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Leaps and lulls in the developmental transcriptome of Dictyostelium discoideum

ABSTRACT: Development of the soil amoeba Dictyostelium discoideum is triggered by starvation. When placed on a solid substrate, the starving solitary amoebae cease growth, communicate via extracellular cAMP, aggregate by tens of thousands and develop into fully integrated multicellular organisms. Early phases of the developmental program are often studied in cells starved in suspension while cAMP is provided exogenously. Previous studies revealed massive shifts in the transcriptome under these developmental conditions and a close relationship between gene expression and morphogenesis, but were limited by the sampling frequency and the resolution of the methods. Here, we combine the superior depth and specificity of RNA-seq with high frequency sampling during filter development and cAMP pulsing in suspension. We found that the developmental transcriptome exhibits mostly gradual changes interspersed by a few instances of large changes. Considering the whole transcriptome as a single phenotype, we treated each time point as an independent entity and were able to characterize development as groups of similar time points separated by gaps. The grouped time points represent gradual changes in mRNA abundance and the gaps represent times during which many genes are differentially expressed rapidly. Comparing development on solid substrate to development in suspension revealed that gene expression in filter developed cells lagged behind cells treated with exogenous cAMP in suspension. The high sampling frequency revealed many genes whose regulation is reproducibly more complex than indicated by previous studies. Gene Ontology enrichment analysis showed that the transition to multicellularity at the mound stage coincided with rapid accumulation of transcripts associated with mitosis and DNA replicative processes. Later development included the up-regulation of organic signaling molecules and co-factor biosynthesis. We observed multiple instances of enrichment of oxidation-reduction and reactive oxygen related terms. Our analysis also demonstrated a high level of synchrony between the developing structures throughout development. Our data describe D. discoideum development as a series of coordinated cellular and multicellular activities. Coordination occurred within fields of aggregating cells and between multicellular bodies, such as mounds or migratory slugs that experience both cell-cell contact and various soluble signaling regimes. These time courses, sampled at the highest temporal resolution to date in this system, provide a comprehensive resource for future studies of developmental gene expression.

ORGANISM(S): Dictyostelium discoideum

PROVIDER: GSE61914 | GEO | 2015/04/21

SECONDARY ACCESSION(S): PRJNA262669

REPOSITORIES: GEO

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Project description:Development of the soil amoeba Dictyostelium discoideum is triggered by starvation. When placed on a solid substrate, the starving solitary amoebae cease growth, communicate via extracellular cAMP, aggregate by tens of thousands and develop into fully integrated multicellular organisms. Early phases of the developmental program are often studied in cells starved in suspension while cAMP is provided exogenously. Previous studies revealed massive shifts in the transcriptome under these developmental conditions and a close relationship between gene expression and morphogenesis, but were limited by the sampling frequency and the resolution of the methods. Here, we combine the superior depth and specificity of RNA-seq with high frequency sampling during filter development and cAMP pulsing in suspension. We found that the developmental transcriptome exhibits mostly gradual changes interspersed by a few instances of large changes. Considering the whole transcriptome as a single phenotype, we treated each time point as an independent entity and were able to characterize development as groups of similar time points separated by gaps. The grouped time points represent gradual changes in mRNA abundance and the gaps represent times during which many genes are differentially expressed rapidly. Comparing development on solid substrate to development in suspension revealed that gene expression in filter developed cells lagged behind cells treated with exogenous cAMP in suspension. The high sampling frequency revealed many genes whose regulation is reproducibly more complex than indicated by previous studies. Gene Ontology enrichment analysis showed that the transition to multicellularity at the mound stage coincided with rapid accumulation of transcripts associated with mitosis and DNA replicative processes. Later development included the up-regulation of organic signaling molecules and co-factor biosynthesis. We observed multiple instances of enrichment of oxidation-reduction and reactive oxygen related terms. Our analysis also demonstrated a high level of synchrony between the developing structures throughout development. Our data describe D. discoideum development as a series of coordinated cellular and multicellular activities. Coordination occurred within fields of aggregating cells and between multicellular bodies, such as mounds or migratory slugs that experience both cell-cell contact and various soluble signaling regimes. These time courses, sampled at the highest temporal resolution to date in this system, provide a comprehensive resource for future studies of developmental gene expression. Dictyosteloium discoideum gene expression (mRNA) profiles from two experimental time courses: development on filters and cAMP signaling in suspension. Filter development consists of 2 replicates of 19 time point samples, while cAMP in suspension contains 3 replicates of 10, 10 and 9 samples each.

Project description:Oscillatory phenomena are ubiquitous across different biological scales, from individual cells to tissues and whole organisms. In physical systems, oscillatory behaviour can emerge from weak coupling of independent stochastic elements. Once established, oscillations can drive coordinated group behaviour and encode robust information through oscillation frequency or amplitude. Here we use experimentation and modelling to understand the emergence and information coding properties of oscillatory cyclic adenosine monophosphate (cAMP) signaling in D. discoideum. Oscillatory cAMP signaling drives aggregation of individual amoebae and coordinated temporal shifts in gene expression. However, it is unknown how the collective behaviour emerges and attenuates in an auto-regulatory manner where temporal transcriptional regulation must decode variation in cAMP pulse count, frequency, or amplitude. To address these questions, we identified a transcription factor, Hbx5, that is essential for the initiation of collective behaviour and its activity provides a single-cell readout of the earliest sign of cAMP signaling. This reveals stochastic pulses in cAMP signaling precede collective oscillations, with Hbx5 dependent transcriptional feedback enhancing signal sensitivity necessary for the emergence of collective oscillations. We demonstrate that once collective oscillations have been established, another cAMP-regulated transcription factor, GtaC, required for subsequent developmental progression becomes activated. Modelling and experimentation suggest that temporal differences in transcription factor activation arise from differences in the threshold at which the protein kinase, ErkB, influences their activity. This leads us to propose that changes in the amplitude of cAMP oscillations during development encode temporal information, driving the orderly progression of development. These studies thus provide crucial insights into the principles driving collective behaviour and the evolution of multicellular systems.

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Leaps and lulls in the developmental transcriptome of Dictyostelium discoideum

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