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Further Development 9.6: What Genes Make a Fly’s Head? Bicoid Plus Hunchback Equal a Buttonhead

The Genetics of Axis Specification in Drosophila

Driever and co-workers (1989) predicted that Bicoid must activate other anterior genes besides hb. First, deletions of hb produced only some of the defects seen in the bicoid mutant phenotype. Second, head formation required higher Bicoid concentrations than thorax formation. Bicoid is now known to activate head-forming target genes such as buttonhead, empty spiracles, and orthodenticle, which are expressed in specific subregions of the anterior part of the embryo (Cohen and Jürgens 1990; Finkelstein and Perrimon 1990; Grossniklaus et al. 1994). Driever and co-workers (1989) also predicted that the promoters of such head-specific genes would have low-affinity binding sites for Bicoid protein, causing them to be activated only at extremely high concentrations of Bicoid—that is, near the anterior tip of the embryo. In addition to needing high Bicoid levels for activation, transcription of these genes also requires the presence of Hunchback protein (Simpson-Brose et al. 1994; Reinitz et al. 1995). Bicoid and Hunchback act synergistically at the enhancers of these “head genes” to promote their transcription in a feedforward manner.

In the posterior half of the embryo, the Caudal protein gradient also activates a number of zygotic genes, including the gap genes knirps (kni) and giant (gt), which are critical for abdominal development (Rivera-Pomar et al. 1995; Schulz and Tautz 1995). Since a second function of Bicoid protein is to inhibit the translation of caudal mRNA, Caudal protein is absent from the anterior portion of the embryo. Thus, the posterior-forming genes are not activated in this region.

Literature Cited

Cohen, S. M. and G. Jürgens. 1990. Mediation of Drosophila head development by gap-like segmentation genes. Nature 346: 482–485.

PubMed Link

Driever, W. and C. Nüsslein-Volhard. 1989. The Bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo. Nature 337: 138–143.

PubMed Link

Finkelstein, R. and N. Perrimon. 1990. The orthodenticle gene is regulated by bicoid and torso and specifies Drosophila head development. Nature 346: 485–488.

PubMed Link

Grossniklaus, U., K. M. Cadigan and W. J. Gehring. 1994. Three maternal coordinate systems cooperate in the patterning of the Drosophila head. Development 120: 3155–3171.

PubMed Link

Reinitz, J., E. Mjolsness and D. H. Sharp. 1995. Model for cooperative control of positional information in Drosophila by bicoid and maternal hunchback. J. Exp. Zool. 271: 47–56.

PubMed Link

Rivera-Pomar, R., X. Lu, N. Perrimon, H. Taubert and H. Jäckle. 1995. Activation of posterior gap gene expression in the Drosophila blastoderm. Nature 376: 253–256.

PubMed Link

Schulz, C. and D. Tautz. 1995. Zygotic caudal regulation by hunchback and its role in abdominal segment formation of the Drosophila embryo. Development121: 1023–1028.

PubMed Link

Simpson-Brose, M., J. Treisman and C. Desplan. 1994. Synergy between the hunchback and bicoid morphogens is required for anterior patterning in DrosophilaCell 78: 855–865.

PubMed Link




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