Abstract
Photoreceptor cells in the eyes of Bilateria are often classified into microvillar cells with rhabdomeric opsin and ciliary cells with ciliary opsin, each type having specialized molecular components and physiology. First data on the recently discovered xenopsin point towards a more complex situation in protostomes. In this study, we provide clear evidence that xenopsin enters cilia in the eye of the larval bryozoan Tricellaria inopinata and triggers phototaxis. As reported from a mollusc, we find xenopsin coexpressed with rhabdomeric-opsin in eye photoreceptor cells bearing both microvilli and cilia in larva of the annelid Malacoceros fuliginosus. This is the first organism known to have both xenopsin and ciliary opsin, showing that these opsins are not necessarily mutually exclusive. Compiling existing data, we propose that xenopsin may play an important role in many protostome eyes and provides new insights into the function, evolution, and possible plasticity of animal eye photoreceptor cells.
Highlights
The photoreceptor cells (PRCs) in animal eyes are often classified according to their structure, that is depending on whether the sensory surface is enlarged by microvilli or by cilia (Eakin, 1979; Eakin, 1963; Eakin, 1968)
The first type of PRCs in many protostomes was shown to depolarize in response to light and to employ rhabdomeric opsin (r-opsin) as a visual pigment, which signals via the Gaq mediated IP3 cascade opening TRP ion channels in the PRC membrane (Fain et al, 2010; Shichida and Matsuyama, 2009)
Xenopsin seems to be an important visual pigment in protostome eyes. This opsin type was overlooked for a long time, probably because most molecular data on protostome light perception are from arthropods, which secondarily lost xenopsin
Summary
The photoreceptor cells (PRCs) in animal eyes are often classified according to their structure, that is depending on whether the sensory surface is enlarged by microvilli or by cilia (Eakin, 1979; Eakin, 1963; Eakin, 1968). Ciliary PRCs of vertebrate eyes are known to signal via the Gai/t mediated cGMP cascade closing CNG channels and leading to a hyperpolarization Since both are found in protostome and deuterostome animals and due to their distinct molecular signatures, it is assumed that these two kinds of PRCs were already present in the last common ancestor of bilaterian animals (Arendt, 2008; Arendt et al, 2004; Arendt et al, 2002; Gomez et al, 2009; Gehring, 2014; Nasi and Gomez, 2009; Panda et al, 2002). We present data suggesting that in protostomes, an additional second kind of ciliary PRCs is widespread and that this may be evolutionarily closer to microvillar PRCs than to vertebrate ciliary eye PRCs
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