Volvoxrhodopsin, a Light-Regulated Sensory Photoreceptor of the Spheroidal Green Alga Volvox carteri

Abstract

Somatic cells of the multicellular alga Volvox carteri contain a visual rhodopsin that controls the organism's phototactic behavior via two independent photoreceptor currents. Here, we report the identification of an opsinlike gene, designated as volvoxopsin (vop). The encoded protein exhibits homologies to the opsin of the unicellular alga Chlamydomonas reinhardtii (chlamyopsin) and to the entire animal opsin family, thus providing new perspectives on opsin evolution. Volvoxopsin accumulates within the eyes of somatic cells. However, the vop transcript is detectable only in the reproductive eyeless gonidia and embryos. vop mRNA levels increase 400-fold during embryogenesis, when embryos develop in darkness, whereas the vop transcript does not accumulate when embryos develop in the light. An antisense transformant, T3, was generated. This transformant produces 10 times less volvoxopsin than does the wild type. In T3, the vop transcript is virtually absent, whereas the antisense transcript is predominant and light regulated. It follows that vop expression is under light-dependent transcriptional control but that volvoxopsin itself is not the regulatory photoreceptor. Transformant T3 is phototactic, but its phototactic sensitivity is reduced 10-fold relative to the parental wild-type strain HK10. Thus, we offer definitive genetic evidence that a rhodopsin serves as the photoreceptor for phototaxis in a green alga.

Sea urchin tube feet are photosensory organs that express a rhabdomeric-like opsin and PAX6

“…This inverse relationship between light and opsin expression also occurs in the multi-cellular alga Volvox carteri, where the expression of an opsin (i.e. channelrhodopsin) homologous to animal opsins is inversely related to the amount of light the alga is exposed to, and is also used for phototaxis by the alga [53]. Similarly, the differential expression of the green sea urchin opsin in tube feet may be an important component of a sea urchin's ability to photoacclimatize to different irradiances on multiple timeframes to regulate the phototransduction of this external stimulus for important organismal functions, such as gametogenesis [3].…”

Algal photoreceptors: in vivo functions and potential applications

“…Like CR1 and CR2, VR1 also belongs to the family of animal-type rhodopsins. It was proposed that VR1 is localized in the eyespot apparatus of somatic cells and serves as the light receptor in phototactic responses (Ebnet et al 1999). But surprisingly, the transcript of VR1 was mainly expressed both in the eyeless reproductive cells and in embryos of V. carteri, whereas the parental somatic cells showed only minor expression of VR1 (Ebnet et al 1999).…”

“…Later, a rhodopsin homologous to CR2, volvoxrhodopsin-1 (VR1 or Vop), was identified in V. carteri (Fig. 7) (Ebnet et al 1999), which shows 61 % sequence identity to CR2. Like CR1 and CR2, VR1 also belongs to the family of animal-type rhodopsins.…”

“…It was proposed that VR1 is localized in the eyespot apparatus of somatic cells and serves as the light receptor in phototactic responses (Ebnet et al 1999). But surprisingly, the transcript of VR1 was mainly expressed both in the eyeless reproductive cells and in embryos of V. carteri, whereas the parental somatic cells showed only minor expression of VR1 (Ebnet et al 1999). The reason for these observations was unclear until Yuishiro Takahashi's group reported in 2009 that the homologous protein, CR2 from Chlamydomonas, forms a 1:1 complex with the chaperone Ycf4 and is likely to be involved in the assembly and biogenesis of photosystem I (Ozawa et al 2009).…”

Historical perspective on the development and evolution of eyes and photoreceptors

“…The most primitive organism in which a rhodopsin has been found which may be related to animal opsins is Volvox, a colonial green alga in the transition zone between protists and multicellular organism. The primary amino acid sequence of Volvoxrhodopsin matches 10 out of 27 residues in a consensus sequence of the retinal binding site with a group of invertebrate rhodopsins (Ebnet et al, 1999). Volvox is a sphere formed by individual flagellates each equipped with an "eye spot" located in the thylacoid membranes of their chloroplast (Fig.…”