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PMID: 15342517 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Extensive sex-specific nonadditivity of gene expression in Drosophila melanogaster.

Genetics ·Vol. 167 ·No. 4 ·2004-08-00 ·Pages 1791-9

Gibson G, Riley-Berger R, Harshman L, Kopp A, Vacha S, Nuzhdin S, Wayne M

Abstract

Assessment of the degree to which gene expression is additive and heritable has important implications for understanding the maintenance of variation, adaptation, phenotypic divergence, and the mapping of genotype onto phenotype. We used whole-genome transcript profiling using Agilent long-oligonucleotide microarrays representing 12,017 genes to demonstrate that gene transcription is pervasively nonadditive in Drosophila melanogaster. Comparison of adults of two isogenic lines and their reciprocal F1 hybrids revealed 5820 genes as significantly different between at least two of the four genotypes in either males or females or across both sexes. Strikingly, while 25% of all genes differ between the two parents, 33% differ between both F1's and the parents, averaged across sexes. However, only 5% of genes show overdominance, suggesting that heterosis for expression is rare.

MeSH Terms
Animals Drosophila melanogaster/genetics Female Gene Expression Regulation/physiology Genotype Male Models, Genetic Models, Statistical Oligonucleotide Array Sequence Analysis Phylogeny Sex Characteristics Transcription, Genetic/physiology
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Gibson Greg
Department of Genetics, North Carolina State University, Raleigh, North Carolina 27695, USA.
Riley-Berger Rebecca
Harshman Larry
Kopp Artyom
Vacha Scott
Nuzhdin Sergey
Wayne Marta
References (26)
26 references, click to expand
  1. Quantitative trait loci affecting components of wing shape in Drosophila melanogaster.
    Genetics. 2000 Jun;155(2):671-83 PMID: 10835390
  2. Genotype-environment interaction at quantitative trait loci affecting sensory bristle number in Drosophila melanogaster.
    Genetics. 1998 Aug;149(4):1883-98 PMID: 9691044
  3. The segment polarity network is a robust developmental module.
    Nature. 2000 Jul 13;406(6792):188-92 PMID: 10910359
  4. Quantitative trait locus mapping of fitness-related traits in Drosophila melanogaster.
    Genet Res. 2001 Feb;77(1):107-16 PMID: 11279827
  5. Expression profiling using microarrays fabricated by an ink-jet oligonucleotide synthesizer.
    Nat Biotechnol. 2001 Apr;19(4):342-7 PMID: 11283592
  6. Analysis of variance for gene expression microarray data.
    J Comput Biol. 2000;7(6):819-37 PMID: 11382364
  7. Analysis of strain and regional variation in gene expression in mouse brain.
    Genome Biol. 2001;2(10):RESEARCH0042 PMID: 11597334
  8. The genetic architecture of quantitative traits.
    Annu Rev Genet. 2001;35:303-39 PMID: 11700286
  9. The contributions of sex, genotype and age to transcriptional variance in Drosophila melanogaster.
    Nat Genet. 2001 Dec;29(4):389-95 PMID: 11726925
  10. Assessing gene significance from cDNA microarray expression data via mixed models.
    J Comput Biol. 2001;8(6):625-37 PMID: 11747616
  11. Robustness, flexibility, and the role of lateral inhibition in the neurogenic network.
    Curr Biol. 2002 May 14;12(10):778-86 PMID: 12015114
  12. Design of studies using DNA microarrays.
    Genet Epidemiol. 2002 Jun;23(1):21-36 PMID: 12112246
  13. Empirical bayes methods and false discovery rates for microarrays.
    Genet Epidemiol. 2002 Jun;23(1):70-86 PMID: 12112249
  14. Gene expression during the life cycle of Drosophila melanogaster.
    Science. 2002 Sep 27;297(5590):2270-5 PMID: 12351791
  15. Combining mapping and arraying: An approach to candidate gene identification.
    Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):14903-6 PMID: 12415114
  16. Finishing a whole-genome shotgun: release 3 of the Drosophila melanogaster euchromatic genome sequence.
    Genome Biol. 2002;3(12):RESEARCH0079 PMID: 12537568
  17. Paucity of genes on the Drosophila X chromosome showing male-biased expression.
    Science. 2003 Jan 31;299(5607):697-700 PMID: 12511656
  18. Natural variation in human gene expression assessed in lymphoblastoid cells.
    Nat Genet. 2003 Mar;33(3):422-5 PMID: 12567189
  19. Genetics of gene expression surveyed in maize, mouse and man.
    Nature. 2003 Mar 20;422(6929):297-302 PMID: 12646919
  20. Rapid evolution of male-biased gene expression in Drosophila.
    Proc Natl Acad Sci U S A. 2003 Aug 19;100(17):9894-9 PMID: 12907700
  21. Trans-acting regulatory variation in Saccharomyces cerevisiae and the role of transcription factors.
    Nat Genet. 2003 Sep;35(1):57-64 PMID: 12897782
  22. Mapping determinants of variation in energy metabolism, respiration and flight in Drosophila.
    Genetics. 2003 Oct;165(2):623-35 PMID: 14573475
  23. Mixed-model reanalysis of primate data suggests tissue and species biases in oligonucleotide-based gene expression profiles.
    Genetics. 2003 Oct;165(2):747-57 PMID: 14573485
  24. Anomalies in the expression profile of interspecific hybrids of Drosophila melanogaster and Drosophila simulans.
    Genome Res. 2004 Mar;14(3):373-9 PMID: 14962989
  25. The use of retrotransposons as markers for mapping genes responsible for fitness differences between related Drosophila melanogaster strains.
    Genet Res. 1993 Oct;62(2):125-31 PMID: 8276230
  26. Gene regulatory networks generating the phenomena of additivity, dominance and epistasis.
    Genetics. 2000 Jun;155(2):969-80 PMID: 10835414
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
2004-08-00
Pages
1791-9
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1471026
Subset
IM
Grants
NIGMS NIH HHS · R24-GM65513 · United States
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