Competition for Factors and Cellular Resources as a Principle of Pattern Formation in Hydra: II. Assistance of Foot Formation by Heads and Buds and a New Model of Pattern Control

Abstract

In Hydra long-range interactions between head, bud, and foot formation take place in addition to short-range interactions which are recognized as induction phenomena, occurring when transplants are placed into an environment of disparate positional value. Here the long-range promotion of foot formation is analyzed. The data show: (1) While head regeneration and the onset of budding are mutually inhibitory, in particular in Hydra vulgaris and strain reg-16 of Hydra magnipapillata, fully developed heads and advanced buds cooperatively support foot formation in both the bud and the parent. Utilizing these interdependences H. vulgaris can be caused to form ectopic feet and to regenerate feet at both ends of excised segments. (2) The foot-promoting activity returns late in head regeneration, as late as the apparent long-range "head inhibition" determined in transplantation studies. (3) While periodic treatment with diacylglycerol (DAG) increases the capacities to form heads and buds, the potency to form feet is transiently reduced. (4) When treatment with DAG is finished the elevated capacities to form heads and buds subside, in reg-16 and H. vulgaris there followed a phase of ectopic foot formation. (5) The foot does not promote head regeneration. Based on the results of this and previous studies the following hypotheses are proposed: (1) Heads and buds compete for resources, such as precursor cells and soluble head-promoting factors that are distributed in the interstitial spaces. (2) The ability to make use of these resources is associated with positional value and decreases down the body column. The decreasing capability is attributed to a decreasing complement of receptors for the head-promoting factors. (3) Feet are made by body regions which are the losers in the competition for these factors. (4) Superiority in the ability to compete for the locally available factors enables transplants to develop head structures, and inferiority causes them to form a foot. (5) Depletion of the head-promoting factors in the whole body column is a significant component of the "head inhibition potential" and mediates the assistance of heads and buds in foot formation. (6) A surplus of resources causes supernumerary head structures and delays or prevents foot regeneration. These interpretations have reference to a new receptor-based model of pattern control and are contrasted with prevailing hypotheses.