Abstract
The finding that Wingless (WG) and Decapentaplegic (DPP) suppress each others transcription provides a mechanism for creating developmental territories in fields of cells. Here, we address the mechanism of that antagonism. The dishevelled (dsh) and shaggy (sgg) genes encode intracellular proteins generally thought of as downstream of WG signaling. We have investigated the effects of changing either DSH or SGG activity on both cell fate and wg and dpp expression. At the level of cell fate in discs, DSH antagonizes SGG activity. At the level of gene expression, SGG positively regulates dpp expression and negatively regulates wg expression while DSH activity suppresses dpp expression and promotes wg expression. Sharp borders of gene expression correlating precisely with clone boundaries suggest that the effects of DSH and SGG on transcription of wg and dpp are not mediated by secreted factors but rather act through intracellular effectors. The interactions described here suggest a model for the antagonism between WG and DPP that is mediated via SGG. The model incorporates autoactivation and lateral inhibition, which are properties required for the production of stable patterns. The regulatory interactions described exhibit extensive ability to organize new pattern in response to manipulation or injury.
Highlights
Surgical grafting in both amphibians and insects shows that growth and patterning are stimulated by bringing cells from different positions in a morphogenetic field into contact (French et al, 1976)
Tissues from different locations are said to possess positional information (Wolpert, 1969) which is operationally defined both by the differentiated structures which a cell produces and by the interaction of that cell with its neighbors
When cells are placed in contact with cells from other locations, they often stimulate growth and organize surrounding normal cells into ectopic structures such as supernumerary limbs. This transmission of positional information to surrounding cells could be mediated via contact-dependent interactions (French et al, 1976; Bryant et al, 1981) or by response to secreted morphogens (Wolpert, 1969; Meinhardt, 1983) or both
Summary
Surgical grafting in both amphibians and insects shows that growth and patterning are stimulated by bringing cells from different positions in a morphogenetic field into contact (French et al, 1976). When cells are placed in contact with cells from other locations, they often stimulate growth and organize surrounding normal cells into ectopic structures such as supernumerary limbs. This transmission of positional information to surrounding cells could be mediated via contact-dependent interactions (French et al, 1976; Bryant et al, 1981) or by response to secreted morphogens (Wolpert, 1969; Meinhardt, 1983) or both. Loss of dsh in clones in leg discs causes patterning responses that mimic the response caused by loss of wg function (Theisen et al, 1994; Klingensmith et al, 1994) while loss of sgg generates ectopic patterns similar to those caused by ectopic expression of wg (Diaz-Benjumea and Cohen, 1994)
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