Academic journal article Genetics

The Drosophila Gap Gene Giant Has an Anterior Segment Identity Function Mediated through Disconnected and Teashirt

Academic journal article Genetics

The Drosophila Gap Gene Giant Has an Anterior Segment Identity Function Mediated through Disconnected and Teashirt

Article excerpt

ABSTRACT

The C2H2 zinc-finger-containing transcription factors encoded by the disconnected (disco) and teashirt (tsh) genes contribute to the regionalization of the Drosophila embryo by establishing fields in which specific Homeotic complex (Hom-C) proteins can function. In Drosophila embryos, disco and the paralogous disco-related (disco-r) are expressed throughout most of the epidermis of the head segments, but only in small patches in the trunk segments. Conversely, tsh is expressed extensively in the trunk segments, with little or no accumulation in the head segments. Little is known about the regulation of these genes; for example, what limits their expression to these domains? Here, we report the regulatory effects of gap genes on the spatial expression of disco, disco-r, and tsh during Drosophila embryogenesis. The data shed new light on how mutations in giant (gt) affect patterning within the anterior gt domain, demonstrating homeotic function in this domain. However, the homeosis does not occur through altered expression of the Hom-C genes but through changes in the regulation of disco and tsh.

THE redundant, paralogous genes disconnected (disco) and disco-related (disco-r), referred to together as the disco genes below, and teashirt (tsh) are differentially expressed in the embryonic head and trunk segments and are therefore markers for head and trunk segment types. In the head segments the disco genes are required for the proper development of the larval mouthpart structures (Mahaffey et al. 2001; Robertson et al. 2004), while in the trunk segments, these genes are necessary for development of the Keilin's organs, small thoracic sensory structures and some peripheral neurons (Robertson et al. 2004; Patel et al. 2007). By contrast, tsh is necessary for proper development ofmost of the ventral trunk epidermis (Fasano et al. 1991; Ro?der et al. 1992; De Zulueta et al. 1994). Both the disco genes and tsh are also members of the proximal-distal patterning network (Erkner et al. 1999; Wu and Cohen 2000; Azpiazu and Morata 2002; Patel et al. 2007). The disco and tsh genes encode C2H2 zinc-finger transcription factors that are expressed early in embryonic development with precise, nearly reciprocal expression patterns in the trunk and head segments, but not much is known as to how these patterns are established. What is known is that ectopically expressing tsh in the head segments converts the expression of the disco genes to a trunk-like pattern. The Spalt major (Salm) protein represses tsh expression in the posterior labial segment (Kuhnlein et al. 1997), but otherwise little is known regarding the regulation of disco and tsh-in particular, what factors distinguish the head and trunk modes of expression. The gap genes are logical candidates for this role.

Patterning the Drosophila embryo involves initial establishment of the axes, regionalization of the embryo, definition of the segments and their polarity, and the specification of unique identities to each segment. The early acting components of this genetic cascade include both maternally and zygotically expressed genes that set in motion the segmentation and segment identity processes. The gap genes are among the earliest zygotic factors involved in these processes. Regulated by maternal morphogens in the blastoderm, and by one another, these genes act via overlapping gradients to divide the embryo into broad regions and to regulate the expression of downstream segmentation genes (see reviews in St. Johnston and Nusslein-Volhard 1992; Pankratz and Jackle 1993; Rivera-Pomar and Jackle 1996; Niessing et al. 1997; Sanson 2001).

Comparative studies in other insects have revealed significant conservation in the function of many segmentation genes (see reviews in French 2001; Davis and Patel 2002; Hughes and Kaufman 2002), but less clear is the functional conservation of the gap genes between insect species. Two studies-one in Tribolium castaneum, examining a giant (gt) homolog (Tc'giant) (Bucher and Klingler 2004), and one in Oncopeltus fasciatus, examining a hunchback (hb) homolog (Of'hb) (Liu and Kaufman 2004)-conclude that the function of these gap genes is one of segmentation and segment identity, differing somewhat fromthe segmentation function characterized in Drosophila. …

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