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. 1994 May 10;91(10):4387–4391. doi: 10.1073/pnas.91.10.4387

Evolution of gene networks by gene duplications: a mathematical model and its implications on genome organization.

A Wagner 1
PMCID: PMC43790  PMID: 8183919

Abstract

Networks of transcriptional regulators have key roles in metazoan development. Important forces in the evolution of these networks are gene duplications and gene deletions, events that may change the spatiotemporal expression pattern of network genes. A measure for the probability of such changes after gene-duplication events is proposed. This measure is based on a simple mathematical model that describes such networks as dynamical systems and on properties of ensembles of these dynamical systems. It is predicted that this probability depends only on the fraction of genes duplicated in a single event and that it is largest if approximately 40% of the genes in a network are duplicated. This property is robust with respect to variations in model parameters. On these grounds, it is argued that (i) evolution of gene networks should preferentially occur either by duplication of single genes or by duplication of all genes involved in a network, and that (ii) tight linkage ("clustering") or strong dispersal are the two evolutionarily most favorable forms of genomic organization of genes forming such networks.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Carey M., Lin Y. S., Green M. R., Ptashne M. A mechanism for synergistic activation of a mammalian gene by GAL4 derivatives. Nature. 1990 May 24;345(6273):361–364. doi: 10.1038/345361a0. [DOI] [PubMed] [Google Scholar]
  2. Davidson E. H. Spatial mechanisms of gene regulation in metazoan embryos. Development. 1991 Sep;113(1):1–26. doi: 10.1242/dev.113.1.1. [DOI] [PubMed] [Google Scholar]
  3. Gogos J. A., Hsu T., Bolton J., Kafatos F. C. Sequence discrimination by alternatively spliced isoforms of a DNA binding zinc finger domain. Science. 1992 Sep 25;257(5078):1951–1955. doi: 10.1126/science.1290524. [DOI] [PubMed] [Google Scholar]
  4. Goodrich J. A., McClure W. R. Competing promoters in prokaryotic transcription. Trends Biochem Sci. 1991 Nov;16(11):394–397. doi: 10.1016/0968-0004(91)90162-o. [DOI] [PubMed] [Google Scholar]
  5. Ingham P. W. The molecular genetics of embryonic pattern formation in Drosophila. Nature. 1988 Sep 1;335(6185):25–34. doi: 10.1038/335025a0. [DOI] [PubMed] [Google Scholar]
  6. Johnson P. F., McKnight S. L. Eukaryotic transcriptional regulatory proteins. Annu Rev Biochem. 1989;58:799–839. doi: 10.1146/annurev.bi.58.070189.004055. [DOI] [PubMed] [Google Scholar]
  7. Kappen C., Schughart K., Ruddle F. H. Two steps in the evolution of Antennapedia-class vertebrate homeobox genes. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5459–5463. doi: 10.1073/pnas.86.14.5459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Kenyon C., Wang B. A cluster of Antennapedia-class homeobox genes in a nonsegmented animal. Science. 1991 Aug 2;253(5019):516–517. doi: 10.1126/science.1677487. [DOI] [PubMed] [Google Scholar]
  9. LeBowitz J. H., Clerc R. G., Brenowitz M., Sharp P. A. The Oct-2 protein binds cooperatively to adjacent octamer sites. Genes Dev. 1989 Oct;3(10):1625–1638. doi: 10.1101/gad.3.10.1625. [DOI] [PubMed] [Google Scholar]
  10. Lufkin T., Dierich A., LeMeur M., Mark M., Chambon P. Disruption of the Hox-1.6 homeobox gene results in defects in a region corresponding to its rostral domain of expression. Cell. 1991 Sep 20;66(6):1105–1119. doi: 10.1016/0092-8674(91)90034-v. [DOI] [PubMed] [Google Scholar]
  11. McGinnis N., Kuziora M. A., McGinnis W. Human Hox-4.2 and Drosophila deformed encode similar regulatory specificities in Drosophila embryos and larvae. Cell. 1990 Nov 30;63(5):969–976. doi: 10.1016/0092-8674(90)90500-e. [DOI] [PubMed] [Google Scholar]
  12. McGinnis W., Krumlauf R. Homeobox genes and axial patterning. Cell. 1992 Jan 24;68(2):283–302. doi: 10.1016/0092-8674(92)90471-n. [DOI] [PubMed] [Google Scholar]
  13. Mermelstein F. H., Flores O., Reinberg D. Initiation of transcription by RNA polymerase II. Biochim Biophys Acta. 1989 Sep 21;1009(1):1–10. doi: 10.1016/0167-4781(89)90071-7. [DOI] [PubMed] [Google Scholar]
  14. Oliviero S., Struhl K. Synergistic transcriptional enhancement does not depend on the number of acidic activation domains bound to the promoter. Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):224–228. doi: 10.1073/pnas.88.1.224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Olson E. N. MyoD family: a paradigm for development? Genes Dev. 1990 Sep;4(9):1454–1461. doi: 10.1101/gad.4.9.1454. [DOI] [PubMed] [Google Scholar]
  16. Rosenfeld M. G. POU-domain transcription factors: pou-er-ful developmental regulators. Genes Dev. 1991 Jun;5(6):897–907. doi: 10.1101/gad.5.6.897. [DOI] [PubMed] [Google Scholar]
  17. Sassone-Corsi P., Ransone L. J., Lamph W. W., Verma I. M. Direct interaction between fos and jun nuclear oncoproteins: role of the 'leucine zipper' domain. Nature. 1988 Dec 15;336(6200):692–695. doi: 10.1038/336692a0. [DOI] [PubMed] [Google Scholar]
  18. Schughart K., Kappen C., Ruddle F. H. Duplication of large genomic regions during the evolution of vertebrate homeobox genes. Proc Natl Acad Sci U S A. 1989 Sep;86(18):7067–7071. doi: 10.1073/pnas.86.18.7067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Sorger P. K., Pelham H. R. Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell. 1988 Sep 9;54(6):855–864. doi: 10.1016/s0092-8674(88)91219-6. [DOI] [PubMed] [Google Scholar]
  20. Whiting J., Marshall H., Cook M., Krumlauf R., Rigby P. W., Stott D., Allemann R. K. Multiple spatially specific enhancers are required to reconstruct the pattern of Hox-2.6 gene expression. Genes Dev. 1991 Nov;5(11):2048–2059. doi: 10.1101/gad.5.11.2048. [DOI] [PubMed] [Google Scholar]
  21. Wilson A. C., Sarich V. M., Maxson L. R. The importance of gene rearrangement in evolution: evidence from studies on rates of chromosomal, protein, and anatomical evolution. Proc Natl Acad Sci U S A. 1974 Aug;71(8):3028–3030. doi: 10.1073/pnas.71.8.3028. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Wright A. P., Gustafsson J. A. Mechanism of synergistic transcriptional transactivation by the human glucocorticoid receptor. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8283–8287. doi: 10.1073/pnas.88.19.8283. [DOI] [PMC free article] [PubMed] [Google Scholar]

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