Developmental gene expression in the eyes of the pygmy squid Xipholeptos notoides

Abstract

The eyes of squids, octopuses, and cuttlefish are a textbook example for evolutionary convergence, due to their striking similarity to those of vertebrates. For this reason, studies on cephalopod photoreception and vision are of importance for a broader audience. Previous studies showed that genes such as pax6, or certain opsin-encoding genes, are evolutionarily highly conserved and play similar roles during ontogenesis in remotely related bilaterians. In this study, genes that encode photosensitive proteins and Reflectins are identified and characterized. The expression patterns of rhodopsin, xenopsin, retinochrome, and two reflectin genes have been visualized in developing embryos of the pygmy squid Xipholeptos notoides by in situ hybridization experiments. Rhodopsin is not only expressed in the retina of X. notoides but also in the olfactory organ and the dorsal parolfactory vesicles, the latter a cephalopod apomorphy. Both reflectin genes are expressed in the eyes and in the olfactory organ. These findings corroborate previous studies that found opsin genes in the transcriptomes of the eyes and several extraocular tissues of various cephalopods. Expression of rhodopsin, xenopsin, retinochrome, and the two reflectin genes in the olfactory organ is a finding that has not been described so far. In other organisms, it has been shown that Retinochrome and Rhodopsin proteins are obligatorily associated with each other as both molecules rely on each other for Retinal isomerisation. In addition, we demonstrate that retinochrome is expressed in the retina of X. notoides and in the olfactory organ. This study shows numerous new expression patterns for Opsin-encoding genes in organs that have not been associated with photoreception before, suggesting that either Opsins may not only be involved in photoreception or organs such as the olfactory organ are involved in photoreception.