A receptor tyrosine kinase from choanoflagellates: Molecular insights into early animal evolution

Abstract

The evolution of the Metazoa from protozoans is one of the major milestones in life's history. The genetic and developmental events involved in this evolutionary transition are unknown but may have involved the evolution of genes required for signaling and gene regulation in metazoans. The genome of animal ancestors may be reconstructed by identification of animal genes that are shared with related eukaryotes, particularly those that share a more recent ancestry and cell biology with animals. The choanoflagellates have long been suspected to be closer relatives of animals than are fungi, the closest outgroup of animals for which comparative genomic information is available. Phylogenetic analyses of choanoflagellate and animal relationships based on small subunit rDNA sequence, however, have yielded ambiguous and conflicting results. We find that analyses of four conserved proteins from a unicellular choanoflagellate, Monosiga brevicollis, provide robust support for a close relationship between choanoflagellates and Metazoa, suggesting that comparison of the complement of expressed genes from choanoflagellates and animals may be informative concerning the early evolution of metazoan genomes. We have discovered in M. brevicollis the first receptor tyrosine kinase (RTK), to our knowledge, identified outside of the Metazoa, MBRTK1. The architecture of MBRTK1, which includes multiple extracellular ligand-binding domains, resembles that of RTKs in sponges and humans and suggests the ability to receive and transduce signals. Thus, choanoflagellates express genes involved in animal development that are not found in other eukaryotes and that may be linked to the origin of the Metazoa.

The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans

“…Divergent use of phosphotyrosine signalling machinery Phosphotyrosine (pTyr)-based signalling was considered unique to metazoans until its recent discovery in choanoflagellates 9,11 . The key domains involved in pTyr signalling are found in abundance in the M. brevicollis genome: tyrosine kinase domains that phosphorylate tyrosine (,120 occurrences), pTyr-specific phosphatases (PTP) that remove the phosphate modification (,30) and SH2 domains that bind pTyr-containing peptides (,80) ( Supplementary Fig.…”

“…Over the past decade or so, evidence supporting this relationship has accumulated from phylogenetic analyses of nuclear and mitochondrial genes [3][4][5][6] , comparative genomics between the mitochondrial genomes of choanoflagellates, sponges and other metazoans 7,8 , and the finding that choanoflagellates express homologues of metazoan signalling and adhesion genes [9][10][11][12] . Furthermore, species-rich phylogenetic analyses demonstrate that choanoflagellates are not derived from metazoans, but instead represent a distinct lineage that evolved before the origin and diversification of metazoans (Fig.…”

“…Gene prediction and annotation. Gene models (9,196) were predicted and annotated using the Joint Genome Institute (JGI) Annotation Pipeline (Supplementary Information). Intron analysis.…”

FGF signaling in gastrulation and neural development in Nematostella vectensis, an anthozoan cnidarian

“…Although no data have addressed the presence of FGF pathways in other nonbilaterians (e.g., ctenophores, placozoans, and sponges), genomic sequencing efforts within these phyla should soon shed light on this issue. The broad question of whether FGF signaling is metazoan specific remains unanswered, but an RTK has been isolated from a choanoflagellate, a taxa considered to be the outgroup to the Metazoa (King and Carroll 2001;King et al 2003). Thus, an evolutionary antecedent of the FGF pathway may have been in place before the metazoan radiation (King and Carroll 2001).…”

An unusual choanoflagellate protein released by Hedgehog autocatalytic processing

“…Choanoflagellates are unicellular protists that are close relatives of multicellular animals ( James-Clark 1866; King & Carroll 2001;Snell et al 2001;Lang et al 2002;Philippe et al 2004). Comparison between choanoflagellates and metazoans should allow insight into the origins of animal genes and animal development.…”