The rosetteless gene controls development in the choanoflagellate S. rosetta

Abstract

The origin of animal multicellularity may be reconstructed by comparing animals with one of their closest living relatives, the choanoflagellate Salpingoeca rosetta. Just as animals develop from a single cell–the zygote–multicellular rosettes of S. rosetta develop from a founding cell. To investigate rosette development, we established forward genetics in S. rosetta. We find that the rosette defect of one mutant, named Rosetteless, maps to a predicted C-type lectin, a class of signaling and adhesion genes required for the development and innate immunity in animals. Rosetteless protein is essential for rosette development and forms an extracellular layer that coats and connects the basal poles of each cell in rosettes. This study provides the first link between genotype and phenotype in choanoflagellates and raises the possibility that a protein with C-type lectin-like domains regulated development in the last common ancestor of choanoflagellates and animals.DOI: http://dx.doi.org/10.7554/eLife.04070.001

Bacterial lipids activate, synergize, and inhibit a developmental switch in choanoflagellates

“…5 B-E). Cells in OMV-induced rosettes were tightly packed and properly localized a specific marker of rosette development, the C-type lectin protein Rosetteless (32), to the extracellular matrix-rich center of the rosette (Fig. 5B).…”

“…1). The orientation of the nascently divided cells around a central focus, the production of extracellular matrix, and the activity of a C-type lectin called Rosetteless, ultimately result in the formation of spherical, multicellular rosettes (30)(31)(32). Rosettes resemble morula-stage embryos, and the transition to multicellularity in S. rosetta evokes ancestral events that spawned the first animals (26, 27, 33).…”

Gene regulation in transition

“…Fortunately, armed with the functionalgenomics insights from this study, and the establishment of forward genetics in choanoflagellates 10 …”

The origin and evolution of synaptic proteins – choanoflagellates lead the way

“…plasmids, proteins) into choanoflagellate cells, as many choanoflagellate species are covered by a thick extracellular matrix (Dayel et al, 2011). However, key advances have recently been made in establishing classical genetics in choanoflagellates, as the choanoflagellate S. rosetta produces morphologically differentiated gametes and engages in sexual reproduction (Levin and King, 2013;Levin et al, 2014). These studies together with the findings described here provide the first evidence that choanoflagellates may serve as a simple model for discovering ancestral functions of synaptic proteins.…”