Limian Zheng and John James Mackrill
Calcium ions are utilised as a second messenger in all forms of cellular life. In contrast to bacteria and archaea, eukaryotes possess endomembrane systems, exemplified by the endoplasmic reticulum. Such organelles act as intracellular stores in Ca2+ signalling processes, with two distantly related calcium channels, the inositol 1,4,5- trisphosphate receptors and ryanodine receptors, acting as Ca2+ release mechanisms. Despite their fundamental role, the evolutionary origins of such Ca2+ release channels have proven difficult to elucidate. The current study presents updates on the phylogeny of this channel superfamily and analyses of the domain architectures of these proteins. We demonstrate that inositol 1,4,5-trisphosphate receptor homologues are present in every major taxonomic group of eukaryotic life, suggesting that they were utilised early on in the evolution of these organisms. Certain taxonomic groups contain multiple Ca2+ release channel homologues, suggesting expansion and diversification. Early diverging fungi and green plants contain a single canonical inositol 1,4,5-trisphosphate receptor, which is absent in later branching members, suggesting loss from at least two distinct lineages. A key difference in the protein architecture of the two channel families is the presence or absence of ryanodine receptor domains. Such ryanodine receptor domains occur in multiple families of proteins present in eukaryotes, bacteriophage viruses, bacteria and archaea. In eukaryotes, canonical ryanodine receptors are first detected in the choanoflagellate/metazoan lineage, but a distinct family of ryanodine receptor domain-containing proteins with the potential to form cation channels, that we name the ‘PKD-RR’ family, are conserved among oomycetes. Modelling of the tertiary structures of ryanodine receptor domains from viruses, bacteria, fungi and oomycetes indicates that they are likely to closely resemble those from mammalian ryanodine receptor channels. We also present evidence that horizontal gene transfer has occurred during the evolution of ryanodine receptor domain-containing proteins, thereby contributing to calcium release channel structural and functional diversity.
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Journal of Phylogenetics & Evolutionary Biology received 911 citations as per Google Scholar report
