bicoid mRNA localization signal: phylogenetic conservation of function and RNA secondary structure.

Transcripts of the bicoid (bcd) gene are localized to the anterior pole of the Drosophila oocyte, thereby allowing formation in the embryo of an anteroposterior gradient of the bcd protein morphogen. We previously showed that a 630 nucleotide portion of the 3' noncoding region of the bcd mRNA is necessary for this localization, and is sufficient to confer anterior localization on a heterologous transcript. Here I have used a comparative analysis to begin to more precisely define the cis-acting mRNA localization signal. The bcd genes from six additional Drosophila species were cloned, and DNA of the 3' noncoding regions sequenced. Three of these regions were tested interspecifically for mRNA localization in D. melanogaster and each functioned correctly; these regions must therefore contain the cis-acting signal. The primary sequences, which are up to 50% divergent from the D. melanogaster gene, show patchy homology throughout most of the region. Interestingly, all seven species can potentially form a large stereotypic secondary structure. This structure is a likely candidate for the localization signal and can be used for the rational design of mutations to test that possibility.

[1]  G. Struhl,et al.  Structure of the Drosophila BicaudalD protein and its role in localizing the posterior determinant nanos , 1989, Cell.

[2]  N. Pace,et al.  Phylogenetic comparative analysis and the secondary structure of ribonuclease P RNA--a review. , 1989, Gene.

[3]  Wolfgang Driever,et al.  Determination of spatial domains of zygotic gene expression in the Drosophila embryo by the affinity of binding sites for the bicoid morphogen , 1989, Nature.

[4]  K. Struhl,et al.  The gradient morphogen bicoid is a concentration-dependent transcriptional activator , 1989, Cell.

[5]  M. Zuker On finding all suboptimal foldings of an RNA molecule. , 1989, Science.

[6]  H. Lipshitz,et al.  Reciprocal effects of hyper- and hypoactivity mutations in the Drosophila pattern gene torso. , 1989, Science.

[7]  Wolfgang Driever,et al.  The bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo , 1989, Nature.

[8]  G. Struhl,et al.  Cis- acting sequences responsible for anterior localization of bicoid mRNA in Drosophila embryos , 1988, Nature.

[9]  J. Fackenthal,et al.  Molecular analysis of the swallow gene of Drosophila melanogaster. , 1988, Genes & development.

[10]  C. Nüsslein-Volhard,et al.  Function of torso in determining the terminal anlagen of the Drosophila embryo , 1988, Nature.

[11]  C. Nüsslein-Volhard,et al.  The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner , 1988, Cell.

[12]  C. Nüsslein-Volhard,et al.  A gradient of bicoid protein in Drosophila embryos , 1988, Cell.

[13]  D Bopp,et al.  The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. , 1988, The EMBO journal.

[14]  Diethard Tautz,et al.  Regulation of the Drosophila segmentation gene hunchback by two maternal morphogenetic centres , 1988, Nature.

[15]  N. Pace,et al.  The secondary structure of ribonuclease P RNA, the catalytic element of a ribonucleoprotein enzyme , 1988, Cell.

[16]  R. Lehmann,et al.  Determination of anteroposterior polarity in Drosophila. , 1987, Science.

[17]  M. Cariou Biochemical phylogeny of the eight species in the Drosophila melanogaster subgroup, including D. sechellia and D. orena. , 1987, Genetical research.

[18]  C. Nüsslein-Volhard,et al.  Maternal genes required for the anterior localization of bicoid activity in the embryo of Drosophila , 1987 .

[19]  M. Noll,et al.  Structure of the segmentation gene paired and the Drosophila PRD gene set as part of a gene network , 1986, Cell.

[20]  G. Struhl,et al.  A molecular gradient in early Drosophila embryos and its role in specifying the body pattern , 1986, Nature.

[21]  C. Nüsslein-Volhard,et al.  Organization of anterior pattern in the Drosophila embryo by the maternal gene bicoid , 1986, Nature.

[22]  W. Theurkauf,et al.  Tissue-specific and constitutive alpha-tubulin genes of Drosophila melanogaster code for structurally distinct proteins. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Ruth Lehmann,et al.  Abdominal segmentation, pole cell formation, and embryonic polarity require the localized activity of oskar, a maternal gene in drosophila , 1986, Cell.

[24]  T. Maniatis,et al.  Regulatory elements involved in Drosophila Adh gene expression are conserved in divergent species and separate elements mediate expression in different tissues. , 1986, The EMBO journal.

[25]  R. Myers,et al.  Fine structure genetic analysis of a beta-globin promoter. , 1986, Science.

[26]  Fotis C. Kafatos,et al.  Regulatory elements controlling chorion gene expression are conserved between flies and moths , 1985, Nature.

[27]  S. Beverley,et al.  Ancient origin for Hawaiian Drosophilinae inferred from protein comparisons. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[28]  A. Wilson,et al.  Molecular Evolution in Drosophila and the Higher Diptera II. A Time Scale for Fly Evolution , 1984 .

[29]  J. Devereux,et al.  A comprehensive set of sequence analysis programs for the VAX , 1984, Nucleic Acids Res..

[30]  G. Rubin,et al.  Vectors for P element-mediated gene transfer in Drosophila. , 1983, Nucleic acids research.

[31]  R. Cortese,et al.  pEMBL: a new family of single stranded plasmids. , 1983, Nucleic acids research.

[32]  G. Rubin,et al.  Genetic transformation of Drosophila with transposable element vectors. , 1982, Science.

[33]  S. McKnight,et al.  Transcriptional control signals of a eukaryotic protein-coding gene. , 1982, Science.

[34]  R. Axel,et al.  Integration, transcription, and control of a Drosophila heat shock gene in mouse cells. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[35]  H. Noller,et al.  Secondary structure of 16S ribosomal RNA. , 1981, Science.

[36]  C. Woese,et al.  5S RNA secondary structure , 1975, Nature.

[37]  F. Crick Diffusion in Embryogenesis , 1970, Nature.

[38]  D. Turner,et al.  Predicting optimal and suboptimal secondary structure for RNA. , 1990, Methods in enzymology.

[39]  D. Turner,et al.  RNA structure prediction. , 1988, Annual review of biophysics and biophysical chemistry.

[40]  R. Lehmann,et al.  Manipulating the anteroposterior pattern of the Drosophila embryo. , 1986, Journal of embryology and experimental morphology.

[41]  R. Gutell,et al.  Comparative anatomy of 16-S-like ribosomal RNA. , 1985, Progress in nucleic acid research and molecular biology.

[42]  W. J. Gehring,et al.  A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes , 1984, Nature.

[43]  H. Noller Structure of ribosomal RNA. , 1984, Annual review of biochemistry.