Learning from Small Fry: The Zebrafish as a Genetic Model Organism for Aquaculture Fish Species

In recent years, the zebrafish has become one of the most prominent vertebrate model organisms used to study the genetics underlying development, normal body function, and disease. The growing interest in zebrafish research was paralleled by an increase in tools and methods available to study zebrafish. While zebrafish research initially centered on mutagenesis screens (forward genetics), recent years saw the establishment of reverse genetic methods (morpholino knock-down, TILLING). In addition, increasingly sophisticated protocols for generating transgenic zebrafish have been developed and microarrays are now available to characterize gene expression on a near genome-wide scale. The identification of loci underlying specific traits is aided by genetic, physical, and radiation hybrid maps of the zebrafish genome and the zebrafish genome project. As genomic resources for aquacultural species are increasingly being generated, a meaningful interaction between zebrafish and aquacultural research now appears to be possible and beneficial for both sides. In particular, research on nutrition and growth, stress, and disease resistance in the zebrafish can be expected to produce results applicable to aquacultural fish, for example, by improving husbandry and formulated feeds. Forward and reverse genetics approaches in the zebrafish, together with the known conservation of synteny between the species, offer the potential to identify and verify candidate genes for quantitative trait loci (QTLs) to be used in marker-assisted breeding. Moreover, some technologies from the zebrafish field such as TILLING may be directly transferable to aquacultural research and production.

[1]  R. Ho,et al.  Induction of muscle pioneers and floor plate is distinguished by the zebrafish no tail mutation , 1993, Cell.

[2]  S. Kolkovski.  Digestive enzymes in fish larvae and juveniles—implications and applications to formulated diets , 2001 .

[3]  A. Amsterdam,et al.  Chapter 5 Retrovirus-Mediated Insertional Mutagenesis in Zebrafish , 1998 .

[4]  R. Brooks.  Variation in female mate choice within guppy populations: population divergence, multiple ornaments and the maintenance of polymorphism. , 2002 .

[5]  M. Fishman,et al.  Cell lineage tracing in heart development. , 1999, Methods in cell biology.

[6]  Corey M. Carlson,et al.  Insertional mutagenesis in mice: new perspectives and tools , 2005, Nature Reviews Genetics.

[7]  Nancy Hopkins,et al.  Insertional mutagenesis in zebrafish rapidly identifies genes essential for early vertebrate development , 2002, Nature Genetics.

[8]  A. Amsterdam,et al.  A large-scale insertional mutagenesis screen in zebrafish. , 1999, Genes & development.

[9]  David Whitmore,et al.  E-box function in a period gene repressed by light , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[10]  S. Oppenheimer,et al.  Atlas of embryonic development , 1984 .

[11]  E. Knapik.  ENU mutagenesis in zebrafish—from genes to complex diseases , 2000, Mammalian Genome.

[12]  C. Ghittino,et al.  Emerging Pathologies in Aquaculture: Effects on Production and Food Safety , 2003, Veterinary Research Communications.

[13]  H. Mitani,et al.  Medaka as a research organism: past, present and future , 2004, Mechanisms of Development.

[14]  C. Ton,et al.  Gene expression profile of zebrafish exposed to hypoxia during development. , 2003, Physiological genomics.

[15]  A. Amsterdam,et al.  Retrovirus-mediated insertional mutagenesis in zebrafish. , 1999, Methods in cell biology.

[16]  Stephen W. Wilson,et al.  Stereotyped pathway selection by growth cones of early epiphysial neurons in the embryonic zebrafish. , 1991, Development.

[17]  V. Dzau,et al.  Construction of a zebrafish cDNA microarray: gene expression profiling of the zebrafish during development. , 2002, Biochemical and biophysical research communications.

[18]  Rajan P. Kulkarni,et al.  Quantum dots are powerful multipurpose vital labeling agents in zebrafish embryos , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[19]  C. Nüsslein-Volhard,et al.  Zebrafish (Danio rerio) Genome and Genetics , 2006 .

[20]  K. Kawakami,et al.  Identification of a functional transposase of the Tol2 element, an Ac-like element from the Japanese medaka fish, and its transposition in the zebrafish germ lineage. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[21]  A. Wargelius,et al.  Double-stranded RNA induces specific developmental defects in zebrafish embryos. , 1999, Biochemical and biophysical research communications.

[22]  S. Russell,et al.  Transposable elements as tools for genomics and genetics in Drosophila. , 2003, Briefings in functional genomics & proteomics.

[23]  J. Campos-Ortega,et al.  Use of the Gal4-UAS technique for targeted gene expression in the zebrafish , 1999, Mechanisms of Development.

[24]  J. Shih,et al.  Fate maps of the zebrafish embryo. , 1995, Current opinion in genetics & development.

[25]  M. Schartl,et al.  Medaka — a model organism from the far east , 2002, Nature Reviews Genetics.

[26]  J. Martial,et al.  Heat shock stimulation of a tilapia heat shock protein 70 promoter is mediated by a distal element. , 2001, The Biochemical journal.

[27]  Christopher P Austin,et al.  The Knockout Mouse Project , 2004, Nature Genetics.

[28]  L. Zon,et al.  Effects of lethal irradiation in zebrafish and rescue by hematopoietic cell transplantation. , 2004, Blood.

[29]  Bacterial artificial chromosome (BAC) clones and the current clone map of the zebrafish genome. , 2004, Methods in cell biology.

[30]  Wilhelm Harder,et al.  ANATOMY OF FISHES , 1976, Fishes: A Guide to Their Diversity.

[31]  S. Burgess,et al.  Transgenic zebrafish produced by retroviral infection of in vitro-cultured sperm. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[32]  S. Henikoff,et al.  High-throughput TILLING for functional genomics. , 2003, Methods in molecular biology.

[33]  J. Wittbrodt,et al.  Medaka and zebrafish, an evolutionary twin study , 2004, Mechanisms of Development.

[34]  G. Corley-Smith,et al.  Production of androgenetic zebrafish (Danio rerio). , 1996, Genetics.

[35]  A. Force,et al.  valentino: a zebrafish gene required for normal hindbrain segmentation. , 1996, Development.

[36]  Ralf Dahm,et al.  Zebrafish: A Practical Approach. Edited by C. NÜSSLEIN-VOLHARD and R. DAHM. Oxford University Press. 2002. 322 pages. ISBN 0 19 963808 X. Price £40.00 (paperback). ISBN 0 19 963809 8. Price £80.00 (hardback). , 2003 .

[37]  Edwin Cuppen,et al.  Efficient target-selected mutagenesis in zebrafish. , 2003, Genome research.

[38]  Z. Gong,et al.  Transcriptome Analysis of Zebrafish Embryogenesis Using Microarrays , 2005, PLoS genetics.

[39]  Paramvir S. Dehal,et al.  Whole-Genome Shotgun Assembly and Analysis of the Genome of Fugu rubripes , 2002, Science.

[40]  C. Tickle,et al.  Morphological Diversity: Taking the Spine out of Three-Spine Stickleback , 2004, Current Biology.

[41]  Y. Torrente,et al.  High‐efficiency gene transfer into adult fish: A new tool to study fin regeneration , 2002, Genesis.

[42]  S. Fraser,et al.  Tracing transgene expression in living zebrafish embryos. , 2001, Developmental biology.

[43]  A. Amsterdam.  Insertional mutagenesis in zebrafish , 2003, Developmental dynamics : an official publication of the American Association of Anatomists.

[44]  A. Schier,et al.  A genetic screen for mutations affecting embryogenesis in zebrafish. , 1996, Development.

[45]  G. Hannon.  RNA interference : RNA , 2002 .

[46]  S. Sivasubbu,et al.  Efficient gene delivery and gene expression in zebrafish using the Sleeping Beauty transposon. , 2003, Developmental biology.

[47]  R. Ho,et al.  Too much interference: injection of double-stranded RNA has nonspecific effects in the zebrafish embryo. , 2000, Developmental biology.

[48]  J. Postlethwait,et al.  Radiation hybrid mapping of the zebrafish genome. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[49]  R. Meyers.  Encyclopedia of molecular cell biology and molecular medicine , 2014 .

[50]  W. Shoji,et al.  Transmembrane Sema4E Guides Branchiomotor Axons to Their Targets in Zebrafish , 2003, The Journal of Neuroscience.

[51]  F. Verbeek,et al.  Transcriptome profiling of adult zebrafish at the late stage of chronic tuberculosis due to Mycobacterium marinum infection. , 2005, Molecular immunology.

[52]  Charles E. Chapple,et al.  Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype , 2004, Nature.

[53]  Tohru Suzuki,et al.  Identification of pepsinogen gene in the genome of stomachless fish, Takifugu rubripes. , 2005, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[54]  J. S. Nelson,et al.  Fishes of the world. , 1978 .

[55]  R. Ho,et al.  Commitment of cell fate in the early zebrafish embryo. , 1993, Science.

[56]  C. Kimmel,et al.  Stages of embryonic development of the zebrafish , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[57]  W. Driever,et al.  Transposition of the nematode Caenorhabditis elegans Tc3 element in the zebrafish Danio rerio , 1998, Current Biology.

[58]  Worldwide Genomic Resources for Non-Model Fish Species , 2003, Comparative and functional genomics.

[59]  홀덴 데이비드윌리암,et al.  Identification of genes , 1995 .

[60]  M. Ekker,et al.  A microsatellite genetic linkage map for zebrafish (Danio rerio) , 1998, Nature Genetics.

[61]  R. Geisler,et al.  Gene expression profiling of gilthead sea bream during early development and detection of stress-related genes by the application of cDNA microarray technology. , 2005, Physiological genomics.

[62]  T. Mizuno,et al.  Cell and tissue transplantation in zebrafish embryos. , 1999, Methods in molecular biology.

[63]  D. Grunwald,et al.  Contribution of early cells to the fate map of the zebrafish gastrula. , 1994, Science.

[64]  H. Baier,et al.  A radiation hybrid map of the zebrafish genome , 1999, Nature Genetics.

[65]  M. Kirby,et al.  Double-stranded RNA injection produces null phenotypes in zebrafish. , 2000, Developmental biology.

[66]  J. Rogers,et al.  Coping with cold: An integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[67]  B. Appelmelk,et al.  A star with stripes: zebrafish as an infection model. , 2004, Trends in microbiology.

[68]  S. Ekker,et al.  Effective targeted gene ‘knockdown’ in zebrafish , 2000, Nature Genetics.

[69]  Weiping Ma,et al.  Embryogenesis Microarray for Profiling Gene Expression Patterns during 15,000 Unique Zebrafish Est Clusters and Their Future Use in Material Supplemental , 2022 .

[70]  G. Streisinger,et al.  Production of clones of homozygous diploid zebra fish (Brachydanio rerio) , 1981, Nature.

[71]  J. Gordon,et al.  Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[72]  A. Sonesson.  POSSIBILITIES FOR MARKER-ASSISTED SELECTION IN FISH , 2003 .

[73]  J. Joly,et al.  Highly efficient zebrafish transgenesis mediated by the meganuclease I-SceI. , 2004, Methods in cell biology.

[74]  A. Amsterdam,et al.  High-Throughput Selection of Retrovirus Producer Cell Lines Leads to Markedly Improved Efficiency of Germ Line-Transmissible Insertions in Zebra Fish , 2002, Journal of Virology.

[75]  T. Becker,et al.  Large-scale enhancer detection in the zebrafish genome , 2005, Development.

[76]  Y. Kohara,et al.  Medaka genomics: a bridge between mutant phenotype and gene function , 2004, Mechanisms of Development.

[77]  R. Ho,et al.  Cell-autonomous action of zebrafish spt-1 mutation in specific mesodermal precursors , 1990, Nature.

[78]  R. Plasterk,et al.  Target-Selected Inactivation of the Zebrafish rag1 Gene , 2002, Science.

[79]  M. Westerfield,et al.  Mutations affecting skeletal muscle myofibril structure in the zebrafish. , 1990, Development.

[80]  Y. Yan,et al.  Zebrafish comparative genomics and the origins of vertebrate chromosomes. , 2000, Genome research.

[81]  M. Justice,et al.  The mutagenic action of N-ethyl-N-nitrosourea in the mouse , 2000, Mammalian Genome.

[82]  A. Fire,et al.  Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans , 1998, Nature.

[83]  A. Meng,et al.  Double-stranded RNA injection produces nonspecific defects in zebrafish. , 2001, Developmental biology.

[84]  M. Westerfield,et al.  Replication, integration and stable germ-line transmission of foreign sequences injected into early zebrafish embryos. , 1988, Development.

[85]  D. Crawford,et al.  Fish as models for environmental genomics , 2005, Nature Reviews Genetics.

[86]  Michael Brand,et al.  Keeping and raising zebrafish , 2002 .

[87]  D A Kane,et al.  The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. , 1996, Development.

[88]  Ralf Dahm,et al.  The Zebrafish as a Model Organism for Eye Development , 2004, Ophthalmic Research.