Abstract

SummaryThe 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.

Highlights

  • Multicellularity allowed cells to specialize and perform different functions within a single organism, giving rise to two fundamental cell types, gametes and somatic cells

  • 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 evolved basal disc and cup cells that respectively anchor the stalk to the substratum and the spore mass to the stalk

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Summary

Introduction

Multicellularity allowed cells to specialize and perform different functions within a single organism, giving rise to two fundamental cell types, gametes and somatic cells. Gene duplication is a key driver of organismal complexity,[7,8,9,10] and in the context of cell type evolution, it has been proposed that duplication of a gene regulatory network can lead to duplication and diversification of a cell type.[1,11,12,13] causal evidence that links duplication of specific genes to the evolution of a novel cell type is still lacking We here explore this issue in the dictyostelid social amoebas and report a case of gene duplication contributing to the evolution of a new cell type

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