Phylogenetic Analysis of the Teneurins: Conserved Features and Premetazoan Ancestry

Abstract

Teneurins are type II transmembrane proteins expressed during pattern formation and neurogenesis with an intracellular domain that can be transported to the nucleus and an extracellular domain that can be shed into the extracellular milieu. In Drosophila melanogaster, Caenorhabditis elegans, and mouse the knockdown or knockout of teneurin expression can lead to abnormal patterning, defasciculation, and abnormal pathfinding of neurites, and the disruption of basement membranes. Here, we have identified and analyzed teneurins from a broad range of metazoan genomes for nuclear localization sequences, protein interaction domains, and furin cleavage sites and have cloned and sequenced the intracellular domains of human and avian teneurins to analyze alternative splicing. The basic organization of teneurins is highly conserved in Bilateria: all teneurins have epidermal growth factor (EGF) repeats, a cysteine-rich domain, and a large region identical in organization to the carboxy-half of prokaryotic YD-repeat proteins. Teneurins were not found in the genomes of sponges, cnidarians, or placozoa, but the choanoflagellate Monosiga brevicollis has a gene encoding a predicted teneurin with a transmembrane domain, EGF repeats, a cysteine-rich domain, and a region homologous to YD-repeat proteins. Further examination revealed that most of the extracellular domain of the M. brevicollis teneurin is encoded on a single huge 6,829-bp exon and that the cysteine-rich domain is similar to sequences found in an enzyme expressed by the diatom Phaeodactylum tricornutum. This leads us to suggest that teneurins are complex hybrid fusion proteins that evolved in a choanoflagellate via horizontal gene transfer from both a prokaryotic gene and a diatom or algal gene, perhaps to improve the capacity of the choanoflagellate to bind to its prokaryotic prey. As choanoflagellates are considered to be the closest living relatives of animals, the expression of a primitive teneurin by an ancestral choanoflagellate may have facilitated the evolution of multicellularity and complex histogenesis in metazoa.

Behavioral idiosyncrasy reveals genetic control of phenotypic variability

“…Within the central brain, Ten-a mutation causes midline fusion defects within the central complex), a brain structure implicated in sensory integration and locomotion (26). Ten-a is highly conserved from insects to mammals (27). To validate the role of Ten-a in modulating variability in turning bias, we used a null allele (Ten-a cbd-KS96 ; Fig.…”

The role of G protein-coupled receptors in the early evolution of neurotransmission and the nervous system

“…Therefore, we wanted to explore whether pre-bilaterians comprise homologues of single transmembrane helix post-synaptic proteins. Interestingly, a recent evolutionary analysis on teneurins, an endogenous ligand of latrophilins (see above), suggested that these single-pass transmembrane proteins, which are involved in neurogenesis, were absent in the genomes of sponges, cnidarians, placozoans and ctenophores (Tucker et al, 2012). This implies that the pre-bilaterian adhesion GPCRs that are similar to family I do not have ligands or interactions partners analogous to those in vertebrates.…”

A family of diatom-like silicon transporters in the siliceous loricate choanoflagellates

“…In M. brevicollis, LGT from both eukaryotic and prokaryotic sources has been proposed to be responsible for the gain of stress-related genes [60]. Stramenopile-derived genes are thought to be unusually frequent in M. brevicollis [57], including genes linked with the evolution of multicellularity [61]. Diatoms are believed to have gained some of their biosilicification machinery (related to longchain polyamine formation) from LGT [62] in addition to other diatom-specific metabolic pathways [58].…”