Mechanism and Bicoid‐dependent control of hairy stripe 7 expression in the posterior region of the Drosophila embryo

Pair‐rule gene hairy (h) expression in seven evenly spaced stripes, along the longitudinal axis of the Drosophila blastoderm embryo, is mediated by a modular array of separate stripe enhancer elements. The minimal enhancer element, which generates reporter gene expression in place of the most posterior h stripe 7 (h7‐element), contains a dense array of binding sites for factors providing the trans‐acting control of h stripe 7 expression as revealed by genetic analyses. The h7‐element mediates position‐dependent gene expression by sensing region‐specific combinations and concentrations of both the maternal homeodomain transcriptional activators, Caudal and Bicoid, and of transcriptional repressors encoded by locally expressed zygotic gap genes. Caudal and Bicoid, which form complementing concentration gradients along the longitudinal axis of the embryo, function as redundant activators, indicating that the anterior determinant Bicoid is able to activate gene expression in the most posterior region of the embryo. The spatial limits of the h stripe 7 domain are brought about by the local activities of repressors which prevent activation. The results suggest that the gradients of Bicoid and Caudal combine their activities to activate segmentation genes along the entire axis of the embryo.

[1]  H. Jäckle,et al.  From gradients to stripes in Drosophila embryogenesis: filling in the gaps. , 1996, Trends in genetics : TIG.

[2]  M Klingler,et al.  Disperse versus compact elements for the regulation of runt stripes in Drosophila. , 1996, Developmental biology.

[3]  M. Levine,et al.  The gap protein knirps mediates both quenching and direct repression in the Drosophila embryo. , 1996, The EMBO journal.

[4]  M. Levine,et al.  Regulation of two pair-rule stripes by a single enhancer in the Drosophila embryo. , 1996, Developmental biology.

[5]  Norbert Perrimon,et al.  marelle Acts Downstream of the Drosophila HOP/JAK Kinase and Encodes a Protein Similar to the Mammalian STATs , 1996, Cell.

[6]  M. Levine,et al.  The eve stripe 2 enhancer employs multiple modes of transcriptional synergy. , 1996, Development.

[7]  R. Tjian,et al.  DNA Template and Activator-Coactivator Requirements for Transcriptional Synergism by Drosophila Bicoid , 1995, Science.

[8]  Robert Tjian,et al.  Multiple TAFIIs Directing Synergistic Activation of Transcription , 1995, Science.

[9]  Norbert Perrimon,et al.  Activation of posterior gap gene expression in the Drosophila blastoderm , 1995, Nature.

[10]  S. Carroll,et al.  Positioning adjacent pair-rule stripes in the posterior Drosophila embryo. , 1994, Development.

[11]  Claude Desplan,et al.  Synergy between the hunchback and bicoid morphogens is required for anterior patterning in Drosophila , 1994, Cell.

[12]  H. Jäckle,et al.  A two-step mode of stripe formation in the Drosophila blastoderm requires interactions among primary pair rule genes , 1994, Mechanisms of Development.

[13]  J. Gergen,et al.  Regulation of runt transcription by Drosophila segmentation genes , 1993, Mechanisms of Development.

[14]  H. Jäckle,et al.  Dimerization and the control of transcription by Krüppel , 1993, Nature.

[15]  H. Jäckle,et al.  Transcriptional cascades in Drosophila. , 1993, Current opinion in cell biology.

[16]  M. Bate,et al.  The development of Drosophila melanogaster , 1993 .

[17]  M. Levine,et al.  Regulation of even‐skipped stripe 2 in the Drosophila embryo. , 1992, The EMBO journal.

[18]  M Hoch,et al.  Competition for overlapping sites in the regulatory region of the Drosophila gene Krüppel. , 1992, Science.

[19]  D. Lindsley,et al.  The Genome of Drosophila Melanogaster , 1992 .

[20]  C. Nüsslein-Volhard,et al.  The origin of pattern and polarity in the Drosophila embryo , 1992, Cell.

[21]  M. Levine,et al.  Regulation of a segmentation stripe by overlapping activators and repressors in the Drosophila embryo. , 1991, Science.

[22]  H. Jäckle,et al.  Concentration-dependent transcriptional activation or repression by Krüppel from a single binding site , 1991, Nature.

[23]  H. Jäckle,et al.  Gene expression mediated by cis‐acting sequences of the Krüppel gene in response to the Drosophila morphogens bicoid and hunchback. , 1991, The EMBO journal.

[24]  M. Levine,et al.  Transcriptional regulation of a pair-rule stripe in Drosophila. , 1991, Genes & development.

[25]  G. Riddihough,et al.  Individual stripe regulatory elements in the Drosophila hairy promoter respond to maternal, gap, and pair-rule genes. , 1991, Genes & development.

[26]  G. Struhl,et al.  Decoding positional information: regulation of the pair-rule gene hairy. , 1990, Development.

[27]  J. Casanova,et al.  Pattern formation under the control of the terminal system in the Drosophila embryo. , 1990, Development.

[28]  Michael J. Pankratz,et al.  Gradients of Krüppel and knirps gene products direct pair-rule gene stripe patterning in the posterior region of the drosophila embryo , 1990, Cell.

[29]  H. Jäckle,et al.  Making stripes in the Drosophila embryo. , 1990, Trends in genetics : TIG.

[30]  H. Jäckle,et al.  Krüppel requirement for knirps enhancement reflects overlapping gap gene activities in the Drosophila embryo , 1989, Nature.

[31]  Tom Maniatis,et al.  Early and late periodic patterns of even skipped expression are controlled by distinct regulatory elements that respond to different spatial cues , 1989, Cell.

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

[33]  P. Ingham.  The molecular genetics of embryonic pattern formation in Drosophila , 1988, Nature.

[34]  P. Ingham,et al.  Region-specific alleles of the Drosophila segmentation gene hairy. , 1988, Genes & development.

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

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

[37]  Robert Tjian,et al.  Isolation of cDNA encoding transcription factor Sp1 and functional analysis of the DNA binding domain , 1987, Cell.

[38]  Walter J. Gehring,et al.  Regulation and function of the Drosophila segmentation gene fushi tarazu , 1987, Cell.

[39]  Diethard Tautz,et al.  Finger protein of novel structure encoded by hunchback, a second member of the gap class of Drosophila segmentation genes , 1987, Nature.

[40]  M. Frasch,et al.  Characterization and localization of the even‐skipped protein of Drosophila. , 1987, The EMBO journal.

[41]  Marek Mlodzik,et al.  Expression of the caudal gene in the germ line of Drosophila: Formation of an RNA and protein gradient during early embryogenesis , 1987, Cell.

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

[43]  F. Studier,et al.  Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. , 1986, Journal of molecular biology.

[44]  Walter J. Gehring,et al.  Control elements of the Drosophila segmentation gene fushi tarazu , 1985, Cell.

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

[46]  J. C. Li,et al.  Development in DROSOPHILA MELANOGASTER. , 1927, Genetics.