Remodeling of the Cone Photoreceptor Mosaic during Metamorphosis of Flounder <i>(Pseudopleuronectes americanus)</i>

Abstract

The retinal cone mosaic of the winter flounder, Pseudopleuronectes americanus, is extensively remodeled during metamorphosis when its visual system shifts from monochromatic to trichromatic. Here we describe the reorganization and re-specification of existing cone subtypes in which larval cones alter their spatial arrangement, morphology, and opsin expression to determine whether mechanisms controlling cell birth, mosaic position, and opsin selection are coordinated or independent. We labeled dividing cells with tritiated (³H) thymidine prior to mosaic remodeling to determine whether existing cone photoreceptors change phenotype. We also used in situ hybridization to identify mosaic type and opsin expression in transitional retinas to understand the sequence of transformation. Our data indicate that in the winter flounder retina the choice of new opsin species and the cellular rearrangement of the mosaic proceed independently. The production of the precise cone mosaic arrangement is not due to a stereotyped series of sequential cellular inductions, but rather might be the product of a set of distinct, flexible processes that rely on plasticity in cell phenotype.

Thyroid hormone accelerates opsin expression during early photoreceptor differentiation and induces opsin switching in differentiated TRα‐expressing cones of the salmonid retina

“…In the winter flounder, for instance, increased levels of thyroid hormone and TRa are required to generate a new complement of photoreceptors as metamorphosis progresses (Mader and Cameron, 2006). Premetamorphic flounder express only green (RH2) opsin in cone photoreceptors, whereas postmetamorphic flounder express two additional opsins, red (LWS) and blue (SWS2), in specific cone types that are morphologically distinct from premetamorphic cones (Hoke et al, 2006).…”

Chromatic organization of cone photoreceptors in the retina of rainbow trout: single cones irreversibly switch from UV (SWS1) to blue (SWS2) light sensitive opsin during natural development

“…In flatfishes (e.g. the winter flounder) (Hoke et al, 2006), metamorphosis involves a complete re-arrangement of the cone mosaic and expression of novel opsins in various cone types. Since thyroid hormone levels are elevated during this time of transformation (Inui and Miwa, 1985), it is likely that the primary role of this hormone in the retina is to regulate opsin expression, as in the mouse.…”

“…Hárosi, 1994;Ebrey and Koutalos, 2001). Though recent work has greatly advanced our understanding of the role that some receptors and their ligands play in regulating opsin expression (Prabhudesai et al, 2005;Roberts et al, 2005;Roberts et al, 2006;Srinivas et al, 2006;Mader and Cameron, 2006;Applebury et al, 2007), the molecular mechanisms that establish the chromatic organization of cone mosaics are not understood, and the plasticity in opsin expression within varying mosaics has only recently begun to be investigated (Shand et al, 2002;Parry et al, 2005;Hoke et al, 2006;Cheng et al, 2006).…”

Pronounced heritable variation and limited phenotypic plasticity in visual pigments and opsin expression of threespine stickleback photoreceptors

“…Modulation of opsin expression has also been documented during development (Wood and Partridge, 1993;Szél et al, 1994;Xiao and Hendrickson, 2000;Cheng and Novales Flamarique, 2004;Takechi and Kawamura, 2005;Spady et al, 2006;Hoke et al, 2006;Applebury et al, 2007;Shand et al, 2008;Cottrill et al, 2009) and, to a lesser extent, following changes in habitat (Fuller et al, 2005;Shand et al, 2008;Cottrill et al, 2009;Hofmann et al, 2010;Fuller and Claricoates, 2011). Studies using fishes and rodents have demonstrated that opsin switching within individual cones is a major mechanism that restructures the chromatic organization of the retina and the colour sensitivity of these animals during development and at early life stages (Szél et al, 1994;Cheng et al, 2006;Novales Flamarique, 2013).…”

“…It thus seems that the reported phenotypic plasticity in opsin expression of fishes is probably based on changes in the relative numbers of spectral cone types. Such alterations in cell numbers can arise via the production and/or pruning of photoreceptors, as occurs in several species (Cornish et al, 2004;Cheng et al, 2006;Hoke et al, 2006;Chen et al, 2008;Hu et al, 2011), or as a switch in the opsin expressed within individual photoreceptors, as has been demonstrated in the rods of the European eel (Wood and Partridge, 1993) and in the cones of salmonid fishes and rodents (Szél et al, 1994;Cheng et al, 2006, Cheng andGlaschke et al, 2011). The importance of opsin phenotypic plasticity in colour sensitivity, and visual function in general, would then depend on the number and types of cones affected and their retinal distributions.…”