Fitzpatrick, David A. and O'Halloran, Damien M. and Burnell, Ann M.
Multiple lineage specific expansions within the guanylyl cyclase gene family.
BMC Evolutionary Biology, 6.
Background: Guanylyl cyclases (GCs) are responsible for the production of the secondary
messenger cyclic guanosine monophosphate, which plays important roles in a variety of
physiological responses such as vision, olfaction, muscle contraction, homeostatic regulation,
cardiovascular and nervous function. There are two types of GCs in animals, soluble (sGCs) which
are found ubiquitously in cell cytoplasm, and receptor (rGC) forms which span cell membranes.
The complete genomes of several vertebrate and invertebrate species are now available. These
data provide a platform to investigate the evolution of GCs across a diverse range of animal phyla.
Results: In this analysis we located GC genes from a broad spectrum of vertebrate and
invertebrate animals and reconstructed molecular phylogenies for both sGC and rGC proteins.
The most notable features of the resulting phylogenies are the number of lineage specific rGC and
sGC expansions that have occurred during metazoan evolution. Among these expansions is a large
nematode specific rGC clade comprising 21 genes in C. elegans alone; a vertebrate specific
expansion in the natriuretic receptors GC-A and GC-B; a vertebrate specific expansion in the
guanylyl GC-C receptors, an echinoderm specific expansion in the sperm rGC genes and a
nematode specific sGC clade. Our phylogenetic reconstruction also shows the existence of a basal
group of nitric oxide (NO) insensitive insect and nematode sGCs which are regulated by O2. This
suggests that the primordial eukaryotes probably utilized sGC as an O2 sensor, with the ligand
specificity of sGC later switching to NO which provides a very effective local cell-to-cell signalling
system. Phylogenetic analysis of the sGC and bacterial heme nitric oxide/oxygen binding protein
domain supports the hypothesis that this domain originated from a cyanobacterial source.
Conclusion: The most salient feature of our phylogenies is the number of lineage specific expansions, which have occurred within the GC gene family during metazoan evolution. Our phylogenetic analyses reveal that the rGC and sGC multi-domain proteins evolved early in eumetazoan evolution. Subsequent gene duplications, tissue specific expression patterns and lineage specific expansions resulted in the evolution of new networks of interaction and new biological functions associated with the maintenance of organismal complexity and homeostasis.
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