Light-dependent changes in the positioning of organelles in photoreceptor cells of arthropods are a well-known phenomenon. In this study, we examine the role of the cytoskeleton in these light-dependent antagonistic movements. In dark-adapted photoreceptor cells of the locust Schistocerca gregaria, prominent sacs of smooth endoplasmic reticulum (ER) oppose the bases of the photoreceptive microvilli. Light stimulation causes a translocation of the ER elements towards the main cell body, and an aggregation of mitochondria adjacent to the microvilli. Immunofluorescence studies and electron-microscopic examination of chemically fixed or high-pressure-frozen, freeze-substituted specimens demonstrate a lack of microtubules in the submicrovillar region. However, numerous filament bundles are aligned in close association with mitochondria and ER elements, along the track of their movement. Fluorescent phallotoxins and monoclonal anti-actin antibodies label filament bundles in the submicrovillar region, indicating that they are composed of F-actin. Finally, depolymerization of the submicrovillar actin filaments by incubation with cytochalasin B results in a blockade of the movement of mitochondria and ER cisternae towards the rhabdom. These results suggest that the light-dependent translocation of both ER cisternae and mitochondria occurs along actin filaments.

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