Skip to main content
Log in

The spatiotemporal expression pattern of trypsinogen and bile salt-activated lipase during the larval development of red porgy (Pagrus pagrus, Pisces, Sparidae)

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The fish larval stage is a critical step since only those specimens that survive will reach the adult stage in future. Knowledge related to fish larval nutritional requirements and digestive enzymes capacity is still scarce, although necessary to obtain satisfactory survival and growth rates. Trypsinogen is the precursor of trypsin, the main proteolytic enzyme acting during the early larval stage. Bile salt-activated lipase (BAL) is a multi-substrate digestive enzyme that hydrolyzes carboxyl ester bonds of acylglycerols, cholesterol esters and fat-soluble vitamin esters. The goal of this study was to determine the pattern of trypsinogen and BAL expression during larval development in red porgy (Pagrus pagrus, Pisces, Sparidae), reared under standard conditions to provide the basis for future experiments testing the possible transcriptional regulation for this enzyme under different nutritional conditions. Thus, partial cDNAs for trypsinogen and BAL from red porgy were isolated. The putative aminoacid sequences obtained for both precursors showed around 80% identity to other fish sequences from GenBank database. Trypsinogen and BAL were expressed from hatching and specifically located in the exocrine pancreas, revealed by in situ hybridization. The present study shows that this species is being prepared for protein and lipid digestion before exogenous feeding starts, exhibiting an ontogenetically programmed pattern for trypsinogen and BAL expression during the yolk-sac stage.

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

Access this article

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

Similar content being viewed by others

References

  • Bolasina S, Pérez A, Yamashita Y (2006) Digestive enzyme activity during ontogenetic development and effect of starvation in Japanese flounder, Paralichthys olivaceus. Aquaculture 252:503–515

    Article  CAS  Google Scholar 

  • Cahu CL, Zambonino-Infante JL, Barbosa V (2003) Effect of dietary phospholipid level and phospholipid/neutral lipid ratio on development of sea bass (Dicentrarchus labrax) fed compound diet. Br J Nutr 90:21–28

    Article  PubMed  CAS  Google Scholar 

  • Chakrabarti N, Gani MA, Chaki KK, Sur R, Misra KK (1995) Digestive enzymes in 11 freshwater teleost fish species in relation to food habit and niche segregation. Comp Biochem Physiol 112A:167–177

    Article  CAS  Google Scholar 

  • Chakrabarti N, Rathore RM, Mittal P, Kumar S (2006) Functional changes in digestive enzymes and characterization of proteases of silver carp (♂) and bighead carp (♀) hybrid, during early ontogeny. Aquaculture 253:694–702

    Article  CAS  Google Scholar 

  • Darias MJ, Murray HM, Martínez-Rodríguez G, Cárdenas S, Yúfera M (2005a) Gene expression of pepsinogen during the larval development of red porgy (Pagrus pagrus). Aquaculture 248:245–252

    Article  CAS  Google Scholar 

  • Darias MJ, Murray HM, Gallant JW, Douglas SE, Yúfera M, Martínez-Rodríguez G (2005b) Differential expression of digestive enzyme precursors in yolk-sac, fed and unfed larvae of Pagrus pagrus. Eur Aquac Soc Spec Publ 36:115–118

    Google Scholar 

  • Darias MJ, Murray HM, Gallant JW, Astola A, Douglas SE, Yúfera M, Martínez-Rodríguez G (2006) Characterization of a partial α-amylase clone from red porgy (Pagrus pagrus): expression during larval development. Comp Biochem Physiol Part B 143:209–218

    Article  CAS  Google Scholar 

  • Diaz JP, Mani-Ponset L, Blasco C, Connes R (2002) Cytological detection of the main phases of lipid metabolism during early post-embryonic development in three teleost species: Dicentrarchus labrax, Sparus aurata and Stizostedion lucioperca. Aquat Living Resour 15:169–178

    Article  Google Scholar 

  • Dhont J, Van Stappen G (2003) Biology, tank production and nutritional value of Artemia. In: Stottrup JG, Mc Envoy LA (eds) Live feeds in marine aquaculture. Blackwell, Oxford, pp 65–121

    Google Scholar 

  • Douglas SE, Gallant JW (1998) Isolation of cDNAs for trypsinogen from the winter flounder, Pleuronectes americanus. J Mar Biotechnol 6:214–219

    PubMed  Google Scholar 

  • García-Gasca A, Galaviz MA, Gutiérrez JN, García-Ortega A (2006) Development of the digestive tract, trypsin activity and gene expression in eggs and larvae of the bullseye puffer fish Sphoeroides annulatus. Aquaculture 251:366–376

    Article  Google Scholar 

  • Gjellesvik DR, Lombardo D, Walter BT (1992) Pancreatic bile salt dependent lipase from cod (Gadus morhua): purification and properties. Biochim Biophys Acta 1124:123–134

    PubMed  CAS  Google Scholar 

  • Gjellesvik DR, Lorens JB, Male R (1994) Pancreatic caboxylester lipase from Atlantic Salmon (Salmo salar): cDNA sequence and computer-assisted modelling of tertiary structure. Eur J Biochem 226:603–612

    Article  PubMed  CAS  Google Scholar 

  • Gudmundsdottir A, Gudmundsdottir E, Oskarsson S, Bjarnason JB, Eakin AK, Craik CS (1993) Isolation and characterization of cDNAs from Atlantic cod encoding two different forms of trypsinogen. Eur J Biochem 217:1091–1097

    Article  PubMed  CAS  Google Scholar 

  • Hamlin HJ, Hunt von Herbing I, Kling LJ (2000) Histological and morphological evaluations of the digestive tract and associated organs of haddock throughout post-hatching ontogeny. J Fish Biol 57:716–732

    Article  Google Scholar 

  • Hernández-Cruz CM, Salhi M, Bessonart M, Izquierdo MS, González MM, Hernández-Palacios H (1999) Rearing techniques for red porgy (Pagrus pagrus) during larval development. Aquaculture 179:489–497

    Article  Google Scholar 

  • Hjelmeland K, Pedersen BH, Nilssen EM (1988) Trypsin content in intestines of herring larvae, Clupea harengus, ingesting inert polystyrene spheres or live crustacean prey. Mar Biol 98:331–335

    Article  CAS  Google Scholar 

  • Hoehne-Reitan K, Kjørsvik E, Gjellesvik DR (2001) Development of bile salt-dependent lipase in larval turbot. J Fish Biol 58:737–745

    Article  CAS  Google Scholar 

  • Jørgensen L (1985) Carbon and nitrogen utilization in developing eggs and larvae of cod (Gadus morhua L.) and variation among different parents. Fish Res 3:337–342

    Article  Google Scholar 

  • Kurowawa T, Suzuki T, Ohta H, Kagawa H, Tanaka H, Unuma T (2002) Expression of pancreatic enzyme genes during the early larval stage of Japanese eel Anguilla japonica. Fisheries Sci 68:736–744

    Article  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 132A:913–919

    CAS  Google Scholar 

  • Lubzens E, Zmora O (2003) Production and nutritional value of rotifers. In: Stottrup JG, Mc Envoy LA (eds) Live feeds in marine aquaculture. Blackwell, Oxford, pp 17–52

    Google Scholar 

  • Male R, Lorens JB, Smalas AO, Torrissen KR (1995) Molecular cloning and characterization of anionic and cationic variants of trypsin from Atlantic salmon. Eur J Biochem 232:237–244

    Article  Google Scholar 

  • Mihelakakis A, Yoshimatsu T, Tsolkas C (2001) Spawning in captivity and early life history of cultured red porgy, Pagrus pagrus. Aquaculture 199:333–352

    Article  Google Scholar 

  • Morais S, Cahu C, Zambonino-Infante JL, Robin J, Rønnestad I, Dinis MT, Conceição LEC (2004) Dietary TAG source and level affect performance and lipase expression in larval sea bass (Dicentrarchus labrax). Lipids 39:449–458

    Article  PubMed  CAS  Google Scholar 

  • Murray HM, Douglas SE, Gallant JW, Pérez-Casanova JC, Johnson SC (2003) Ontogeny of lipase expression in winter flounder, Pseuodopleuronectes americanus. J Fish Biol 62:816–833

    Article  CAS  Google Scholar 

  • Murray HM, Pérez-Casanova JC, Gallant JW, Johnson SC, Douglas SE (2004) Trypsinogen expression during the development of the exocrine pancreas in winter flounder (Pseudopleuronectes americanus). Comp Biochem Physiol Part A 138:53–59

    Article  CAS  Google Scholar 

  • Oku H, Koizumi N, Okumura T, Kobayashi T, Umino T (2006) Molecular characterization of lipoprotein lipase, hepatic lipase and pancreatic lipase genes: effects of fasting and refeeding on their gene expression in red sea bream Pagrus major. Comp Biochem Physiol Part B 145:168–178

    Article  Google Scholar 

  • Olsen RE, Henderson RJ, Sountama J, Hemre G -I, Ringø E, Melle W, Tocher DR (2004) Atlantic salmon, Salmo salar, utilizes was esters-rich oil from Calanus finmarchicus effectively. Aquaculture 240:433–449

    Article  CAS  Google Scholar 

  • Oozeki Y, Bailey KM (1995) Ontogenetic development of digestive enzyme activities in larval walleye pollock, Theragra chalcogramma. Mar Biol 122:177–186

    CAS  Google Scholar 

  • Ortiz-Delgado JB, Darias MJ, Cañavate JP, Yúfera M, Sarasquete C (2003) Organogenesis of the digestive tract in the white seabream, Diplodus sargus. Histological and histochemical approaches. Histol Histopathol 18:1141–1154

    PubMed  CAS  Google Scholar 

  • Patton JS, Warner TG, Benson AA (1977) Partial characterization of the bile-salt-dependent triacylglycerol lipase from the leopard shark pancreas. Biochim Biophys Acta 486:322–330

    PubMed  CAS  Google Scholar 

  • Péres A, Zambonino-Infante JL, Cahu C (1998) Dietary regulation of activities and mRNA levels of trypsin and amylase in sea bass (Dicentrarchus labrax) larvae. Fish Physiol Biochem 19:145–152

    Article  Google Scholar 

  • Pérez-Casanova JC, Murray HM, Gallant JW, Ross NW, Douglas SE, Johnson SC (2004) Bile-salt activated lipase expression during larval development in the haddock (Melanogrammus aeglefinus). Aquaculture 235:601–617

    Article  Google Scholar 

  • Pérez-Casanova JC, Murray HM, Gallant JW, Ross NW, Douglas SE, Johnson SC (2006) Development of the digestive capacity in larvae of haddock (Melanogrammus aeglefinus) and Atlantic cod (Gadus morhua). Aquaculture 251:377–401

    Article  Google Scholar 

  • Rainuzzo JR, Reitan V, Olsen Y (1997) The significance of lipids at early stages of marine fish: a review. Aquaculture 155:103–115

    Article  CAS  Google Scholar 

  • Rathore RM, Kumar S, Chakrabarti R (2005) Digestive enzyme patterns and evaluation of protease classes in Catla catla (Family: Cyprinidae) during early development stages. Comp Biochem Physiol 142B:98–106

    CAS  Google Scholar 

  • Ribeiro L, Zambonino-Infante JL, Cahu C, Dinis MT (1999) Development of digestive enzymes in larvae of Solea senegalensis, Kaup 1858. Aquaculture 179:465–473

    Article  CAS  Google Scholar 

  • Roo FJ, Socorro J, Izquierdo MS, Caballero MJ, Hernández-Cruz CM, Fernández A, Hernández-Palacios H (1999) Development of red porgy Pagrus pagrus visual system in relation with changes in the digestive tract and larval feeding habits. Aquaculture 179:499–512

    Article  Google Scholar 

  • Sarasquete MC, Polo A, Yúfera M (1995) Histology and histochemistry of the development of the digestive system of larval gilthead seabream, Sparus aurata L. Aquaculture 130:79–92

    Article  Google Scholar 

  • Srivastava AS, Kurokawa T, Suzuki T (2002) mRNA expression of pancreatic enzyme precursors and estimation of protein digestibility in first feeding larvae of the Japanese flounder, Paralichtys olivaceus. Comp Biochem Physiol Part A 132:629–635

    Article  Google Scholar 

  • Suzuki T, Srivastava AS, Kurokawa T (2002) cDNA cloning and phylogenetic analysis of pancreatic serine proteases from Japanese flounder, Paralichtys olivaceus. Comp Biochem Physiol Part B 131:63–70

    Article  Google Scholar 

  • Wang C, Hartsuck JA (1993) Bile salt-activated lipase. A multiple function lipolytic enzyme. Biochim Biophys Acta 1166:1–19

    PubMed  CAS  Google Scholar 

  • Yúfera M (2001) Studies on Brachionus (Rotifera): an example of interaction between fundamental and applied research. Hydrobiologia 446/447:383–392

    Article  Google Scholar 

  • Zambonino-Infante JL, Cahu C (1999) High dietary lipid levels enhance digestive tract maturation and improve Dicentrarchus labrax larval development. J Nutr 129:1195–1200

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr P. Pousaõ from INIAP/IPIMAR (Olhão, Portugal) for supplying the biological material used in this work, and E. García-Ramos Neto and J. A. Miquel for their helpful technical assistance. This work was supported by the Comisión Interministerial de Ciencia y Tecnología, Spain (CICYT Proyect AGL2000-0697-C02-01), to MY. MJD was supported by a FPI fellowship from MCYT, Spain (FP2000-5265). All experiments carried out in this study comply with de current Spanish ethical laws.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to María J. Darias.

Additional information

Communicated by S.A. Poulet.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Darias, M.J., Murray, H.M., Gallant, J.W. et al. The spatiotemporal expression pattern of trypsinogen and bile salt-activated lipase during the larval development of red porgy (Pagrus pagrus, Pisces, Sparidae). Mar Biol 152, 109–118 (2007). https://doi.org/10.1007/s00227-007-0663-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-007-0663-7

Keywords

Navigation