BzpF is a CREB-like transcription factor that regulates spore maturation and stability in Dictyostelium

The cAMP response element-binding protein (CREB) is a highly conserved transcription factor that integrates signaling through the cAMP-dependent protein kinase A (PKA) in many eukaryotes. PKA plays a critical role in Dictyostelium development but no CREB homologue has been identified in this system. Here we show that Dictyostelium utilizes a CREB-like protein, BzpF, to integrate PKA signaling during late development. bzpF− mutants produce compromised spores, which are extremely unstable and germination defective. Previously, we have found that BzpF binds the canonical CRE motif in vitro. In this paper, we determined the DNA binding specificity of BzpF using protein binding microarray (PBM) and showed that the motif with the highest specificity is a CRE-like sequence. BzpF is necessary to activate the transcription of at least 15 PKA-regulated, late-developmental target genes whose promoters contain BzpF binding motifs. BzpF is sufficient to activate two of these genes. The comparison of RNA sequencing data between wild type and bzpF− mutant revealed that the mutant fails to express 205 genes, many of which encode cellulose-binding and sugar-binding proteins. We propose that BzpF is a CREB-like transcription factor that regulates spore maturation and stability in a PKA-related manner. ► Dictyostelium bZIP protein BzpF binds to CRE-like sequence with high specificity. ► bzpF is expressed preferentially in spores during late culmination stage. ► Loss of BzpF results in severe defects in spore maturation and stability. ► We found 15 PKA-regulated, late-developmental genes as potential BzpF direct targets. ► Many under-expressed genes in bzpF− encode cellulose- and sugar-binding proteins.