Selective Gene Loss of Visual and Olfactory Guanylyl Cyclase Genes Following the Two Rounds of Vertebrate-Specific Whole-Genome Duplications

Abstract

Photoreceptors convey visual information and come in two flavours; dim-light and bright-light dedicated rod and cones. Both cell types feature highly specialized phototransduction cascades that convert photonic energy into intracellular signals. While a substantial amount of phototransduction gene ohnologs are expressed either in rods or cones, visual guanylyl cyclases (GCs) involved in the calcium (Ca2+) dependent feedback regulation of phototransduction are neither rod nor cone specific. The co-existence of visual GCs in both photoreceptor types suggests that specialization of these ohnologs occurred despite their overlapping expression. Here, we analyse gene retention and inactivation patterns of vertebrate visual and closely related olfactory GCs following two rounds (2R) of vertebrate specific whole genome duplication events (2R WGD). While eutherians generally use two visual and one olfactory GCs, independent inactivation occurred in some lineages. Sauropsids (birds, lizards, snakes, turtles and crocodiles) generally have only one visual GC (GC-E). Additionally turtles (testodes) also lost the olfactory GC (GC-D). Pseudogenization in mammals occurred in specific species/families likely according to functional needs (i.e. many species with reduced vision only have GC-E). Likewise, some species not relying on scent marks lack GC-D, the olfactory GC enzyme. Interestingly, in the case of fish, no species can be found with fewer than three (two visual and one olfactory) genes and the teleost specific 3R WGD can increase this number to up to five. This suggests that vision in fish now requires at least two visual GCs.

Evolution of visual guanylyl cyclases and their activating proteins with respect to clade and species-specific visual system adaptation

“…In a previous study we have investigated the preservation, inactivation and possible functional adaptation of guanylyl cyclase genes across more than 300 different vertebrate species ( Gesemann and Neuhauss, 2020 ). We have shown that eutherians commonly use two visual GCs, namely GC-E and GC-F.…”

“…In the tetrapod lineage two visual (GC-E and GC-F) and one phylogenetically closely related olfactory guanylyl cyclase receptor (GC-D) have been identified ( Lamb and Hunt, 2018 ; Gesemann and Neuhauss, 2020 ). While GC-E is expressed in rods and cones ( Dizhoor et al, 1994 ), GC-F is predominantly expressed in rods ( Yang et al, 1995 ; Yang and Garbers, 1997 ).…”

“…In a previous study we have analyzed the evolution of guanylyl cyclase following the two rounds of WGD ( Gesemann and Neuhauss, 2020 ). Some clades and isolated species lack either GC-F, GC-D or both receptors relying on a single membrane linked cyclase to control the calcium feedback system of phototransduction.…”

Biochemistry and physiology of zebrafish photoreceptors

“…The generation, deletion, and fate of these duplicated genes add a fascinating complexity to the teleost visual transduction cascade that is beyond the scope of this review. However, the multitude of gene variants to be discussed in the following is the direct consequence of whole-genome duplications in the past [ 63 , 103 , 104 , 106 , 99 , 100 , 60 ].…”

“…Mammals have two photoreceptor-specific GCs, GC-E (known as GC1) and GC-F (known as GC2), both of which are co-expressed in rods and cones [ 103 , 88 , 60 ]. GC-E is more concentrated in cones, while the expression of GC-F is more prominent in rods.…”