Abstract
BackgroundNervous systems are thought to be important to the evolutionary success and diversification of metazoans, yet little is known about the origin of simple nervous systems at the base of the animal tree. Recent data suggest that ctenophores, a group of macroscopic pelagic marine invertebrates, are the most ancient group of animals that possess a definitive nervous system consisting of a distributed nerve net and an apical statocyst. This study reports on details of the evolution of the neural cell type specifying transcription factor family of LIM homeobox containing genes (Lhx), which have highly conserved functions in neural specification in bilaterian animals.ResultsUsing next generation sequencing, the first draft of the genome of the ctenophore Mnemiopsis leidyi has been generated. The Lhx genes in all animals are represented by seven subfamilies (Lhx1/5, Lhx3/4, Lmx, Islet, Lhx2/9, Lhx6/8, and LMO) of which four were found to be represented in the ctenophore lineage (Lhx1/5, Lhx3/4, Lmx, and Islet). Interestingly, the ctenophore Lhx gene complement is more similar to the sponge complement (sponges do not possess neurons) than to either the cnidarian-bilaterian or placozoan Lhx complements. Using whole mount in situ hybridization, the Lhx gene expression patterns were examined and found to be expressed around the blastopore and in cells that give rise to the apical organ and putative neural sensory cells.ConclusionThis research gives us a first look at neural cell type specification in the ctenophore M. leidyi. Within M. leidyi, Lhx genes are expressed in overlapping domains within proposed neural cellular and sensory cell territories. These data suggest that Lhx genes likely played a conserved role in the patterning of sensory cells in the ancestor of sponges and ctenophores, and may provide a link to the expression of Lhx orthologs in sponge larval photoreceptive cells. Lhx genes were later co-opted into patterning more diversified complements of neural and non-neural cell types in later evolving animals.
Highlights
Nervous systems are thought to be important to the evolutionary success and diversification of metazoans, yet little is known about the origin of simple nervous systems at the base of the animal tree
Full-length cDNA transcripts for all four Mnemiopsis LIM homeobox containing genes (Lhx) genes were isolated by 5’ and 3’ RACE RT-polymerase chain reaction (PCR) from mixed-stage embryonic cDNA
Lhx gene complements By probing the full genome of M. leidyi, we find that it has a genetic complement more similar to that of the sponge lineage than to the complete repertoire of Lhx gene subfamilies found in placozoans, cnidarians, and bilaterians
Summary
Nervous systems are thought to be important to the evolutionary success and diversification of metazoans, yet little is known about the origin of simple nervous systems at the base of the animal tree. This study reports on details of the evolution of the neural cell type specifying transcription factor family of LIM homeobox containing genes (Lhx), which have highly conserved functions in neural specification in bilaterian animals. Lhx genes have roles in cell specification, tissue differentiation and neural patterning In both vertebrate and invertebrate taxa, Lhx genes have conserved roles in the patterning of sensory neurons, interneurons, and motor neurons (reviewed in [4,7]). It has been suggested that cells expressing different combinations of Lhx genes form a “LIM code” that is important in specifying cell types within a tissue or organ [8], and motor neuron axon pathway finding [5]
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