Cooperation of Compartments for the Generation of Positional Information

A mechanism is proposed for pattern formation in developmental subfields. In application to imaginal disks, the compartmentalization appears as a prerequisite for the generation of positional information in the proximo-distal dimension. Cooperation of three or four compartments in the production of a morphogen leads to a cone-shaped morphogen distribution, since a high production rate of the morphogen is possible only at the intersection of compartment borders. The local concentration of the cone-shaped distribution is a measure for the distance from this center and can be used as positional information. In agreement with the experimental observations, the model predicts that (i) the distalmost structures are formed at the intersection of compartment borders; (ii) distal transformation occurs whenever cells of all compartments come close to each other; (iii) distal transformation does not require a complete set of circumferential structures; (iv) mutants exist in which the positional information and not the response of the cells is altered and (v) no distal to proximal intercalation of missing leg segments occur. Regeneration and formation of supernumerary insect legs can be explained as well. Simple molecular reaction can account for this type of pattern formation. The “complete circle rule” of French, Bryant and Bryant (Science 193,969-981 (1976)) for distal transformation may be simplified by a “cooperation of compartments” rule.