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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 comprised of 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.

ORGANISM(S): Dictyostelium discoideum

PROVIDER: GSE68063 | GEO | 2016/04/13

SECONDARY ACCESSION(S): PRJNA281643

REPOSITORIES: GEO

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Project description:The greenbeard allorecognition pathway of Dictyostelium discoideum is mediated by the polymorphic transmembrane proteins TgrB1 and TgrC1. TgrC1 is a ligand and TgrB1 is its receptor, and together they mediate allorecognition with accompanying altruism during the transition from unicellular to multicellular development. A genetic screen for suppressors of developmental defects in the non-compatible allotype TgrB1-C1 pathway revealed activating mutations in tgrB1 and inactivating mutations in rapgapB which encodes a regulator of the small GTPase protein RapA. Inactivation of either tgrB1, tgrC1, or rapgapB leads to developmental defects. However, surprisingly, the respective double-mutant strains rapgapB-tgrB1- and rapgapB-tgrC1- develop well and produce wild-type-like fruiting bodies. This mutual suppression could result from the induction of an alternative developmental pathway or restoration of the wild-type pathway, but morphological analyses alone could not resolve this question. Here we show that the mutual suppressors restore wild-type development. We used RNA-sequencing analyses to compare the transcriptomes of the wild type to those of six mutant strains and found that the single-gene mutations resulted in attenuated transcriptome progression over developmental time, whereas the double-gene mutation strains exhibited near wild-type transcriptomes. We also analyzed a strain that carries an activated tgrB1 allele in the wild type and found evidence for interactions between the activated and the resident alleles. Our findings suggest that tgrB1, tgrC1, and rapgapB are involved in a regulatory feedback pathway in which rapgapB negatively regulates tgrB1 and tgrC1 whereas tgrB1 and tgrC1 positively regulate rapgapB. These findings suggest that the D. discoideum greenbeard pathway interfaces with the central RapGAPB-RapA regulatory pathway, providing molecular insight into a mutual suppression mechanism in which combining two deleterious mutations leads to the restoration of wild-type behavior.

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

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