Home LiteratureArticle Details
PMID: 8670876 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The functional conservation of proteins in evolutionary alleles and the dominant role of enhancers in evolution.

The EMBO journal ·Vol. 15 ·No. 14 ·1996-07-15 ·Pages 3722-31

Xue L, Noll M

Abstract

Drosophila paired- embryos can be rescued to viable adults by the evolutionary alleles prd-Gsb and prd-Pax3, which express the Drosophila Gooseberry and mouse Pax3 proteins under the control of the paired cis-regulatory region. As prd-Gsb uncovers a prd function involved in the proper abdominal segmentation of adults, evolutionary alleles, defined and constructed in this manner, may often be weak and thus serve to discover hitherto unknown functions of a gene. Our findings show that the Gooseberry and Pax3 proteins have conserved most or all functions of the related Drosophila Paired protein although their C-terminal halves appear unrelated in sequence but not in 3-D structure essential for function. It follows that the acquisition of new cis-regulatory regions rather than the divergence of the C-terminal coding regions has been the primary device for the functional diversification of the Drosophila genes paired and gooseberry and the mouse Pax3 gene. The operation of this mechanism in insects as well as vertebrates suggests a major role in evolution.

MeSH Terms
Alleles Animals Animals, Genetically Modified Base Sequence Binding Sites DNA-Binding Proteins/genetics,physiology Drosophila Drosophila Proteins Enhancer Elements, Genetic Evolution, Molecular Gene Dosage Homeodomain Proteins Mice Molecular Sequence Data Oligodeoxyribonucleotides PAX3 Transcription Factor Paired Box Transcription Factors Phenotype Proteins/genetics,physiology Structure-Activity Relationship Transcription Factors
Chemicals
DNA-Binding Proteins Drosophila Proteins Homeodomain Proteins Oligodeoxyribonucleotides PAX3 Transcription Factor PAX3 protein, human Paired Box Transcription Factors Proteins Prrx1 protein, mouse Transcription Factors prd protein, Drosophila Pax3 protein, mouse
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Xue L
Institute for Molecular Biology (II), University of Zürich, Switzerland.
Noll M
References (36)
36 references, click to expand
  1. The mouse Hox-1.3 gene is functionally equivalent to the Drosophila Sex combs reduced gene.
    Genes Dev. 1993 Mar;7(3):343-54 PMID: 8095481
  2. Conservation of a large protein domain in the segmentation gene paired and in functionally related genes of Drosophila.
    Cell. 1986 Dec 26;47(6):1033-40 PMID: 2877747
  3. Separable regulatory elements mediate the establishment and maintenance of cell states by the Drosophila segment-polarity gene gooseberry.
    EMBO J. 1993 Apr;12(4):1427-36 PMID: 8096813
  4. Human Hox-4.2 and Drosophila deformed encode similar regulatory specificities in Drosophila embryos and larvae.
    Cell. 1990 Nov 30;63(5):969-76 PMID: 1979526
  5. Analysis of the gooseberry locus in Drosophila embryos: gooseberry determines the cuticular pattern and activates gooseberry neuro.
    Development. 1993 May;118(1):21-31 PMID: 8375335
  6. The initiation of pair-rule stripes in the Drosophila blastoderm.
    Curr Opin Genet Dev. 1991 Aug;1(2):255-60 PMID: 1822273
  7. Evolution of distinct developmental functions of three Drosophila genes by acquisition of different cis-regulatory regions.
    Nature. 1994 Jan 6;367(6458):83-7 PMID: 7906390
  8. An inversion that disrupts the Antennapedia gene causes abnormal structure and localization of RNAs.
    Cell. 1986 Dec 26;47(6):1017-23 PMID: 2430723
  9. Isolation of two tissue-specific Drosophila paired box genes, Pox meso and Pox neuro.
    EMBO J. 1989 Nov;8(11):3447-57 PMID: 2573516
  10. Rescue of the En-1 mutant phenotype by replacement of En-1 with En-2.
    Science. 1995 Aug 4;269(5224):679-82 PMID: 7624797
  11. An exonic mutation in the HuP2 paired domain gene causes Waardenburg's syndrome.
    Nature. 1992 Feb 13;355(6361):637-8 PMID: 1347149
  12. Mouse Hox-2.2 specifies thoracic segmental identity in Drosophila embryos and larvae.
    Cell. 1990 Nov 30;63(5):961-7 PMID: 1979525
  13. Structure of the segmentation gene paired and the Drosophila PRD gene set as part of a gene network.
    Cell. 1986 Dec 5;47(5):735-46 PMID: 2877746
  14. Waardenburg's syndrome patients have mutations in the human homologue of the Pax-3 paired box gene.
    Nature. 1992 Feb 13;355(6361):635-6 PMID: 1347148
  15. Borders of parasegments in Drosophila embryos are delimited by the fushi tarazu and even-skipped genes.
    Nature. 1987 Jul 30-Aug 5;328(6129):440-2 PMID: 2886916
  16. Homeotic genes and the evolution of arthropods and chordates.
    Nature. 1995 Aug 10;376(6540):479-85 PMID: 7637779
  17. Mutations affecting segment number and polarity in Drosophila.
    Nature. 1980 Oct 30;287(5785):795-801 PMID: 6776413
  18. The origin of pattern and polarity in the Drosophila embryo.
    Cell. 1992 Jan 24;68(2):201-19 PMID: 1733499
  19. Redesigning the body plan of Drosophila by ectopic expression of the homoeotic gene Antennapedia.
    Nature. 1987 Feb 26-Mar 4;325(6107):816-8 PMID: 3821869
  20. Splotch (Sp2H), a mutation affecting development of the mouse neural tube, shows a deletion within the paired homeodomain of Pax-3.
    Cell. 1991 Nov 15;67(4):767-74 PMID: 1682057
  21. Genetic transformation of Drosophila with transposable element vectors.
    Science. 1982 Oct 22;218(4570):348-53 PMID: 6289436
  22. The gooseberry-zipper region of Drosophila: five genes encode different spatially restricted transcripts in the embryo.
    EMBO J. 1987 Sep;6(9):2793-801 PMID: 16453795
  23. A B-cell coactivator of octamer-binding transcription factors.
    Nature. 1995 Jan 26;373(6512):360-2 PMID: 7779176
  24. Multiple regulatory elements direct the complex expression pattern of the Drosophila segmentation gene paired.
    Mech Dev. 1994 Nov;48(2):119-28 PMID: 7873402
  25. Molecular analysis of the dominant homeotic Antennapedia phenotype.
    EMBO J. 1987 Jan;6(1):201-6 PMID: 16453748
  26. Conservation of the paired domain in metazoans and its structure in three isolated human genes.
    EMBO J. 1989 Apr;8(4):1183-90 PMID: 2501086
  27. Complex demethylation patterns at Sp1 binding sites in F9 embryonal carcinoma cells.
    FEBS Lett. 1995 Aug 21;370(3):170-4 PMID: 7656970
  28. Boundaries and fields in early embryos.
    Cell. 1992 Jan 24;68(2):221-35 PMID: 1346367
  29. Structure of two genes at the gooseberry locus related to the paired gene and their spatial expression during Drosophila embryogenesis.
    Genes Dev. 1987 Dec;1(10):1247-67 PMID: 3123319
  30. Pax-3, a novel murine DNA binding protein expressed during early neurogenesis.
    EMBO J. 1991 May;10(5):1135-47 PMID: 2022185
  31. The role of segment polarity genes during Drosophila neurogenesis.
    Genes Dev. 1989 Jun;3(6):890-904 PMID: 2501154
  32. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback.
    Chromosoma. 1989 Aug;98(2):81-5 PMID: 2476281
  33. Evolution and role of Pax genes.
    Curr Opin Genet Dev. 1993 Aug;3(4):595-605 PMID: 8241771
  34. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes.
    J Mol Biol. 1986 May 5;189(1):113-30 PMID: 3537305
  35. Role of the gooseberry gene in Drosophila embryos: maintenance of wingless expression by a wingless--gooseberry autoregulatory loop.
    EMBO J. 1993 Dec;12(12):4499-509 PMID: 8223460
  36. Complex regulation of early paired expression: initial activation by gap genes and pattern modulation by pair-rule genes.
    Development. 1993 Feb;117(2):609-23 PMID: 8330531
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1996-07-15
Pages
3722-31
Language
English
Region
England
NLM ID
8208664
PMCID
PMC452034
Subset
IM
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