accessed 27 May 2010

  • Domart-Coulon I, Doumenc D, Auzoux-Bordenave S, Fichant YL (1994) Identification of media supplements that improve the viability of primarily cell cultures of Crassostrea gigas oysters. Cytotechnology 16:109–120

    Article  PubMed  CAS  Google Scholar 

  • Dos Reis Falcão V, Tonon AP, Oliveira MC, Colepicolo P (2008) RNA Isolation method for polysaccharide rich algae: agar producing Gracilaria tenuistipitata (Rhodophyta). J Appl Phycol 20:9–12

    Article  Google Scholar 

  • Elliott NG (2000) Genetic improvement programmes in abalone: what is the future? Aquac Res 31:51–59

    Article  Google Scholar 

  • Flynn A, Proud CG (1996) Insulin-stimulated phosphorylation of initiation factor 4E is mediated by the MAP kinase pathway. FEBS Lett 389:162–166

    Article  PubMed  CAS  Google Scholar 

  • Franchini P, Van der Merwe M, Roodt-Wilding R (2011) Transcriptome characterization of the South African abalone Haliotis midae using sequencing-by-synthesis. BMC Research Notes 4:59

    Article  PubMed  CAS  Google Scholar 

  • Gagnaire B, Thomas-Guyon H, Renault T (2004) In vitro effects of cadmium and mercury on Pacific oyster, Crassostrea gigas (Thunberg), haemocytes. Fish Shellfish Immunol 16:501–512

    Article  PubMed  CAS  Google Scholar 

  • Gagnaire B, Frouin H, Moreau K, Thomas-Guyon H, Renault T (2006) Effects of temperature and salinity on haemocyte activities of the Pacific oyster, Crassostrea gigas (Thunberg). Fish Shellfish Immunol 20:536–547

    Article  PubMed  CAS  Google Scholar 

  • Gambacurta A, Piro AM, Ascoli F (1993) Cooperative homodimeric hemoglobin from Scapharca inaequivalvis cDNA cloning and expression of the fully functional protein in E. coli. FEBS Lett 330:90–94

    Article  PubMed  CAS  Google Scholar 

  • Giard W, Lebel J, Boucaud-Camou E, Favrel P (1998) Effects of vertebrate growth factors on digestive gland cells from the mollusc Pecten maximus L.: an in vitro study. J Comp Physiol B 168:81–86

    Article  PubMed  CAS  Google Scholar 

  • Gricourt L, Bonnec G, Boujard D, Mathieu M, Kellner K (2003) Insulin-like system and growth regulation in the Pacific oyster Crassostrea gigas: hrIGF-1 effect on protein synthesis of mantle edge cells and expression of an homologous insulin receptor-related receptor. Gen Comp Endocrinol 134:44–56

    Article  PubMed  CAS  Google Scholar 

  • Guo YJ, Ribeiro JMC, Anderson JM, Bour S (2009) dCAS: a desktop application for cDNA sequence annotation. Bioinformatics 25:1195–1196

    Article  PubMed  CAS  Google Scholar 

  • Hahn KO (1989) CRC handbook of culture of abalone and other marine gastropods, 1st edn. CRC, Florida, 348 pp

    Google Scholar 

  • Haruta T, Uno T, Kawahara J, Takano A, Egawa K, Sharma PM, Olefsky JM, Kobayashi M (2000) A rapamycin-sensitive pathway down-regulates insulin signaling via phosphorylation and proteasomal degradation of insulin receptor substrate-1. Mol Endocrinol 14:783–794

    Article  PubMed  CAS  Google Scholar 

  • Hayes B, Baranski M, Goddard ME, Robinson N (2007) Optimisation of marker assisted selection for abalone breeding programs. Aquaculture 265:61–69

    Article  Google Scholar 

  • Humphries JE, Yoshino TP (2003) Cellular receptors and signal transduction in molluscan hemocytes: connections with the innate immune system of vertebrates. Integr Comp Biol 43:305–312

    Article  PubMed  CAS  Google Scholar 

  • ICES (2008) Report of the working group on the application of genetics in fisheries and mariculture (WGAGFM). Pitlochry, Scotland, 77 pp

    Google Scholar 

  • Illumina Inc. (2008) Paired-end sequencing user guide for cluster station and genome analyzer. San Diego, USA

  • Kal AJ, Van Zonneveld AJ, Benes V, Van den Berg M, Koerkamp MG, Albermann K, Strack N, Ruijter JM, Richter A, Dujon B, Ansorge W, Tabak HF (1999) Dynamics of gene expression revealed by comparison of serial analysis of gene expression transcript profiles from yeast grown on two different carbon sources. Mol Biol Cell 10:1859–1872

    PubMed  CAS  Google Scholar 

  • Kanehisa Laboratories (2010) MAPK signaling pathway—Homo sapiens (human). Homepage of Kanehisa Laboratories. http://www.genome.jp/kegg/pathway/hsa/hsa04010.html. Accessed 17 June 2010

  • Kanehisa M, Goto S (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28:27–30

    Article  PubMed  CAS  Google Scholar 

  • Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, Kawashima S, Katayama T, Araki M, Hirakawa M (2006) From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34:D354–D357

    Article  PubMed  CAS  Google Scholar 

  • Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M (2010) KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res 38:D355–D360

    Article  PubMed  CAS  Google Scholar 

  • Lande R, Thompson R (1990) Efficiency of marker-assisted selection in the improvement of quantitative traits. Genetics 124:743–756

    PubMed  CAS  Google Scholar 

  • Lawler J, Duquette M, Whittaker CA, Adams JC, McHenry K, DeSimone DW (1993) Identification and characterization of thrombospondin-4, a new member of the thrombospondin gene family. J Cell Biol 120:1059–1067

    Article  PubMed  CAS  Google Scholar 

  • Lebel JM, Giard W, Favrel P, Boucaud-Camou E (1996) Effects of different vertebrate growth factors on primary cultures of hemocytes from the gastropod mollusc, Haliotis tuberculata. Biol Cell 86:67–72

    Article  PubMed  CAS  Google Scholar 

  • Li X (2008) Abalone aquaculture subprogram: Selective breeding of farmed abalone to enhance growth rates (II). FRDC Final Report. 2001/254. West Beach, South Australia, South Australian Research and Development Institute (SARDI)

  • Liu X, Liu X, Zhang G (2007) Identification of quantitative trait loci for growth-related traits in the Pacific abalone Haliotis discus hannai Ino. Aquac Res 38:789–797

    Article  CAS  Google Scholar 

  • Lucas T (2007) Investigating genetic and molecular aspects of growth of the tropical abalone Haliotis asinina. Unpublished PhD dissertation, University of Queensland, Queensland, Australia

  • Machado CR, Garofalo MAR, Roselino JES, Kettlehut IC, Migliorini RH (1988) Effects of starvation, refeeding, and insulin on energy-linked metabolic processes in catfish (Rhamdia hilarii) adapted to a carbohydrate-rich diet. Gen Comp Endocrinol 71:429–437

    Article  PubMed  CAS  Google Scholar 

  • Marin F, Luquet G (2004) Molluscan shell proteins. C R Palevol 3:469–492

    Article  Google Scholar 

  • Meuwissen THE, Goddard ME (1996) The use of marker haplotypes in animal breeding schemes. Genet Sel Evol 28:161–176

    Article  Google Scholar 

  • Montserrat N, Gómez-Requeni P, Bellini G, Capilla E, Pérez-Sánchez J, Navarro I, Gutiérrez J (2007) Distinct role of insulin and IGF-I and its receptors in white skeletal muscle during the compensatory growth of gilthead sea bream (Sparus aurata). Aquaculture 267:188–198

    Article  CAS  Google Scholar 

  • Moroz LL, Edwards JR, Puthanveettil SV, Kohn AB, Ha T, Heyland A, Knudsen B, Sahni A, Yu F, Liu L, Jezzini S, Lovell P, Iannucculli W, Chen M, Nguyen T, Sheng H, Shaw R, Kalachikov S, Panchin YV, Farmerie W, Russo JJ, Ju J, Kandel ER (2006) Neuronal transcriptome of Aplysia: neuronal compartments and circuitry. Cell 127:1453–1467

    Article  PubMed  CAS  Google Scholar 

  • Mottin E, Caplat C, Mahaut M, Costil K, Barillier D, Lebel J, Serpentini A (2010) Effect of in vitro exposure to zinc on immunological parameters of haemocytes from the marine gastropod Haliotis tuberculata. Fish Shellfish Immunol 29:846–853

    Article  PubMed  CAS  Google Scholar 

  • Nanba R, Fujita N, Nagata S (2010) Structure and expression of myelin basic protein gene products in Xenopus laevis. Gene 459:32–38

    Article  PubMed  CAS  Google Scholar 

  • Nogare DED, Arguello A, Sazer S, Lane ME (2007) Zebrafish cdc25a is expressed during early development and limiting for post-blastoderm cell cycle progression. Dev Dyn 236:3427–3435

    Article  PubMed  Google Scholar 

  • Pfaffl MW, Corbett Research (2008) Relative expression software tool. Australia

  • Pyronnet S, Imataka H, Gingras AC, Fukunaga R, Hunter T, Sonenberg N (1999) Human eukaryotic translation initiation factor 4G (eIF4G) recruits Mnk1 to phosphorylate eIF4E. EMBO J 18:270–279

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen R (2001) Quantification on the LightCycler. In: Meuer S, Wittwer C, Nakagawara K (eds) Rapid cycle real-time PCR: methods and applications. Springer, Heidelberg, pp 21–34

    Google Scholar 

  • Reinecke M (2010) Influences of the environment on the endocrine and paracrine fish growth hormone—insulin-like growth factor-I system. J Fish Biol 76:1233–1254

    Article  PubMed  CAS  Google Scholar 

  • Rhode C, Slabbert R, Roodt-Wilding R (2008) Microsatellite flanking regions: a SNP mine in South African abalone (Haliotis midae). Anim Genet 39:328–332

    Article  Google Scholar 

  • Ross G, Dyer JR, Castellucci VF, Sossin WF (2006) Mnk is a negative regulator of cap-dependent translation in Aplysia neurons. J Neurochem 97:79–91

    Article  PubMed  CAS  Google Scholar 

  • Serpentini A, Ghayor C, Poncet JM, Hebert V, Galera P, Pujol JP, Boucaud-Camou E, Lebel JM (2000) Collagen study and regulation of the de novo synthesis by IGF-I in hemocytes from the gastropod mollusc, Haliotis tuberculata. J Exp Zool 287:275–284

    Article  PubMed  CAS  Google Scholar 

  • Shipley GL (2006) An introduction to real-time PCR. In: Dorak MT (ed) Real-time PCR. Taylor and Francis Group, Abingdon, pp 1–31

    Google Scholar 

  • Slabbert R, Ruivo NR, Van Den Berg NC, Lizamore DL, Roodt-Wilding R (2008) Isolation and characterization of 63 microsatellite loci for the abalone, Haliotis midae. J World Aquacult Soc 39:429–435

    Article  Google Scholar 

  • Slabbert R, Hepple J, Venter A, Nel S, Swart L, Van den Berg NC, Roodt-Wilding R (2010) Isolation and segregation of 44 microsatellite loci in the South African abalone Haliotis midae L. Anim Genet 41:332–336

    Article  PubMed  CAS  Google Scholar 

  • Sonesson AK (2007) Within-family marker-assisted selection for aquaculture species. Genet Sel Evol 39:301–317

    Article  PubMed  Google Scholar 

  • Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov S, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:41–54

    Article  PubMed  Google Scholar 

  • Taylor S, Wakem M, Dijkman G, Alsarraj M, Nguyen M (2010) A practical approach to RT-qPCR—publishing data that conform to the MIQE guidelines. Methods 50:S1–S5

    Article  PubMed  CAS  Google Scholar 

  • DOE JGI (U.S. Department of Energy Joint Genome Institute) (2007) Lottia gigantea v1.0. Homepage of U.S. Department of Energy Joint Genome Institute (DOE JGI)]. http://genome.jgi-psf.org/Lotgi1/Lotgi1.home.html. Accessed 27 May 2010

  • Urry LA, Whittaker CA, Duquette M, Lawler J, DeSimone DW (1998) Thrombospondins in early Xenopus embryos: dynamic patterns of expression suggest diverse roles in nervous system, notochord, and muscle development. Dev Dyn 211:390–407

    Article  PubMed  CAS  Google Scholar 

  • Van der Merwe M (2010) Growth-related gene expression in Haliotis midae. Unpublished PhD dissertation, Stellenbosch University, Stellenbosch, South Africa

  • Van der Merwe M, Auzoux-Bordenave S, Niesler C, Roodt-Wilding R (2010) Investigating the establishment of primary cell culture from different abalone (Haliotis midae) tissues. Cytotechnology 62:265–277

    Article  PubMed  Google Scholar 

  • Villesen P (2009). Welcome to FaBox (1.35)—an online fasta sequence toolbox. Homepage of Aarhus University, Denmark. http://www.birc.au.dk/fabox. Accessed 27 May 2010

  • Wan Q, Whang I, Lee J (2008) Molecular characterization of mu class glutathione-S-transferase from disk abalone (Haliotis discus discus), a potential biomarker of endocrine-disrupting chemicals. Comp Biochem Physiol B 150:187–199

    Article  PubMed  Google Scholar 

  • Wang S, Sha Z, Sonstegard TS, Liu H, Xu P, Somridhivej B, Peatman E, Kucuktas H, Liu Z (2008) Quality assessment parameters for EST-derived SNPs from catfish. BMC Genomics 9:450–461

    Article  PubMed  Google Scholar 

  • Waskiewicz AJ, Flynn A, Proud CG, Cooper JA (1997) Mitogen-activated protein kinases activate the serine/threonine kinases Mnk1 and Mnk2. EMBO J 16:1909–1920

    Article  PubMed  CAS  Google Scholar 

  • Weiss IM, Göhring W, Fritz M, Mann K (2001) Perlustrin, a Haliotis laevigata (Abalone) nacre protein, is homologous to the insulin-like growth factor binding protein N-terminal module of vertebrates. Biochem Biophys Res Commun 285:244–249

    Article  PubMed  CAS  Google Scholar 

  • White YAR, Kyle JT, Wood AW (2009) Targeted gene knockdown in zebrafish reveals distinct intraembryonic functions for insulin-like growth factor II signaling. Endocrinology 150:4366–4375

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by a research grant from the NRF Innovation Fund and Industry partners (Irvin & Johnson Limited, Abagold (Pty) Ltd, Aquafarm Development Company (Pty) Ltd., HIK Abalone (Pty) Ltd. and Roman Bay Sea Farm (Pty) Ltd.). Stellenbosch University is thanked for facilities provided and Roman Bay Sea Farm and HIK Abalone for providing samples.

Author information

Authors and Affiliations

  1. Molecular Aquatic Research Group, Department of Genetics, Stellenbosch University, Private Bag X1, Matieland, 7602, South Africa

    Mathilde van der Merwe, Paolo Franchini & Rouvay Roodt-Wilding

Authors
  1. Mathilde van der Merwe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paolo Franchini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rouvay Roodt-Wilding
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rouvay Roodt-Wilding.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 937 kb)

ESM 2

(XLS 276 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

van der Merwe, M., Franchini, P. & Roodt-Wilding, R. Differential Growth-Related Gene Expression in Abalone (Haliotis midae). Mar Biotechnol 13, 1125–1139 (2011). https://doi.org/10.1007/s10126-011-9376-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-011-9376-5

Keywords

Search

Navigation