The Expression of a Novel Mitochondrially-Encoded Gene in Gonadic Precursors May Drive Paternal Inheritance of Mitochondria

Abstract

Mitochondria have an active role in germ line development, and their inheritance dynamics are relevant to this process. Recently, a novel protein (RPHM21) was shown to be encoded in sperm by the male-transmitted mtDNA of Ruditapes philippinarum, a species with Doubly Uniparental Inheritance (DUI) of mitochondria. In silico analyses suggested a viral origin of RPHM21, and we hypothesized that the endogenization of a viral element provided sperm mitochondria of R. philippinarum with the ability to invade male germ line, thus being transmitted to the progeny. In this work we investigated the dynamics of germ line development in relation to mitochondrial transcription and expression patterns using qPCR and specific antibodies targeting the germ line marker VASPH (R. philippinarum VASA homolog), and RPHM21. Based on the experimental results we conclude that both targets are localized in the primordial germ cells (PGCs) of males, but while VASPH is detected in all PGCs, RPHM21 appears to be expressed only in a subpopulation of them. Since it has been predicted that RPHM21 might have a role in cell proliferation and migration, we here suggest that PGCs expressing it might gain advantage over others and undertake spermatogenesis, accounting for RPHM21 presence in all spermatozoa. Understanding how foreign sequence endogenization and co-option can modify the biology of an organism is of particular importance to assess the impact of such events on evolution.

Early gametogenesis in the Pacific oyster: new insights using stem cell and mitotic markers

“…Likewise, Obata et al (2010) identified vasa-positive cells in Mytilus galloprovincialis, again suggesting the existence of GSCs in connective tissue during the non-reproductive season in mussel. Interestingly, as will be further discussed below, Milani et al (2015Milani et al ( , 2017 confirmed through confocal microscopy that Vasa is a germ cell marker in several species of bivalve.…”

“…Gametogenesis has long been of interest in bivalves (reviewed in Galtsoff, 1964), and has received renewed attention following the development of genomics in bivalves (Fabioux et al, 2004a(Fabioux et al, ,b, 2009Llera-Herrera et al, 2013;Milani et al, 2015Milani et al, , 2017Obata et al, 2010;Teaniniuraitemoana et al, 2017) and, more recently, because of current environmental concerns (Barranger et al, 2014;Cubero-Leon et al, 2012;de Sousa et al, 2014).…”

“…The oyster gonad is not permanent, and thus the location of GSCs during the resting period and at the beginning of the sexual cycle is not yet completely clear despite recent progress (Fabioux et al, 2004a;Obata et al, 2010;Milani et al, 2015Milani et al, , 2017. Because GSCs are stem cells that perform several rounds of mitotic division before executing germ cell-specific meiosis (reviewed in Spradling et al, 2011), we examined gametogenesis at an early stage of the oyster sexual cycle using molecular markers for stem cells, for DNA replication and for mitosis.…”

Germ cell line during the seasonal sexual rest of clams: finding niches of cells for gonad renewal

“…For histological sample preparation, the entire body was processed for hematoxylin and eosin staining following the method in Bettini et al [17]. Tissue samples for immunohistochemistry were processed as described in Milani et al [18] with the following modifications: the entire body was collected from animals in the spent phase and fixed for 3.5 hours, while, given their larger body dimensions, pieces of the body of about 0.5-0.8 cm 3 were sampled from specimens in the gametogenic phase (July 2015-2016) and fixed for 3 hours. Details on antisera production as well as specificity tests and experimental controls are provided in Milani et al [18].…”

ggtern: Ternary Diagrams Using ggplot2

“…ggplot2 is an implementation of The Grammar of Graphics (Wilkinson 2005) and rigorously enforces Wilkinson's series of grammatical rules for creating perceivable graphs, therefore, by using ggplot2 as a basis for the present work, we inherit this compelling philosophy, perhaps, from time-to-time, allowing the user to create graphical poetry (Wickham 2010). Under peer-review, ggtern has already been utilized in various publications and fields, including for example, works by Witte, Bradley, Enright, and Muljo (2015), Milani, Ghiselli, Pecci, Maurizii, and Passamonti (2015); Wenger, Buzgariu, and Galliot (2016); Kalenitchenko et al (2016); Chu, Ma, Prince, Antony, Seferovic, and Aagaard (2017) and Nesbitt et al (2017).…”