Dictyostelium: Cell Sorting and Patterning

Abstract

Multicellular development of the social amoeba Dictyostelium discoideum results from the chemotactic aggregation of single cells to form a fruiting body consisting of a stalk supporting a spore mass. The interplay of two extracellular signalling molecules, cAMP (cyclic adenosine monophosphate) and the chlorinated hexaphenone DIF‐1 (differentiation‐inducing factor 1), directs cellular differentiation, and cAMP is also the chemo‐attractant that orchestrates all of morphogenesis. Although this is a relatively unusual mode of pattern formation, most of the fundamental processes that typify development in higher organism are on display, and the genetic accessibility of the organism makes it a very powerful and relevant model system. It has proven particularly valuable for understanding the basic mechanism of chemotaxis and the role that chemotaxis can play in the morphogenesis of a multicellular structure. Key concepts: Dictyostelium cells aggregate by chemotaxis in response to propagating cAMP waves. cAMP waves propagate through cAMP relay, the ability of the cells to detect a small cAMP signal, synthesis and secrete cAMP in response and thus pass the cAMP signal on to their neighbours. Adaptation of the relay response ensures unidirectional wave propagation away from the centre. Chemotactic cell movement involves detection of a cAMP gradient across the length of the cell, resulting in a polarization of actin–myosin cytoskeletal dynamics and movement up the gradient. Multicellular morphogenesis, the arrangement of tissue in space and time, is controlled by the interplay of cAMP wave propagation and chemotaxis during all stages of development. Dictyostelium development is separated from cell division but a cell's fate can be biased by its cell cycle position when development starts. Prespore cells are formed in response to cAMP signalling. Differentiation of prestalk cells is induced by a small organic molecule, DIF, which is secreted by the prespore cells. This induction forms part of a feedback loop that controls the prestalk–prespore ratio. The tip‐organizer cells are a subset of the prestalk cells that differentiation in response to a high local cAMP concentation. Dictyostelium pattern formation occurs by the sorting out of differentiated cell types.