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Evolution of a novel cell type in Dictyostelia required gene duplication of a cudA-like transcription factor

Authors: Kin, Koryu; Chen, Zhi-Hui; Forbes, Gillian; Schaap, Pauline;

Evolution of a novel cell type in Dictyostelia required gene duplication of a cudA-like transcription factor

Abstract

The evolution of novel cell types has been proposed to result from duplication of gene regulatory networks, but proven examples are rare. In addition to stalk cells and spores that make up the fruiting bodies of three major groups of Dictyostelia, those in group 4 additionally evolved basal disc and cup cells that respectively anchor the stalk to the substratum and the spore mass to the stalk. We noted a putative group-4-specific duplication of a cudA-like transcription factor (TF) in a comparative analysis of group-representative genomes. Using increased taxon sampling, we here confirmed that this TF, cdl1, duplicated into cdl1a and cdl1b in the common ancestor to group 4. cdl1a, but not cdl1b, showed signatures of positive selection, indicative of functional innovation. Deletion of cdl1a in Dictyostelium discoideum resulted in fruiting bodies with sagging spore heads that lacked the supporting cup cells and expression of cup-specific genes. Deletion of cdl1b resulted in thinner fruiting body stalks, while a cdl1b-cdl1a- double knockout showed more severe stalk defects, suggesting an ancestral role of cdl1 in stalk formation. This was confirmed in a closely related non-group 4 species, Polysphondylium violaceum, where cdl1 knockout caused defective stalk formation. These data indicate that the group-specific duplication of cdl1 and subsequent diversification of cdl1a played a pivotal role in the evolution of a novel somatic cell type in group 4 Dictyostelia.

Keywords

570, cup gene expression, Gene duplication, Article, transcription factor evolution, /dk/atira/pure/subjectarea/asjc/2800/2800, Gene Duplication, name=General Biochemistry,Genetics and Molecular Biology, name=General Agricultural and Biological Sciences, evolution of soma, Dictyostelium, Polysphondylia, Tanscription factor evolution, Dictyostelia, /dk/atira/pure/subjectarea/asjc/1100/1100, /dk/atira/pure/subjectarea/asjc/1300/1300, Genome, Cell-type specialization, gene duplication, Stalk morphogenesis, name=General Neuroscience, phylogenetics, Phylogenetics, Gene Expression Regulation, cell-type specialization, Cup gene expression, RNA-seq, stalk morphogenesis, Evolution of soma, Transcription Factors

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citations
This is an alternative to the "Influence" indicator, which also reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Citations provided by BIP!
popularity
This indicator reflects the "current" impact/attention (the "hype") of an article in the research community at large, based on the underlying citation network.
BIP!Popularity provided by BIP!
influence
This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Influence provided by BIP!
impulse
This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.
BIP!Impulse provided by BIP!
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