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VASA-induced cytoplasmic localization of CYTB-positive mitochondrial substance occurs by destructive and nondestructive mitochondrial effusion, respectively, in early and late spermatogenic cells of the Manila clam

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Abstract

To analyze the release of mitochondrial material, a process that is believed to be (i) induced by the VASA protein derived from germplasm granules, and (ii) which appears to play an important role during meiotic differentiation, the localization of the CYTB protein was studied in the process of spermatogenesis of the bivalve mollusk Ruditapes philippinarum (Manila clam). It was found that in early spermatogenic cells, such as spermatogonia and spermatocytes, the CYTB protein shows dispersion in the cytoplasm following the total disaggregation of VASA-invaded mitochondria, what is called here as “destructive mitochondrial effusion (DME).” It was found that the mitochondria of the maturing sperm cells also uptake VASA. It is accompanied by extramitochondrial transmembrane localization of CYTB assuming mitochondrial content release without mitochondrion demolishing. This phenomenon is called here as “nondestructive mitochondrial effusion (NDME).” Thus, in the spermatogenesis of the Manila clam, two patterns of mitochondrial release, DME and NDME, were found, which function, respectively, in early spermatogenic cells and in maturing spermatozoa. Despite the morphological difference, it is assumed that both DME and NDME have a similar functional nature. In both cases, the intramitochondrial localization of VASA coincides with the extramitochondrial localization of the mitochondrial matrix.

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Acknowledgments

This study was funded by the Italian Ministry of Education, University and Research MIUR-SIR Program (Grant Number RBSI14G0P5) funded to LM. We are deeply indebted to Mr. D.F. Fomin (National Scientific Centre of Marine Biology, Far Eastern Branch of Russian Academy of Sciences, Vladivostok, Russia) for the helpful assistance during our observations using the electron microscopes. Some part of the analyses by electron microscopy were performed in the Microscopy Facility at St. Francis Xavier University (Antigonish, NS, Canada).

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Authors and Affiliations

  1. Department of Biology, St. Francis Xavier University, Antigonish, NS, B2G 2W5, Canada

    Arkadiy Reunov

  2. Far Eastern Branch of Russian Academy of Sciences, National Scientific Centre of Marine Biology, Vladivostok, 690041, Russia

    Arkadiy Reunov, Yana Alexandrova, Alina Komkova, Yulia Reunova, Evgenia Pimenova & Evgenia Vekhova

  3. Department of Biological, Geological and Environmental Sciences, University of Bologna, Via Selmi, 3, 40126, Bologna, Italy

    Liliana Milani

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  1. Arkadiy Reunov
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  4. Yulia Reunova
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  7. Liliana Milani
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Contributions

AR designed the study, implemented most of the TEM work, and was a major contributor to writing the manuscript. YA performed material collection/processing and part of the TEM analysis. AK performed part of the TEM analysis. YR performed part of the TEM analysis and the quantitative analysis. EP performed part of the TEM analysis. EV performed the SEM analysis. LM designed the antibody generation, performed material collection/processing, provided images, and was a contributor to discussion and writing the manuscript. All authors read and approved the final manuscript.

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Correspondence to Arkadiy Reunov.

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Reunov, A., Alexandrova, Y., Komkova, A. et al. VASA-induced cytoplasmic localization of CYTB-positive mitochondrial substance occurs by destructive and nondestructive mitochondrial effusion, respectively, in early and late spermatogenic cells of the Manila clam. Protoplasma 258, 817–825 (2021). https://doi.org/10.1007/s00709-020-01601-1

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