MBE Advance Access published online on March 25, 2009
Molecular Biology and Evolution, doi:10.1093/molbev/msp060
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Research Article |
Calcium-activated potassium (BK) channels are encoded by duplicate slo1 genes in teleost fishes
Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853
Contact Information: Kevin N. Rohmann, Department of Neurobiology and Behavior, W233 Mudd Hall, Tower Road, Ithaca, NY 14853, Tel: 607-254-4373, Fax: 607-254-1303, Email: knr9{at}cornell.edu
Received for publication February 6, 2009. Revision received March 18, 2009. Accepted for publication March 21, 2009.
Calcium-activated, large conductance potassium (BK) channels in tetrapods are encoded by a single slo1 gene, which undergoes extensive alternative splicing. Alternative splicing generates a high level of functional diversity in BK channels that contributes to the wide range of frequencies electrically tuned by the inner ear hair cells of many tetrapods. To date, the role of BK channels in hearing among teleost fishes has not been investigated at the molecular level, although teleosts account for approximately half of all extant vertebrate species. We identified slo1 genes in teleost and non-teleost fishes using PCR and genetic sequence databases. In contrast to tetrapods, all teleosts examined were found to express duplicate slo1 genes in the central nervous system, while non-teleosts that diverged prior to the teleost whole genome duplication event express a single slo1 gene. Phylogenetic analyses further revealed that while other slo1 duplicates were the result of a single duplication event, an independent duplication occurred in a basal teleost (Anguilla rostrata) following the slo1 duplication in teleosts. A third, independent slo1 duplication (autotetraploidization) occurred in salmonids. Comparison of teleost slo1 genomic sequences to their tetrapod orthologue revealed a reduced number of alternative splice sites in both slo1 co-orthologues. For the teleost Porichthys notatus, a focal study species that vocalizes with maximal spectral energy in the range electrically tuned by BK channels in the inner ear, peripheral tissues show the expression of either one (e.g. vocal muscle) or both (e.g. inner ear) slo1 paralogues with important implications for both auditory and vocal physiology. Additional loss of expression of one slo1 paralogue in non-neural tissues in P. notatus suggests that slo1 duplicates were retained via subfunctionalization. Together, the results predict that teleost fish achieve a diversity of BK channel subfunction via gene duplication, rather than increased alternative splicing as witnessed for the tetrapod and invertebrate orthologue.
Key Words: BK channels • hearing • gene duplications