Abstract

The ocelloid is an extraordinary eyespot organelle found only in the dinoflagellate family Warnowiaceae. It contains retina- and lens-like structures called the retinal body and the hyalosome. The ocelloid has been an evolutionary enigma because of its remarkable resemblance to the multicellular camera-type eye. To determine if the ocelloid is functionally photoreceptive, we investigated the warnowiid dinoflagellate Erythropsidinium. Here, we show that the morphology of the retinal body changed depending on different illumination conditions and the hyalosome manifests the refractile nature. Identifying a rhodopsin gene fragment in Erythropsidinium ESTs that is expressed in the retinal body by in situ hybridization, we also show that ocelloids are actually light sensitive photoreceptors. The rhodopsin gene identified is most closely related to bacterial rhodopsins. Taken together, we suggest that the ocelloid is an intracellular camera-type eye, which might be originated from endosymbiotic origin.

Highlights

  • The evolution of the eye has been of special interest in discussing the origin of complex organs

  • We have focused on the ocelloid of Erythropsidinium spp. for the following two reasons: (i) We can regularly collect a relatively large number of specimens of this species from coastal water in Japan and (ii) the ocelloid of Erythropsidinium is larger in size than in the other two genera of warnowiids[7], making it easier to handle experimentally

  • Our results demonstrate that the ocelloid changes its structure in response to changing illumination and that the retinal body is destroyed by strong illumination

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Summary

Introduction

The evolution of the eye has been of special interest in discussing the origin of complex organs. To examine Darwin’s hypothesis, the evolutionary transition of eye form has been studied in various systems, e.g., the pit eyes of worms, and mollusks, and the complex camera-type eyes of vertebrates. Those studies are restricted to eumetazoan animals[2]. Diverse types of photoreceptive organs have been observed at every level of structural design and ontogenetic origin In spite of such enormous diversity, an eye can be defined as a photoreceptor shielded on one side by pigment which allows the detection of a source of light and its direction[3]. Based on this simple definition of PLOS ONE | DOI:10.1371/journal.pone.0118415 March 3, 2015

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