Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals.

Alex De Mendoza,Manuel Irimia,Jon Permanyer,Hiroshi Suga,Iñaki Ruiz-Trillo

doi:10.7554/elife.08904

Abstract

Cell-type specification through differential genome regulation is a hallmark of complex multicellularity. However, it remains unclear how this process evolved during the transition from unicellular to multicellular organisms. To address this question, we investigated transcriptional dynamics in the ichthyosporean Creolimax fragrantissima, a relative of animals that undergoes coenocytic development. We find that Creolimax utilizes dynamic regulation of alternative splicing, long inter-genic non-coding RNAs and co-regulated gene modules associated with animal multicellularity in a cell-type specific manner. Moreover, our study suggests that the different cell types of the three closest animal relatives (ichthyosporeans, filastereans and choanoflagellates) are the product of lineage-specific innovations. Additionally, a proteomic survey of the secretome reveals adaptations to a fungal-like lifestyle. In summary, the diversity of cell types among protistan relatives of animals and their complex genome regulation demonstrates that the last unicellular ancestor of animals was already capable of elaborate specification of cell types.

Highlights

The process by which multicellular animals develop from a unicellular zygote is believed to mirror the first evolutionary steps that led to the origins of animal multicellularity from a unicellular species (King, 2004)
As the development of complex multicellularity is dependent upon differential genome regulation, the evolutionary onset of animal multicellularity must likewise have involved the appearance of differential genome regulatory capacities leading to distinct cell types
We show that Creolimax employs complex gene regulation including alternative splicing and the use of long intergenic non-coding RNAs

Summary

Introduction

The process by which multicellular animals develop from a unicellular zygote is believed to mirror the first evolutionary steps that led to the origins of animal multicellularity from a unicellular species (King, 2004). Many of the genes involved in the control of animal development and cell type identity, including signaling pathways and transcription factors (TFs), pre-date animal origins (Sebe-Pedros et al, 2011; SebePedros et al, 2012; Suga et al, 2012; Richter and King, 2013). As these genes are known to be present in the genomes of the protistan relatives of animals, the unicellular holozoans (King et al, 2008; Suga et al, 2013; Fairclough et al, 2013), the evolution of complex multicellularity, with cell type-specific transcriptional programs, must have involved changes in gene regulation.

Methods

Results

Conclusion