Related Gα subunits play opposing roles during Dictyostelium development

Of the several known Dictyostelium G protein subunits, the G alpha4 and G alpha5 subunits are the most closely related pair based on phylogenetic analysis and expression patterns, but these subunits perform different roles during development. To investigate potential relationships between these subunits with respect to cell differentiation, chimeric organisms composed of strains lacking or overexpressing either subunit were created and examined for developmental morphogenesis and spore production. Chimeras of g alpha4 null and g alpha5 null strains or G alpha4 and G alpha5 overexpression strains displayed compensatory morphogenesis, implying that the subunits promote complementary developmental processes. However, chimeras composed of g alpha4 null and G alpha5 overexpression strains or g alpha5 null and G alpha4 overexpression strains displayed distorted tip morphogenesis, suggesting the strains of these chimeras share common developmental deficiencies. Cells lacking the G alpha5 subunit localized to the prespore region of chimeras similar to the pattern observed for cells overexpressing the G alpha4 subunit, and cells overexpressing the G alpha5 subunit displayed localization patterns similar to g alpha4 null mutants. A strain overexpressing both subunits displayed a partial suppression of morphology, gene expression, and cell localization phenotypes associated with the overexpression of the individual G alpha subunit genes, suggesting that each G alpha subunits can inhibit signaling mediated by the other subunit. Overexpression of the G alpha5 subunit inhibited chemotaxis and cGMP accumulation in response to folic acid, indicating that the G alpha5 subunit can inhibit early steps in the G alpha4-mediated signal transduction pathway. The contrasting phenotypes of the G alpha mutants suggest the G alpha4 and Ga5 subunits provide opposing functions in cell differentiation, localization, and chemotactic responses to folic acid.