Principles of branch formation and branch patterning in Hydrozoa

Abstract

The freshwater polyp Hydra produces buds which separate from the parent. Other Hydrozoa produce branches which remain connected to the parent, thus forming a colony. Some Hydrozoa grow by means of an organ that is like a shoot apical meristem. Others display a sympodial type of growth. In this article, I propose that these different types of branches are organized by a common pattern-forming system. This system has self-organizing properties. It causes branch tip formation and is kept active in the tip when the tip finally differentiates into a hypostome of a polyp. The system does not cause structure formation directly but rather, determines a tissue property called positional value, in such a way that a gradient of values forms in the tissue of the bud or branch. The local value determines the local morphodynamic processes, including differentiation of the hypostome (highest positional value), tentacles and basal disc and of the exoskeleton pattern along the shoot. A high positional value favors the onset of a new selforganizing process and by lateral inhibition, such a process prevents the initiation of a further process in its surroundings. Small quantitative differences in the range of the signals involved determine whether a bud or a branch forms and whether monopodial and sympodial growth follows.

Compartments in Scyphozoa

“…The positional values form a gradient from the oral end (maximal value / highest density of sources) to the basal end (Wolpert 1969;Gierer and Meinhardt 1972;Meinhardt 1993;Sherratt et al 1995;Berking 2003Berking , 2006. Recently, with respect to Hydra indications for a differential role of ectoderm and endoderm in the control of pattern formation have been found (Zeretzke and Berking 2002), but until now models have not been adjusted to account for these results.…”

Ediacaran developmental biology

“…In thectate hydroids, this same pattern of monopodial growth cannot occur due to the presence of the theca. In these forms, the apical stem tip acts in a fashion similar to a meristem, specifying new lateral shoots on both sides of the organism simultaneously (Berking, 2006). Sympodial growth involves the cessation of growth at the apical growth tip, and the re‐specification of the ‘apex’ as outgrowths from successive lateral growth tips (Berking, 2006).…”

“…However, organisms of cnidarian grade may also exhibit truly terminal differentiation (e.g. monopodially growing athectate hydrozoans; Berking, 2006). A placozoan affinity for Dickinsonia (Sperling & Vinther, 2010) is difficult to evaluate on developmental grounds given the low diversity and disparity of extant placozoans, and remains a viable possibility (Fig.…”

A model for tube formation and branching in Cnidaria

“…The pattern-forming systems which define this field should simultaneously cause a polar organization of the field, in such a way that cells in the centre develop the apical end of the future animal while the periphery cells develop the basal structures. It is argued that a gradient of positional values causes this polarity [9,10,[28][29][30][31]. Usually at this stage the various published models for bud formation end.…”

“…The observed pattern of the stem is a time recording of the hardening regime at the growing tip. The actual position of hardening is argued to be controlled by the positional value reached in the growing tip [31].…”