Expression Dynamics and Protein Localization of Rhabdomeric Opsins in Platynereis Larvae

Nadine Randel,Réza Shahidi,Martin Gühmann,Luis A Bezares-Calderón,Gáspár Jékely

doi:10.1093/icb/ict046

Abstract

The larval stages of polychaete annelids are often responsive to light and can possess one to six eyes. The early trochophore larvae of the errant annelid Platynereis dumerilii have a single pair of ventral eyespots, whereas older nectochaete larvae have an additional two pairs of dorsal eyes that will develop into the adult eyes. Early Platynereis trochophores show robust positive phototaxis starting on the first day of development. Even though the mechanism of phototaxis in Platynereis early trochophore larvae is well understood, no photopigment (opsin) expression has yet been described in this stage. In late trochophore larvae, a rhabdomeric-type opsin, r-opsin1, expressed in both the eyespots and the adult eyes has already been reported. Here, we identify another Platynereis rhabdomeric opsin, r-opsin3, that is expressed in a single photoreceptor in the eyespots in early trochophores, suggesting that it mediates early larval phototaxis. We also show that r-opsin1 and r-opsin3 are expressed in adjacent photoreceptor cells in the eyespots in later stages, indicating that a second eyespot-photoreceptor differentiates in late trochophore larvae. Using serial transmission electron microscopy (TEM), we identified and reconstructed both photoreceptors and a pigment cell in the late larval eyespot. We also characterized opsin expression in the adult eyes and found that the two opsins co-express there in several photoreceptor cells. Using antibodies recognizing r-opsin1 and r-opsin3 proteins, we demonstrate that both opsins localize to the rhabdomere in all six eyes. In addition, we found that r-opsin1 mRNA is localized to, and translated in, the projections of the adult eyes. The specific changes we describe in opsin transcription and translation and in the cellular complement suggest that the six larval eyes undergo spectral and functional maturation during the early planktonic phase of the Platynereis life cycle.

Highlights

Positive phototaxis of early larval stages is a widespread phenomenon among marine invertebrates, characteristic of approximately 80% of the benthic invertebrates with a pelagic larva (Thorson 1964)
The early trochophore larvae of the errant annelid Platynereis dumerilii have a single pair of ventral eyespots, whereas older nectochaete larvae have an additional two pairs of dorsal eyes that will develop into the adult eyes
A rhabdomeric-type opsin, r-opsin1, expressed in both the eyespots and the adult eyes has already been reported. We identify another Platynereis rhabdomeric opsin, r-opsin3, that is expressed in a single photoreceptor in the eyespots in early trochophores, suggesting that it mediates early larval phototaxis

Summary

Introduction

Positive phototaxis of early larval stages is a widespread phenomenon among marine invertebrates, characteristic of approximately 80% of the benthic invertebrates with a pelagic larva (Thorson 1964). Simple larval eyes are widespread among marine invertebrates and have been characterized morphologically in the larval stages of sponges (Leys and Degnan 2001), cnidarians (Nordstrom et al 2003), annelids (Bartolomaeus 1992a), mollusks (Bartolomaeus 1992b), nemerteans (Dohren and Bartolomaeus 2007), flatworms (Eakin and Brandenburger 1981), brachiopods (Passamaneck et al 2011), hemichordates (Brandenburger et al 1973), cephalochordates (Lacalli 1996), and crustaceans (Lacalli 2009). A better understanding of the molecular and functional characteristics of the eyes of larval marine invertebrates would allow a more reliable reconstruction of early stages of evolution of eyes in bilaterians, because the eyes of some larvae may have retained an ancestral organization (Arendt and Wittbrodt 2001; Jekely et al 2008).

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