By LeeAnn Louie (Scripps College) and Vanessa Ho (Pomona College) [edited by Lars Schmitz, as part of BIOL 167 “Sensory Evolution”, an upper division class at the Claremont Colleges]
Photoreceptors are the receptors for visual information and thus, unsurprisingly, are present in eyes. Specifically, the two types of photoreceptors, the rods and cones, are buried on the retina at the back of the eye. As light enters the eye through the pupil, the iris controls the size of the pupil to protect the eye from too much excess brightness. The light is then focused onto the retina where the photoreceptors convert the light signals into electrical ones interpretable by the brain. As important as the initial steps in the light’s pathway to the retina are, the photoreceptors are what enable us to see a range of light and colors. So their location deep within the eye seems logical. However, it turns out that there are a few examples of the occurrence of functional photoreceptors outside from proper eyes. The pineal organ in some vertebrataes is one such example. Another example is provided by Backfisch et al. 2013. In successfully labeling r-opsin (a marker for photoreceptors) in the annelid worm Platynereis dumereilii, Backfisch and his team found additional photoreceptors in the ventral nerve cord and segmental dorsal appendages, and not just in the eye-cups as previously expected. The researchers conducted many experiments related to r-opsin expression in the trunk but most surprisingly, upon decapitation, the trunk of Platynereis still demonstrated photoavoidance despite the fact the eyes had been removed.
Platynereis is a marine annelid worm that is a key species for studying eye and brain development in basal metazoans. Thus the ability to see the expression of key components in brains and eyes makes Backfisch’s experiment useful for further research in Platynereis. They performed transgenesis to co-express EGFP, an enhanced version of the green fluorescent protein (GFP), in regulatory regions of r-opsin, allowing for visibility of all photoreceptors in the annelid. While they did find photoreceptors in the eyespots and correlated eyelets in the brain as anticipated, they also found further expression of photoreceptors on other parts of the body than the head. When they exposed a dim-light-adapted trunk to a light stimulus, the tail moved away from the light as far as 4 mm (a long distance for an animal of about 20-25 mm in total length!) even in the absence of a brain or eyes.
Further investigations into the developmental genetics of these newly identified photoreceptors revealed that these non-cephalic (located outside of the head) photoreceptors do not develop under the same regulatory genes as those in vertebrate eyes. This is shown by the distinctly separate expression of r-opsin and pax6, a transcriptional regulator involved in eye development in chordates. Instead, these photoreceptors were found to coexpress dach, which is associated with eye development, pax2/5/8, which regulate neural differentiation, and brn3c, which is expressed in sensory neuron development. These findings suggest that the trunk photoreceptors may have different evolutionary origins from other photoreceptors expressing pax6, but may be related to cephalochordate photoreceptors, which are associated with dach, pax2/5/8, and brn3c.
While the genetics of non-cephalic photoreceptors can clarify developmental relations, the expression of r-opsin in zebrafish, a vertebrate, shows striking similarity to that of Platynereis. The correlation between brn3c and r-opsin expression in Platynereis prompted Backfisch et al. to label r-opsin orthologs in zebrafish, which revealed the presence of these photoreceptor markers in the neuromasts, mechanosensory cells of the lateral line associated with body orientation, and neurons of the peripheral nervous system. This suggests a developmental, and possibly evolutionary relationship between photoreceptors and mechanoreceptors. While expression in Platynereis shows the presence of photoreceptors outside of eyes, characteristic photoreceptor markers are found in other non-cephalic sensory cells in a vertebrate species.
Similar to zebrafish, photoreceptor markers are also found in mechanosensory cells in the auditory organ (Johnston’s organ) of Drosophila melanogaster. Upon screening genes involved in hearing, Senthilan and his team suggest that Drosophila r-opsin play a critical role of mechanotransduction channel gating in auditory function. Furthermore, the development of many sensory organs in Drosophila are governed by the atonal gene suggesting common evolutionary origins in which a protosensory organ eventually diversified into the many different sensory organs metazoans have today.
Backfisch et al. posits that photoreceptors and mechanorecptors have a common evolutionary origin, but Smith summarizes in his textbook that mechanoreceptors, given their presence in organisms as simple as bacteria, are the true sensory precursors. He also notes that transmembrane signalling in mechanoreceptors are present across the clades indicating a likely common evolutionary origin early on. It is unclear which hypothesis, if either, is correct. The finding that r-opsin are present in mechanosensory organs despite that these organs do not require photosensitive information presents an interesting conundrum. This area of research would certainly benefit from studies into the molecular basis of these receptors across species to better pinpoint evolutionary origins.
Though the current findings add insightful contributions to the possible developmental and evolutionary origins of photoreceptors, eyes and other sensory organs, the induction of stable transgenesis perhaps holds more research potential in Platynereis. Specifically, the present study illustrates how stable transgenesis in Platynereis can contribute to the growing field of developmental and evolutionary biology by providing an in-depth characterization of the labeled cell types under investigation. Additionally, Backfisch et al. are hopeful that other assays will also be considered when investigating the photoreceptors associated in photoavoidance or hormonal activity. This current study elucidates the “molecular fingerprint” of noncephalic photoreceptors and strives to uncover their evolutionary origins.
- Backfisch, B, et al. “Stable transgenesis in the marine annelid Platynereis dumerilli sheds new light on photoreceptor evolution.” PNAS. 110.1 2012. 193-198.
- Senthilan, P.R. et al. “Drosophila Auditory Organ Genes and Genetic Hearing Defects.” Cell. 150.5 (2012): 1042–1054. Web. 15 Mar. 2013.
- Smith, Christopher. Biology of Sensory Systems. 2nd edition. Wiley, 2009. 75.