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Evolutionarily conserved developmental pathways


Spemann's organizer: Is there a homologous structure in Drosophila?

Neither a few paragraphs nor a small site on the Net can do justice to anything as complex as Spemann's organizer; nonetheless, mention must be made. The organizer is associated with the dorsal lip of the blastopore in Xenopus, and found at the anterior end of the primitive streak in the Mouse. It has two functions: it sends a dorsalizing signal to mesoderm, and it induces ectoderm to become neuroectoderm. Vertebrate goosecoid is known to be both active in and essential to the organizer function. The cloning of the Drosophila gene goosecoid (homologous to vertebrate goosecoid), hints at the existence of an organizer region in Drosophila.

Goosecoid is expressed in two domains: the region of the head that develops into the brain, and the anlage of the stomatogastric nervous system. This second cluster follows the movements of foregut invagination and is incorporated into the roof of the stomodeum (abutting the endodermic anterior midgut territory). goosecoid expressing cells are found in the anterior foregut, the ring gland and the stomatogastric nervous system, the latter tissue being modified in mutants lacking Gsc.

The roles played by Decapentaplegic and Short gastrulation in dorsal-ventral polarity have direct counterparts in the vertebrate organizer. This evolutionarily conserved developmental pathway is reviewed at the site titled Dorsal-ventral polarity - Decapentaplegic: interacting proteins, receptors and downstream targets.

Two other proteins, T-related gene and Optomotor blind, both homologs of the vertebrate Brachyury, allow additional speculation as to the existence of an organizer function in Drosophila. The two Brachyury homologs are expressed in different domains. T-related gene is required for specification of hindgut and anal pads. Optomotor blind shows anterior activity in the brain and central nervous system. Vertebrate Brachyury has a major role in differentiation of the notochord and in the formation of the mesendoderm. Neither of these functions are found associated with either of Brachyury's Drosophila homologs.

The expression of two other genes is also relevant: wingless (the Drosophila wnt prototype) and Forkhead. wingless expression is required not as an instructive signal, but as a permissive factor coordinating morphoregulatory signals within the stomatogastric nervous system anlage. Wnt has a role in the vertebrate organizer; ectopic Wnt expression can induce a second axis in Xenopus.

A comparison of Forkhead action to that of its vertebrate homolog (HNF3ß) yields paradoxical results. Forkhead drives invagination of anterior and posterior midgut primordia (endodermal structures), and appears to have no role in mesoderm formation. In contrast, HNF3ß as expressed in the mouse organizer, is required for specification of the notochord, a mesodermal structure. HNF3ß is also required cell autonomously in the gut. It therefore appears that HNF3ß has an additional function in vertebrates, not found in Drosophila.

What conclusion can be reached about the existence of an organizer in Drosophila? Can any conclusions be reached about the organizer in vertebrates? It is clear that in Drosophila there is not one organizer function, but several. Perhaps the same conclusion will ultimately be reached for vertebrates. For example, in spite of the seemingly unitary origin of mesoderm, an examination of zebrafish goosecoid, coding for a homeodomain protein and no tail, the fish Brachyury homolog, reveals a complex organization: initially, expressions overlap, but with time these genes take on separate roles. goosecoid is expressed in a precoidal area, while no tail is expressed in the presumptive mesoderm (see T-related gene).

Originally Spemann and Mangold proposed that the amphibian organizer is not a uniform population of cells. When grafted in early gastrulae, late gastrula prechordal plate mesoderm can induce ectopic head, while progressively more posterior axial mesoderm can induce more posterior trunk or tail regions, leading to the distinction between head, trunk and tail organizers. This substructure is reflected by the pattern of expression of organizer genes. At the mechanistic level, Bmp4 signaling is involved in the creation and function of the trunk organizer and in neural induction (two properties that are probably linked), while the homeobox genes lim1, Samois and Goosecoid might act in the definition of the head organizer. Xnot (a brachyury homolog) and Hnf3ß, both involved in trunk differention, while not necessary for the inducing properties of organizer cells, are required for their terminal differentiation (Lemaire, 1996).

An important aspect of the vertebrate organizer may be unique, with no counterpart in Drosophila. The initial triggering of organizer activity is carried out in the frog by the wingless signaling pathway, with a direct involvement of ß-catenin (Drosophila homolog: Armadillo), zeste white 3 (Drosophila homolog: Shaggy), and the HMG-box transcription factor XTCF3 (Drosophila homolog: Pangolin). These signals eminate from a dorsalizing region, called the Nieuwkoop center, which functions to induce the overlying mesodermal cells to become the Spemann Organizer. The Nieuwkoop center was named after Prof. P. Nieuwkoop who worked at the Hubrecht Laboratory for Developmental Biology in Utrecht. There is no reason to believe that there is an early involvement of the wingless pathway in the establishment of any organizer analog in Drosophila. For further discussion of the involvement of wingless in gastrulation in Drosophila, see Gastrulation and posterior patterning: a conserved roles for Caudal.

REFERENCE

Lemaire, P and Kodjabachin, L. (1996). The vertebrate organizer: structure and molecules. Trends Genet. 12: 525-531. PubMed Citation: 9257536


date revised: 13 Jan 97

Developmental Pathways conserved in Evolution

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