Developmental gene regulation by an ancient intercellular communication system in social amoebae

Abstract

The social amoebae (Dictyostelia) use quorum sensing-like communication systems to coordinate the periodic transition from uni- to multicellularity. The monophyletic descent of the Dictyostelia provides a unique opportunity to study the origin and adaptive evolution of such intercellular communication systems. We determined that the ability of aggregation-competent cells to respond to the intercellular messenger glorin occurred in the most ancient taxa of the Dictyostelia. We show using Illumina sequencing technology that glorin mediates rapid changes in gene expression at the transition from vegetative growth to aggregation. We conclude that peptide-based communication is the most ancient form of intercellular signaling in the evolution of multicellularity in the social amoebae, but has been repeatedly replaced by other communication systems during the monophyletic evolution of the social amoebae. Glorin communication has parallels with quorum sensing in that the molecule diffuses into the field, stimulates gene expression in receptive cells and coordinates a population-wide response.