Home LiteratureArticle Details
PMID: 16132083 Published · ppublish English Journal Article

Transcriptome analysis of zebrafish embryogenesis using microarrays.

PLoS genetics ·Vol. 1 ·No. 2 ·2005-08-00 ·Pages 260-76

Mathavan S, Lee SG, Mak A, Miller LD, Murthy KR, Govindarajan KR, Tong Y, Wu YL, Lam SH, Yang H, Ruan Y, Korzh V, Gong Z, Liu ET, Lufkin T

Abstract

Zebrafish (Danio rerio) is a well-recognized model for the study of vertebrate developmental genetics, yet at the same time little is known about the transcriptional events that underlie zebrafish embryogenesis. Here we have employed microarray analysis to study the temporal activity of developmentally regulated genes during zebrafish embryogenesis. Transcriptome analysis at 12 different embryonic time points covering five different developmental stages (maternal, blastula, gastrula, segmentation, and pharyngula) revealed a highly dynamic transcriptional profile. Hierarchical clustering, stage-specific clustering, and algorithms to detect onset and peak of gene expression revealed clearly demarcated transcript clusters with maximum gene activity at distinct developmental stages as well as co-regulated expression of gene groups involved in dedicated functions such as organogenesis. Our study also revealed a previously unidentified cohort of genes that are transcribed prior to the mid-blastula transition, a time point earlier than when the zygotic genome was traditionally thought to become active. Here we provide, for the first time to our knowledge, a comprehensive list of developmentally regulated zebrafish genes and their expression profiles during embryogenesis, including novel information on the temporal expression of several thousand previously uncharacterized genes. The expression data generated from this study are accessible to all interested scientists from our institute resource database (http://giscompute.gis.a-star.edu.sg/~govind/zebrafish/data_download.html).

Authors & Affiliations
15 authors, click to expand affiliations / ORCID
Mathavan Sinnakaruppan
Genome Institute of Singapore, Singapore.
Lee Serene G P
Mak Alicia
Miller Lance D
Murthy Karuturi Radha Krishna
Govindarajan Kunde R
Tong Yan
Wu Yi Lian
Lam Siew Hong
Yang Henry
Ruan Yijun
Korzh Vladimir
Gong Zhiyuan
Liu Edison T
Lufkin Thomas
Conflict of Interest

Competing interests. The authors have declared that no competing interests exist.

References (75)
75 references, click to expand
  1. Structure and function of ubiquitin conjugating enzyme E2-25K: the tail is a core-dependent activity element.
    Biochemistry. 1997 Aug 26;36(34):10526-37 PMID: 9265633
  2. GATA-1 expression pattern can be recapitulated in living transgenic zebrafish using GFP reporter gene.
    Development. 1997 Oct;124(20):4105-11 PMID: 9374406
  3. Exploring the metabolic and genetic control of gene expression on a genomic scale.
    Science. 1997 Oct 24;278(5338):680-6 PMID: 9381177
  4. Rapid identification and isolation of zebrafish cDNA clones.
    Gene. 1997 Nov 12;201(1-2):87-98 PMID: 9409775
  5. RNA helicase A is essential for normal gastrulation.
    Proc Natl Acad Sci U S A. 1998 Nov 10;95(23):13709-13 PMID: 9811865
  6. Zebrafish hox clusters and vertebrate genome evolution.
    Science. 1998 Nov 27;282(5394):1711-4 PMID: 9831563
  7. Cluster analysis and display of genome-wide expression patterns.
    Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14863-8 PMID: 9843981
  8. Zebrafish: a new model for human disease.
    Genome Res. 1999 Feb;9(2):99-100 PMID: 10022974
  9. Mapping and characterization of the functional domains of the nucleolar protein RNA helicase II/Gu.
    Exp Cell Res. 1999 Mar 15;247(2):389-98 PMID: 10066367
  10. Joint action of two RNA degradation pathways controls the timing of maternal transcript elimination at the midblastula transition in Drosophila melanogaster.
    EMBO J. 1999 May 4;18(9):2610-20 PMID: 10228172
  11. Developmental activation of the capability to undergo checkpoint-induced apoptosis in the early zebrafish embryo.
    Dev Biol. 1999 May 15;209(2):409-33 PMID: 10328930
  12. DNA arrays for analysis of gene expression.
    Methods Enzymol. 1999;303:179-205 PMID: 10349646
  13. Characterization of two zebrafish cDNA clones encoding egg envelope proteins ZP2 and ZP3.
    Biochim Biophys Acta. 1999 Jul 7;1446(1-2):156-60 PMID: 10395930
  14. A view from the genome: spatial control of transcription in sea urchin development.
    Curr Opin Genet Dev. 1999 Oct;9(5):530-41 PMID: 10508696
  15. A large-scale insertional mutagenesis screen in zebrafish.
    Genes Dev. 1999 Oct 15;13(20):2713-24 PMID: 10541557
  16. Microarray analysis of Drosophila development during metamorphosis.
    Science. 1999 Dec 10;286(5447):2179-84 PMID: 10591654
  17. Zebrafish: a model system for the study of human disease.
    Curr Opin Genet Dev. 2000 Jun;10(3):252-6 PMID: 10826982
  18. Ubiquitination and degradation of the zebrafish paired-like homeobox protein VSX-1.
    J Neurochem. 2000 Jul;75(1):48-55 PMID: 10854246
  19. Isolation and characterization of medaka ribosomal protein S3a (fte-1) cDNA and gene.
    Gene. 2000 May 30;250(1-2):209-17 PMID: 10854794
  20. Asynchronous activation of 10 muscle-specific protein (MSP) genes during zebrafish somitogenesis.
    Dev Dyn. 2000 Oct;219(2):201-15 PMID: 11002340
  21. Effective targeted gene 'knockdown' in zebrafish.
    Nat Genet. 2000 Oct;26(2):216-20 PMID: 11017081
  22. Identification, characterization, and mapping of expressed sequence tags from an embryonic zebrafish heart cDNA library.
    Genome Res. 2000 Dec;10(12):1915-27 PMID: 11116087
  23. Cloning and characterization of a novel nuclear Bcl-2 family protein, zfMcl-1a, in zebrafish embryo.
    Biochem Biophys Res Commun. 2000 Dec 20;279(2):725-31 PMID: 11118352
  24. Dispersion of cyclin B mRNA aggregation is coupled with translational activation of the mRNA during zebrafish oocyte maturation.
    Dev Biol. 2001 Jan 15;229(2):421-31 PMID: 11150242
  25. Zygotic regulation of maternal cyclin A1 and B2 mRNAs.
    Mol Cell Biol. 2001 Mar;21(5):1662-71 PMID: 11238903
  26. Significance analysis of microarrays applied to the ionizing radiation response.
    Proc Natl Acad Sci U S A. 2001 Apr 24;98(9):5116-21 PMID: 11309499
  27. Developmental analysis of ceruloplasmin gene and liver formation in zebrafish.
    Mech Dev. 2001 May;103(1-2):137-9 PMID: 11335121
  28. A novel method using edge detection for signal extraction from cDNA microarray image analysis.
    Exp Mol Med. 2001 Jun 30;33(2):83-8 PMID: 11460886
  29. A novel rhamnose-binding lectin family from eggs of steelhead trout (Oncorhynchus mykiss) with different structures and tissue distribution.
    Biosci Biotechnol Biochem. 2001 Jun;65(6):1328-38 PMID: 11471732
  30. Patterns of gene expression during Drosophila mesoderm development.
    Science. 2001 Aug 31;293(5535):1629-33 PMID: 11486054
  31. Genomics. Zebrafish--the canonical vertebrate.
    Science. 2001 Nov 9;294(5545):1290-1 PMID: 11701913
  32. Homologues of c-hairy1 (her9) and lunatic fringe in zebrafish are expressed in the developing central nervous system, but not in the presomitic mesoderm.
    Dev Genes Evol. 2001 Oct;211(10):493-500 PMID: 11702199
  33. Insertional mutagenesis in zebrafish rapidly identifies genes essential for early vertebrate development.
    Nat Genet. 2002 Jun;31(2):135-40 PMID: 12006978
  34. Translational machinery of channel catfish: I. A transcriptomic approach to the analysis of 32 40S ribosomal protein genes and their expression.
    Gene. 2002 May 29;291(1-2):177-86 PMID: 12095691
  35. Comparative analysis of somitogenesis related genes of the hairy/Enhancer of split class in Fugu and zebrafish.
    BMC Genomics. 2002 Aug 5;3(1):21 PMID: 12160468
  36. Tissue-specific expression of rhamnose-binding lectins in the steelhead trout (Oncorhynchus mykiss).
    Biosci Biotechnol Biochem. 2002 Jun;66(6):1427-30 PMID: 12162575
  37. Expression profiling of Drosophila imaginal discs.
    Genome Biol. 2002 Jul 24;3(8):RESEARCH0038 PMID: 12186645
  38. Construction of a zebrafish cDNA microarray: gene expression profiling of the zebrafish during development.
    Biochem Biophys Res Commun. 2002 Sep 6;296(5):1134-42 PMID: 12207891
  39. Expressed sequence tag analysis of expression profiles of zebrafish testis and ovary.
    Gene. 2002 Jul 10;294(1-2):45-53 PMID: 12234666
  40. Gene expression during the life cycle of Drosophila melanogaster.
    Science. 2002 Sep 27;297(5590):2270-5 PMID: 12351791
  41. Beta-catenin/Tcf-regulated transcription prior to the midblastula transition.
    Development. 2002 Dec;129(24):5743-52 PMID: 12421713
  42. Optimal gene expression analysis by microarrays.
    Cancer Cell. 2002 Nov;2(5):353-61 PMID: 12450790
  43. Zygotic control of maternal cyclin A1 translation and mRNA stability.
    Dev Dyn. 2002 Dec;225(4):511-21 PMID: 12454927
  44. Survivin mRNA is down-regulated during early Xenopus laevis embryogenesis.
    Dev Dyn. 2002 Dec;225(4):597-601 PMID: 12454937
  45. Real-time visualization of mycobacterium-macrophage interactions leading to initiation of granuloma formation in zebrafish embryos.
    Immunity. 2002 Dec;17(6):693-702 PMID: 12479816
  46. A segmental nearest neighbor normalization and gene identification method gives superior results for DNA-array analysis.
    Proc Natl Acad Sci U S A. 2003 Feb 4;100(3):1122-7 PMID: 12529501
  47. Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta.
    Dev Cell. 2003 Jan;4(1):67-82 PMID: 12530964
  48. Systematic determination of patterns of gene expression during Drosophila embryogenesis.
    Genome Biol. 2002;3(12):RESEARCH0088 PMID: 12537577
  49. 15000 unique zebrafish EST clusters and their future use in microarray for profiling gene expression patterns during embryogenesis.
    Genome Res. 2003 Mar;13(3):455-66 PMID: 12618376
  50. Survivin acts as an antiapoptotic factor during the development of mouse preimplantation embryos.
    Dev Biol. 2003 Apr 15;256(2):331-41 PMID: 12679106
  51. Down-regulation of RNA helicase II/Gu results in the depletion of 18 and 28 S rRNAs in Xenopus oocyte.
    J Biol Chem. 2003 Oct 3;278(40):38847-59 PMID: 12851405
  52. Tissue-specific gene expression and ecdysone-regulated genomic networks in Drosophila.
    Dev Cell. 2003 Jul;5(1):59-72 PMID: 12852852
  53. Regulation of maternal transcript destabilization during egg activation in Drosophila.
    Genetics. 2003 Jul;164(3):989-1001 PMID: 12871909
  54. Silencing of RNA helicase II/Gualpha inhibits mammalian ribosomal RNA production.
    J Biol Chem. 2003 Dec 26;278(52):52307-14 PMID: 14559904
  55. Apoptosis in zebrafish development.
    Comp Biochem Physiol B Biochem Mol Biol. 2003 Dec;136(4):731-42 PMID: 14662298
  56. Dynamics of global gene expression changes during mouse preimplantation development.
    Dev Cell. 2004 Jan;6(1):117-31 PMID: 14723852
  57. A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo.
    Dev Cell. 2004 Jan;6(1):133-44 PMID: 14723853
  58. Maternal control of vertebrate development before the midblastula transition: mutants from the zebrafish I.
    Dev Cell. 2004 Jun;6(6):771-80 PMID: 15177026
  59. Maternal control of development at the midblastula transition and beyond: mutants from the zebrafish II.
    Dev Cell. 2004 Jun;6(6):781-90 PMID: 15177027
  60. Microarray gene expression profiling during the segmentation phase of zebrafish development.
    Comp Biochem Physiol C Toxicol Pharmacol. 2004 Jul;138(3):351-62 PMID: 15533793
  61. Tissue-restricted accumulation of a ribosomal protein mRNA is not coordinated with rRNA transcription and precedes growth of the sea urchin pluteus larva.
    Dev Biol. 1992 Jan;149(1):27-40 PMID: 1728593
  62. The three postblastoderm cell cycles of Drosophila embryogenesis are regulated in G2 by string.
    Cell. 1990 Aug 10;62(3):469-80 PMID: 2199063
  63. Expression of ribosomal protein genes and regulation of ribosome biosynthesis in Xenopus development.
    Trends Biochem Sci. 1989 May;14(5):175-8 PMID: 2672437
  64. Changes in the rate of cell divisions in the course of early development of diploid and haploid loach embryos.
    J Embryol Exp Morphol. 1968 Sep;20(2):141-50 PMID: 5699955
  65. Expression of ribosomal-protein genes in Xenopus laevis development.
    Cell. 1982 Aug;30(1):163-71 PMID: 6889922
  66. The zebrafish midblastula transition.
    Development. 1993 Oct;119(2):447-56 PMID: 8287796
  67. Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development.
    Nucleic Acids Res. 1993 Mar 11;21(5):1087-95 PMID: 8464695
  68. Zebrafish cyclin D1 is differentially expressed during early embryogenesis.
    Biochim Biophys Acta. 1995 Dec 27;1264(3):257-60 PMID: 8547308
  69. Stages of embryonic development of the zebrafish.
    Dev Dyn. 1995 Jul;203(3):253-310 PMID: 8589427
  70. Expression domains of a zebrafish homologue of the Drosophila pair-rule gene hairy correspond to primordia of alternating somites.
    Development. 1996 Jul;122(7):2071-8 PMID: 8681788
  71. Identification of a novel ubiquitin-conjugating enzyme involved in mitotic cyclin degradation.
    Curr Biol. 1996 Apr 1;6(4):455-66 PMID: 8723350
  72. Highly efficient germ-line transmission of proviral insertions in zebrafish.
    Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7777-82 PMID: 8755552
  73. Zygotic degradation of two maternal Cdc25 mRNAs terminates Drosophila's early cell cycle program.
    Genes Dev. 1996 Aug 1;10(15):1966-77 PMID: 8756353
  74. Parallel human genome analysis: microarray-based expression monitoring of 1000 genes.
    Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):10614-9 PMID: 8855227
  75. Zebrafish cyclin E regulation during early embryogenesis.
    Dev Dyn. 1996 May;206(1):1-11 PMID: 9019240
Article Info
Journal
PLoS genetics
Abbr.
PLoS Genet
ISSN
1553-7390
DOI
10.1371/journal.pgen.0010029
Published
2005-08-00
Epub
2005-00-26
Pages
260-76
Language
English
Region
United States
NLM ID
101239074
PMCID
PMC1193535
External Links
PubMed source DOI: 10.1371/journal.pgen.0010029 PMC Full Text
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2