Mutual suppression between mutations in the Dictyostelium Greenbeard pathway restores wild-type development

BMC Genomics. 2025 Jun 5;26(1):563. doi: 10.1186/s12864-025-11745-0.

Abstract

Background: The Dictyostelium greenbeard pathway is mediated by two polymorphic transmembrane proteins, the TgrC1 ligand and the TgrB1 receptor. These proteins mediate allorecognition, altruism, and the developmental transition to multicellularity. A genetic suppressor screen revealed activating mutations in tgrB1 and inactivating mutations in rapgapB, a regulator of the GTPase protein RapA. Inactivation of either tgrB1, tgrC1, or rapgapB leads to developmental defects, but the respective double-mutant strains rapgapB-tgrB1- and rapgapB-tgrC1- develop well and produce spores. This mutual suppression could result from inducing an alternative pathway or from restoring wild-type development, but morphological analyses alone could not resolve this question.

Results: Here, we show that the mutual suppression between rapgapB- and tgrB1- restores wild-type development. We also analyzed an activated tgrB1 allele in the wild-type background and found evidence for interactions between the wild-type and the activated alleles. Using RNA-sequencing analyses, we compared the transcriptomes of the wild type to those of several mutant strains and found that the single-gene mutations attenuated transcriptome progression over developmental time, whereas the double-gene mutation strain rapgapB-tgrB1- and the activated tgrB1 mutation exhibited near wild-type transcriptomes. Our findings suggest that tgrB1, tgrC1, and rapgapB are involved in a pathway in which rapgapB negatively regulates tgrB1 and tgrC1 expression, whereas tgrB1 and tgrC1 positively regulate rapgapB expression.

Conclusions: These findings suggest that the Dictyostelium greenbeard pathway interfaces with the central RapGAPB-RapA regulatory pathway, providing molecular insight into a mutual suppression mechanism in which two deleterious mutations restore wild-type behavior.

Keywords: Dictyostelium allorecognition; Dictyostelium development; Greenbeard pathway; Mutual suppression; Transcriptome phenotyping.

MeSH terms

  • Dictyostelium* / genetics
  • Dictyostelium* / growth & development
  • Dictyostelium* / metabolism
  • GTPase-Activating Proteins / genetics
  • GTPase-Activating Proteins / metabolism
  • Mutation*
  • Protozoan Proteins* / genetics
  • Protozoan Proteins* / metabolism
  • Signal Transduction

Substances

  • Protozoan Proteins
  • GTPase-Activating Proteins