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J M Nickerson, Natecia Williams, Shannon Getz, Micah A Chrenek, Jeffrey H Boatright; Coincident birth of the IRBP gene and the vertebrate eye. Invest. Ophthalmol. Vis. Sci. 2014;55(13):1279.
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© ARVO (1962-2015); The Authors (2016-present)
The vertebrate eye is more efficient than the invertebrate in several ways. IRBP co-evolved with these improvements over the invertebrate eye. In 1989, we predicted that the unusual structure of the IRBP gene derived from an internal quadruplication of a much smaller ancestral single-repeat gene that had not previously functioned in vision (Borst et al J Biol Chem 264:1115-23). In 2006, we predicted that IRBP took on a new visual function by exaptation early in the appearance of the vertebrate eye, and we predicted that vertebrates have a "classic tetrapod" style IRBP gene (Nickerson et al Mol Vis 12:1565-85). To test these predictions, we are now analyzing IRBP protein, mRNA, and gene sequences of many vertebrates, including the coelacanth, spotted gar, lamprey, and amphioxus, a pre-vertebrate chordate.
Sequence data from more than 200 vertebrate species were obtained from databases (NCBI, Ensembl, GenomeWIKI, JGI, BGI, etc). Preliminary reverse transcriptase PCRs and RNA fluorescence ISH were undertaken with the Florida lancelet.
We found that all analyzed vertebrate genes are almost identical to the "classic tetrapod” IRBP gene, with four repeats of 300 amino acids each. The first exon is always large (~1 kb) and encodes all the first three repeats and part of the fourth repeat. The remaining fourth repeat is split among Exons 2, 3, and 4. The only violations of the these rules are in the teleost fish, which contains either a single "Gene 2" or a "Gene 1 and Gene 2" tandem IRBP gene pair as previously established (Nickerson et al. 2006). The pre-teleost fishes, the coelacanth and spotted gar, have the "classic tetrapod" gene, establishing that the teleost IRBP locus arose from an ancestral "classic tetrapod" gene. Also, the lamprey has the "classic tetrapod" IRBP gene structure. Critically, the IRBP gene of amphioxus, a pre-vertebrate chordate, is very different from the vertebrate: it contains only one repeat, and has at least 8 exons.
Our analyses bracket the appearance of the “classic tetrapod” IRBP gene between the divergence from the lancelet, a chordate, and the lamprey, an early vertebrate, roughly 540 Myr ago. IRBP's appearance coincides with the beginnings of a Darwinian “intermediate form" of the eye, an eyespot with an RPE and primitive ciliated photoreceptors at about 90° in the lancelet. Whether coincidental or causal in eye evolution, we wonder whether lancelet IRBP functions in vision.
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