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Protein import into cyanelles and complex chloroplasts

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Abstract

Higher-plant, green and red algal chloroplasts are surrounded by a double membrane envelope. The glaucocystophyte plastid (cyanelle) has retained a prokaryotic cell wall between the two envelope membranes. The complex chloroplasts of Euglena and dinoflagellates are surrounded by three membranes while the complex chloroplasts of chlorarachniophytes, cryptomonads, brown algae, diatoms and other chromophytes, are surrounded by 4 membranes. The peptidoglycan layer of the cyanelle envelope and the additional membranes of complex chloroplasts provide barriers to chloroplast protein import not present in the simpler double membrane chloroplast envelope. Analysis of presequence structure and in vitro import experiments indicate that proteins are imported directly from the cytoplasm across the two envelope membranes and peptidoglycan layer into cyanelles. Protein import into complex chloroplasts is however fundamentally different. Analysis of presequence structure and in vitro import into microsomal membranes has shown that translocation into the ER is the first step for protein import into complex chloroplasts enclosed by three or four membranes. In vivo pulse chase experiments and immunoelectronmicroscopy have shown that in Euglena, proteins are transported from the ER to the Golgi apparatus prior to import across the three chloroplast membranes. Ultrastructural studies and the presence of ribosomes on the outermost of the four envelope membranes suggests protein import into 4 membrane-bounded complex chloroplasts is directly from the ER like outermost membrane into the chloroplast. The fundamental difference in import mechanisms, post-translational direct chloroplast import or co-translational translocation into the ER prior to chloroplast import, appears to reflect the evolutionary origin of the different chloroplast types. Chloroplasts with a two-membrane envelope are thought to have evolved through the primary endosymbiotic association between a eukaryotic host and a photosynthetic prokaryote while complex chloroplasts are believed to have evolved through a secondary endosymbiotic association between a heterotrophic or possibly phototrophic eukaryotic host and a photosynthetic eukaryote.

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Authors and Affiliations

  1. School of Biological Sciences, University of Nebraska, Lincoln, NE, 68588, USA (author for correspondence; e-mail

    Steven D. Schwartzbach

  2. Department of Life Sciences, Nippon Sport Science University, 1221 Kamosida, Aoba-ku, Yokohama, 227, Japan

    Tetsuaki Osafune

  3. Institute of Biochemistry and Molecular Cell Biology, University of Vienna, and Ludwig-Boltzmann-Forschungsstelle für Biochemie, 1030, Vienna, Austria

    Wolfgang Löffelhardt

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Schwartzbach, S.D., Osafune, T. & Löffelhardt, W. Protein import into cyanelles and complex chloroplasts. Plant Mol Biol 38, 247–263 (1998). https://doi.org/10.1023/A:1006029919283

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