Divergence in cis-regulatory sequences surrounding the opsin gene arrays of African cichlid fishes

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Date
2011-05-09Author
O'Quin, Kelly E
Smith, Daniel
Naseer, Zan
Schulte, Jane
Engel, Sanuel D
Loh, Yong-Hwee E
Streelman, J Todd
Boore, Jeffrey L
Carleton, Karen L
Citation
O’Quin et al. BMC Evolutionary Biology 2011, 11:120 http://www.biomedcentral.com/1471-2148/11/120
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Show full item recordAbstract
Background: Divergence within cis-regulatory sequences may contribute to the adaptive evolution of gene
expression, but functional alleles in these regions are difficult to identify without abundant genomic resources.
Among African cichlid fishes, the differential expression of seven opsin genes has produced adaptive differences in
visual sensitivity. Quantitative genetic analysis suggests that cis-regulatory alleles near the SWS2-LWS opsins may
contribute to this variation. Here, we sequence BACs containing the opsin genes of two cichlids, Oreochromis
niloticus and Metriaclima zebra. We use phylogenetic footprinting and shadowing to examine divergence in
conserved non-coding elements, promoter sequences, and 3’-UTRs surrounding each opsin in search of candidate
cis-regulatory sequences that influence cichlid opsin expression.
Results: We identified 20 conserved non-coding elements surrounding the opsins of cichlids and other teleosts,
including one known enhancer and a retinal microRNA. Most conserved elements contained computationallypredicted binding sites that correspond to transcription factors that function in vertebrate opsin expression;
O. niloticus and M. zebra were significantly divergent in two of these. Similarly, we found a large number of
relevant transcription factor binding sites within each opsin’s proximal promoter, and identified five opsins that
were considerably divergent in both expression and the number of transcription factor binding sites shared
between O. niloticus and M. zebra. We also found several microRNA target sites within the 3’-UTR of each opsin,
including two 3’-UTRs that differ significantly between O. niloticus and M. zebra. Finally, we examined interspecific
divergence among 18 phenotypically diverse cichlids from Lake Malawi for one conserved non-coding element,
two 3’-UTRs, and five opsin proximal promoters. We found that all regions were highly conserved with some
evidence of CRX transcription factor binding site turnover. We also found three SNPs within two opsin promoters
and one non-coding element that had weak association with cichlid opsin expression.
Conclusions: This study is the first to systematically search the opsins of cichlids for putative cis-regulatory
sequences. Although many putative regulatory regions are highly conserved across a large number of
phenotypically diverse cichlids, we found at least nine divergent sequences that could contribute to opsin
expression differences in cis and stand out as candidates for future functional analyses.