Allorecognition, via TgrB1 and TgrC1, mediates the transition from unicellularity to multicellularity in the social amoebae Dictyostelium discoideum

Abstract

The social amoeba Dictyostelium discoideum integrates into a multicellular organism when individual starving cells aggregate and form a mound. The cells then integrate into defined tissues and develop into a fruiting body that consists of a stalk and spores. Aggregation is initially orchestrated by waves of extracellular cyclic adenosine monophosphate (cAMP), and previous theory suggested that cAMP and other field-wide diffusible signals mediate tissue integration and terminal differentiation as well. Cooperation between cells depends on an allorecognition system comprising the polymorphic adhesion proteins TgrB1 and TgrC1. Binding between compatible TgrB1 and TgrC1 variants ensures that non-matching cells segregate into distinct aggregates prior to terminal development. Here, we have embedded a small number of cells with incompatible allotypes within fields of developing cells with compatible allotypes. We found that compatibility of the allotype encoded by the tgrB1 and tgrC1 genes is required for tissue integration, as manifested in cell polarization, coordinated movement and differentiation into prestalk and prespore cells. Our results show that the molecules that mediate allorecognition in D. discoideum also control the integration of individual cells into a unified developing organism, and this acts as a gating step for multicellularity.

Wild Dictyostelium discoideum social amoebae show plastic responses to the presence of nonrelatives during multicellular development

“…discoideum . We considered two previous hypotheses with opposite predictions: (a) cells in chimeras race to become spores (Kuzdzal‐Fick, Queller, & Strassmann, ) and (b) discoordination due to mixing two genotypes slows down development (Hirose et al, ). We compared the gene expression patterns of our samples to a developmental time series from the axenic laboratory strain AX4 (Rosengarten et al, ) and tested whether there was a consistent difference by social condition that may hint toward a relative acceleration or delay in development in chimeras.…”

Gene discovery by chemical mutagenesis and whole-genome sequencing in Dictyostelium

“…TgrB1 and TgrC1 are cell-surface adhesion proteins that form heterophilic interactions in trans (Chen et al 2013). Cells carrying a mismatched allelic pair of the tgrB1 and tgrC1 genes exhibit impaired cell-cell recognition and are unable to complete development (Benabentos et al 2009;Hirose et al 2011Hirose et al , 2015. The tgrB1 AX4 tgrC1…”

“…These results suggest that our So far, we have relied on multiple alleles and on published results to validate our screen results. The highest numbers of alleles were found in rapgapB and tgrB1, and we know that TgrB1 and TgrC1 interact to regulate development (Hirose et al 2015) and that rapgapB encodes a RapA GTPase regulatory protein B that regulates cell-cell and cell-substrate adhesion (Parkinson et al 2009). This knowledge and the availability of molecular tools allowed us to perform direct causality tests of these mutations.…”

Interbacterial signaling via Burkholderia contact-dependent growth inhibition system proteins

“…In the social amoeba Dictyostelium discoideum, kin discrimination and cooperation between self cells is achieved by interactions between matching allelic pairs of surface proteins (4,5). Similarly, allele-specific interactions between surface proteins restrict Myxococcus xanthus outer membrane protein exchange and multicellular activities to occur only between certain individuals (6,7).…”