Abstract
Vertebrates develop an olfactory system that detects odorants and pheromones through their interaction with specialized cell surface receptors on olfactory sensory neurons. During development, the olfactory system forms from the olfactory placodes, specialized areas of the anterior ectoderm that share cellular and molecular properties with placodes involved in the development of other cranial senses. The early-diverging chordate lineages amphioxus, tunicates, lampreys and hagfishes give insight into how this system evolved. Here, we review olfactory system development and cell types in these lineages alongside chemosensory receptor gene evolution, integrating these data into a description of how the vertebrate olfactory system evolved. Some olfactory system cell types predate the vertebrates, as do some of the mechanisms specifying placodes, and it is likely these two were already connected in the common ancestor of vertebrates and tunicates. In stem vertebrates, this evolved into an organ system integrating additional tissues and morphogenetic processes defining distinct olfactory and adenohypophyseal components, followed by splitting of the ancestral placode to produce the characteristic paired olfactory organs of most modern vertebrates.
Highlights
There are two major olfactory subsystems in jawed vertebrates: the main olfactory system (MOS) and the accessory olfactory system (AOS), and relevant neuronal cell types are summarized in table 1
When a chemical stimulus flows into the MOS or AOS, it is detected by olfactory sensory neurons (OSNs) through specific membrane chemoreceptors
In the recesses of the mammalian main olfactory epithelium, there is an expression of chemoreceptors from the guanylate cyclase D receptor family, and the MS4A gene family, in the cilia of a specific group of OSNs known as the necklace OSNs
Summary
AOS lost in some tetrapod lineages demonstrated only in rodents dominance of V2Rs, with few TAARs, V1Rs and ORs genes It is not precisely known which receptor is expressed by each sensory cell type migrate from placode to hypothalamus, but this has only been demonstrated in chicken migrate from olfactory placode to hypothalamus and pre-optic area. The possible contribution of neural crest to other cell types in the olfactory placode such as the GnRH neurons is debated and controversial, and there is no coherent vision on the lineage origin of the major neural cell types royalsocietypublishing.org/journal/rsob Open Biol. Precise lineage cell-tracing data in zebrafish argue against a contribution from the neural crest and support the view that all the different neuronal populations within the olfactory epithelium originate from overlapping pools of progenitors in the PPE [19]. It is possible these apparently conflicting reports reflect genuine differences between species
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