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Germ plasm provides clues on meiosis: the concerted action of germ plasm granules and mitochondria in gametogenesis of the clam Ruditapes philippinarum

Published online by Cambridge University Press:  07 December 2018

Arkadiy Reunov Open the ORCID record for Arkadiy Reunov [Opens in a new window] ,
Yana Alexandrova ,
Yulia Reunova ,
Alina Komkova  and
Liliana Milani
Arkadiy Reunov*
Affiliation:
University of Ottawa Heart Institute, Electron Microscopy Laboratory, 40 Ruskin Street, Ottawa, ON K1Y 4W7, Canada National Scientific Centre of Marine Biology, Laboratory of Cell Differentiation, Far Eastern Branch of Russian Academy of Sciences, Vladivostok, 690041, Russia
Yana Alexandrova
Affiliation:
National Scientific Centre of Marine Biology, Laboratory of Cell Differentiation, Far Eastern Branch of Russian Academy of Sciences, Vladivostok, 690041, Russia
Yulia Reunova
Affiliation:
National Scientific Centre of Marine Biology, Laboratory of Cell Differentiation, Far Eastern Branch of Russian Academy of Sciences, Vladivostok, 690041, Russia
Alina Komkova
Affiliation:
National Scientific Centre of Marine Biology, Laboratory of Cell Differentiation, Far Eastern Branch of Russian Academy of Sciences, Vladivostok, 690041, Russia
Liliana Milani
Affiliation:
University of Bologna, Department of Biological, Geological and Environmental Sciences, Via Selmi 3, 40126 Bologna, Italy
*
Address for correspondence: Arkadiy Reunov. Electron Microscopy Laboratory, University of Ottawa Heart Institute, 40 Ruskin St, Ottawa ON K1Y 4W7, Canada. Tel: +1 613 761 5282. Fax: +1 613 761 4998. E-mail: [email protected]
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Summary

Germ plasm-related structures (GPRS) are known to accompany meiotic cell differentiation but their dynamics are still poorly understood. In this study, we analyzed the ultrastructural mechanisms of GPRS transformation during oogenesis and spermatogenesis of the bivalve mollusc Ruditapes philippinarum (Manila clam), exploring patterns of GPRS activity occurring at meiosis onset, sex-specific difference/similarity of such patterns, and the involvement of mitochondria during GPRS-assigned events. In the two sexes, the zygotene–pachytene stage of meiosis is anticipated by three shared steps. First, the dispersion of germ plasm granules containing the germ line determinant VASA occurs. Second, the VASA protein deriving from germ plasm granules enters neighbouring mitochondria and appears to induce mitochondrial matter release, as supported by cytochrome B localization outside the mitochondria. Third, intranuclear VASA entrance occurs and the protein appears involved in chromatin reorganization, as supported by VASA localization in synaptonemal complexes. In spermatogenesis, these three steps are sufficient for the normal course of meiosis. In oogenesis, these are followed by the action of ‘germ plasm granule formation complex’, a novel type of structure that appears alternative to the Balbiani body. The possibility of germ plasm involvement in reproductive technologies is also suggested.

Keywords

CYTBGametogenesisGerm plasm-related structures (GPRS)Manila clamMeiotic differentiationMitochondriaRuditapes philippinarumVASA
Type
Research Article
Information
Zygote , Volume 27 , Issue 1 , February 2019 , pp. 25 - 35
Copyright
© Cambridge University Press 2018 

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References

Ables, ET (2015) Drosophila oocytes as a model for understanding meiosis: an educational primer to accompany ‘Corolla is a novel protein that contributes to the architecture of the synaptonemal complex of Drosophila’. Genetics 199, 17–23.Google Scholar
Amikura, R, Kashikawa, M, Nakamura, A and Kobayashi, S (2001) Presence of mitochondria-type ribosomes outside mitochondria in germ plasm of Drosophila embryos. Proc Natl Acad Sci USA 98, 9133–9138.Google Scholar
Amikura, R, Sato, K and Kobayashi, S (2005) Role of mitochondrial ribosome dependent translation in germline formation in Drosophila embryos. Mech Dev 122, 1087–1093.Google Scholar
Bilinski, SM, Kloc, M and Tworzydlo, W (2017) Selection of mitochondria in female germline cells: is Balbiani body implicated in this process? J Assist Reprod Genet 34, 1405–1412.Google Scholar
Carré, D, Djediat, C and Sardet, C (2002) Formation of a large Vasa-positive germ granule and its inheritance by germ cells in the enigmatic Chaetognaths. Development 129, 661–670.Google Scholar
Castrillon, DH, Quade, BJ, Wang, TY, Quigley, C, Crum, CP (2000) The human VASA gene is specifically expressed in the germ cell lineage. Proc Natl Acad Sci USA 97, 9585–9590.Google Scholar
Chang, P, Torres, J, Lewis, RA, Mowry, KL, Houliston, E and King, ML (2004) Localization of RNAs to the mitochondrial cloud in Xenopus oocytes through entrapment and association with endoplasmic reticulum. Mol Biol Cell 15, 4669–4681.Google Scholar
Cox, RT and Spradling, AC (2003) A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development 130, 1579–1590.Google Scholar
Cuykendall, TN and Houston, DW (2010) Identification of germ plasm-associated transcripts by microarray analysis of Xenopus vegetal cortex RNA. Dev Dyn 239, 1838–1848.Google Scholar
Delgado, M and Perez-Camacho, A (2007) Comparative study of gonadal development of Ruditapes philippinarum (Adams and Reeve) and Ruditapes decussates (L.) (Mollusca; Bivalvia): influence of temperature. Scientia Marina 71, 471–484.Google Scholar
Eckelbarger, KJ (2005) Oogenesis and oocytes. Hydrobiologia 535/536, 179–198.Google Scholar
Findley, SD, Tamanaha, M, Clegg, NJ and Ruohola-Baker, H (2003) Maelstrom, a Drosophila spindle-class gene, encodes a protein that colocalizes with Vasa and RDE1/AGO1 homolog, Aubergine, in nuage. Development 130, 859–871.Google Scholar
Gur, Y and Breitbart, H (2006) Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes. Genes Dev 20, 411–416.Google Scholar
Gur, Y and Breitbart, H (2008) Protein synthesis in sperm: dialog between mitochondria and cytoplasm. Mol Cell Endocrinol 282, 45–55.Google Scholar
Gustafson, EA and Wessel, GM (2010) Vasa genes: emerging roles in the germ line and in multipotent cells. Bioessays 32, 626–637.Google Scholar
Hendriks, S, Dancet, EAF, van Pelt, AMM, Hamer, G and Repping, S (2015) Artificial gametes: a systematic review of biological progress towards clinical application. Hum Reprod Update 21, 285–296.Google Scholar
Kalt, MR (1973) Ultrastructural observations on the germ line of Xenopus laevis . Z. Zellforsch 138, 41–62.Google Scholar
Kashikawa, M, Amikura, R and Kobayashi, S (2001) Mitochondrial small ribosomal RNA is a component of germinal granules in Xenopus embryos. Mech Dev 101, 71–77.Google Scholar
Kashir, J, Jones, C, Child, T, Williams, SA and Coward, K (2012) Viability assessment for artificial gametes: the need for biomarkers of functional competency. Biol Reprod 87, 1–11.Google Scholar
Kloc, M, Bilinski, S, Chan, AP and Etkin, LD (2001) Mitochondrial ribosomal RNA in the germinal granules in Xenopus embryos revisited. Differentiation 67, 80–83.Google Scholar
Kloc, M, Dougherty, MT, Bilinski, S, Chan, AP, Brey, E, King, ML, Patrick, CW Jr and Etkin, LD (2002) Three-dimensional ultrastructural analysis of RNA distribution within germinal granules of Xenopus . Dev Biol 241, 79–93.Google Scholar
Kobayashi, S, Amikura, R and Okada, M (1993) Presence of mitochondrial large ribosomal RNA outside mitochondria in germ plasm of Drosophila melanogaster . Science 260, 1521–1524.Google Scholar
Kobayashi, S, Amikura, R and Okada, M (1994) Localization of mitochondrial large rRNA in germinal granules and the consequent segregation of germ line. Int J Dev Biol 38, 193–199.Google Scholar
Kobayashi, S, Amikura, R and Mukai, M (1998) Localization of mitochondrial large ribosomal RNA in germ plasm of Xenopus embryos. Curr Biol 8, 1117–1120.Google Scholar
Lasko, PF and Ashburner, M (1988) The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature 335, 611–617.Google Scholar
Liang, L, Diehl-Jones, W and Lasko, P (1994) Localization of vasa protein to the Drosophila pole plasm is independent of its RNA-binding and helicase activities. Development 120, 1201–1211.Google Scholar
Lippai, M, Gobet, I, Tomkowiak, M, Durocher, Y, Leclerc, C, Moreau, M and Guerrier, P (1995) Thimerosal triggers meiosis reinitiation in oocytes of the Japanese clam Ruditapes philippinarum by eliciting an intracellular Ca2+ surge. Int J Dev Biol 39, 401–407.Google Scholar
Mahowald, AP (1962) Fine structure of pole cells and polar granules in Drosophila melanogaster. J Exp Zool 151, 201–205.Google Scholar
Matova, N and Cooley, L (2001) Comparative aspects of animal oogenesis. Dev Biol 231, 291–320.Google Scholar
Medrano, JV, Reijo Pera, RA and Simon, C (2013) Germ cell differentiation from pluripotent cells. Semin Reprod Med 31, 14–23.Google Scholar
Milani, L, Ghiselli, F, Maurizii, MG and Passamonti, M (2011) Doubly uniparental inheritance of mitochondria as a model system for studying germ line formation. PLoS One 6, e28194.Google Scholar
Milani, L, Ghiselli, F, Pecci, A, Maurizii, MG and Passamonti, M (2015) The expression of a novel mitochondrially-encoded gene in gonadic precursors may drive paternal inheritance of mitochondria. PLoS One 10, e0137468 Google Scholar
Milani, L, Pecci, A, Ghiselli, F, Passamonti, M, Bettini, S, Franceschini, V, Maurizii, MG (2017) VASA expression suggests shared germ line dynamics in bivalve molluscs. Histochem Cell Biol 148, 157–171.Google Scholar
Moreno, I, Miguez-Forjan, JM and Simon, C (2015) Artificial gametes from stem cells. Clin Exp Reprod Med 42, 33–44.Google Scholar
Nikolic, A, Volarevic, V, Armstrong, L, Lako, M and Stojkovic, M (2016) Primordial germ cells: current knowledge and perspectives. Stem Cell Int Article ID 1741072, http://dx.doi.org/10.1155/2016/1741072.Google Scholar
Ninomiya, Y and Ichinose, S (2007) Subcellular distribution of mitochondrial ribosomal RNA in the mouse oocyte and zygote. PLoS One 2, e1241.Google Scholar
Pek, JW and Kai, T (2011) A role for Vasa in regulating mitotic chromosome condensation in Drosophila . Curr Biol 21, 39–44.Google Scholar
Raz, E (2000) The function and regulation of vasa-like genes in germ-cell development. Genome Biol 1, 1–6.Google Scholar
Reunov, AA (2004) Is there a germ plasm in mouse oocytes? Zygote 12, 329–332.Google Scholar
Reunov, AA and Reunova, YA (2015) In mouse oocytes the mitochondrion-originated germinal body-like structures accumulate mouse Vasa homologue (MVH) protein. Zygote 23, 501–506.Google Scholar
Reunov, AA, Isaeva, VV, Au, DWT and Wu, RSS (2000) Nuage constituents arising from mitochondria: is it possible? Dev Growth Differ 42, 139–143.Google Scholar
Reunov, AA, Yurchenko, OV, Alexandrova, YN and Radashevsky, VI (2009) Spermatogenesis in Boccardiella hamata (Polychaeta: Spionidae) from the sea of Japan: sperm formation mechanisms as characteristics for future taxonomic revision. Acta Zoologica 91, 447–456.Google Scholar
Saffman, EE and Lasko, P (1999) Germline development in vertebrates and invertebrates. Cell Mol Life Sci 55, 1141–1163.Google Scholar
Strome, S and Wood, WB (1983) Generation of asymmetry and segregation of germ line granules in early C elegans embryos. Cell 35, 11–25.Google Scholar
Villegas, J, Araya, P, Bustos-Obregon, E and Burzio, LO (2002) Localization of the 16S mitochondrial rRNA in the nucleus of mammalian spermatogenic cells. Mol Hum Reprod 8, 977–983.Google Scholar
Watanabe, M, Itoh, K, Abe, K, Akizawa, T, Ikenishi, K and Furusawa, M (1992) Immuno-localization of DEAD family proteins in germ line cells of Xenopus embryos. Dev Growth Differ 34, 223–231.Google Scholar
Wilk, K, Bilinski, S, Dougherty, MT and Kloc, M (2004) Delivery of germinal granules and localized RNAs via the messenger transport organizer pathway to the vegetal cortex of Xenopus oocytes occurs through directional expansion of the mitochondrial cloud. Int J Dev Biol 49, 17–21.Google Scholar
Williamson, A and Lehmann, R (1996) Germ cell development in Drosophila . Annu Rev Cell Dev Biol 12, 365–391.Google Scholar
Wolf, PM, Priess, J and Hirsh, D (1983) Segregation of germline granules in early embryos of Caenorhabditis elegans. An electron microscopic analysis. J Embryol Exp Morphol 73, 297–306.Google Scholar
Yajima, M and Wessel, GM (2011) The multiple hats of Vasa function and its regulation of cell cycle progression. Mol Reprod Dev 78, 861–867.Google Scholar
Yakovlev, KV (2016) Localization of germ plasm-related structures during sea urchin oogenesis. Dev Dynam 245, 56–66.Google Scholar