Ectopic head and foot formation in Hydra: Diacylglycerol-induced increase in positional value and assistance of the head in foot formation

Abstract

Abstract In wild type Hydra magnipapillata, daily application of the protein kinase C activator diacylglycerol (DAG) evokes sprouting of periodically spaced ectopic heads along the body column and leads to loss of the ability to regenerate proximal structures including the foot [23]. The present transplantation studies show that the appearance of ectopic heads is preceded by an early increase in the ‘positional value’ ( P-value) or ‘head activation potential’ of the gastric column. Long before ectopic head structures emerge, pieces of DAG-treated tissue transplanted into the corresponding positional level of untreated hosts induce head formation instead of being integrated, whereas pieces implanted from untreated donors into DAG-treated hosts form feet. Foot formation implies a decrease in the P-value. This down-regulation is promoted through long-range assistance by the head. Thus, after termination of the DAG treatment ectopic feet are intercalated midway between the periodically spaced heads; moreover, untreated polyps onto which additional distal heads have been grafted regenerate feet faster than do one-headed polyps and may form supernumerary feet. Multiheaded animals can also be produced using two substances (K-252a and xanthate D609) that interfere with signal transduction, but the mode by which secondary heads arise is different from DAG-induced ectopic head formation. Presumably because the assistance by the parental head is impaired, buds fail to form a foot and detach and instead give rise to stable secondary body axes. It is assumed that the P-value along the body varies according to the number of cellular receptors for factors serving as intercellular signals. A species of these factors promotes the existence of such receptors and hence increases and stabilizes the P-value. The head aids in down-regulation of the P-value at distant sites by competing most successfully for these mobile factors. The hypothesis also explains the ‘rule of distal transformation’, which is obeyed by several hydroids as well as by the limbs of vertebrates.