A set of genes conserved in sequence and expression traces back the establishment of multicellularity in social amoebae

Abstract

BackgroundThe developmental cycle of Dictyostelid amoebae represents an early form of multicellularity with cell type differentiation. Mutant studies in the model Dictyostelium discoideum revealed that its developmental program integrates the actions of genes involved in signal transduction, adhesion, motility, autophagy and cell wall and matrix biosynthesis. However, due to functional redundancy and fail safe options not required in the laboratory, this single organism approach cannot capture all essential genes.To understand how multicellular organisms evolved, it is essential to recognize both the conserved core features of their developmental programs and the gene modifications that instigated phenotypic innovation. For complex organisms, such as animals, this is not within easy reach, but it is feasible for less complex forms, such as the Dictyostelid social amoebas.ResultsWe compared global profiles of gene expression during the development of four social amoebae species that represent 600 mya of Dictyostelia evolution, and identified orthologous conserved genes with similar developmental up-regulation of expression using three different methods. For validation, we disrupted five genes of this core set and examined the phenotypic consequences.ConclusionAt least 71 of the developmentally regulated genes that were identified with all methods were likely to be already present in the last ancestor of all Dictyostelia. The lack of phenotypic changes in null mutants indicates that even highly conserved genes either participate in functionally redundant pathways or are necessary for developmental progression under adverse, non-standard laboratory conditions. Both mechanisms provide robustness to the developmental program, but impose a limit on the information that can be obtained from deleting single genes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3223-z) contains supplementary material, which is available to authorized users.

dictyExpress: a web-based platform for sequence data management and analytics in Dictyostelium and beyond

“…Transcriptomics datasets also extend to taxonomic comparisons between P. pallidum , D. fasciculatum , and D. lacteum [13, 14]. Further, the application hosts the first comprehensive catalog of ncRNA abundance during development [7] and whole genome variant analysis of chemically mutagenized strains [9].…”

Diversity and Functional Evolution of Terpene Synthases in Dictyostelid Social Amoebae

“…The transition from the unicellular form to fruiting bodies is a tightly regulated developmental process 1 . With the aid of genome sequencing and comparative genomics, genes underlying conditional multicellularity in dictyostelids continue to be identified and characterized 2 – 4 . Among the many features of the genome sequences of dictyostelids is the presence of notable types and numbers of genes of secondary metabolism 5 , 6 , among which polyketide synthase genes are the best recognized 7 .…”

A Tripeptidyl peptidase 1 is a binding partner of GPHR (Golgi pH regulator) in Dictyostelium

“…Next, we collected expression data for the seven genes from publicly available RNA-seq data ( Parikh et al, 2010 ; Schilde et al, 2016 ; see Materials and Methods). For all genes, with the exception of tpp1F we observed remarkable changes during development.…”

“…The RNA-seq raw data were obtained from a previous study (AX4 strain two replicates; Parikh et al, 2010 ) and the NC4 data from water agar developmental time points (one experiment). The NC4 RNA-seq data were published in Schilde et al (2016) . These data were combined with the RNA-seq data from Parikh et al (2010) .…”

“…No transcripts are detected in vegetative cells, but they accumulate during development and reach a maximum at late developmental stages. Overall, the transcripts were found to be not very abundant when examined by RNA-seq ( Parikh et al, 2010 ; Schilde et al, 2016 ). Disruption of the gene causes developmental defects: in particular, spore formation was defective, and culture under autophagy-inducing conditions left the tpp1A mutant cells less viable than control cells.…”