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

• Published in: PloS one 2015-09, Vol.10 (9), p.e0137468-e0137468
• Main Authors: Milani, Liliana, Ghiselli, Fabrizio, Pecci, Andrea, Maurizii, Maria Gabriella, Passamonti, Marco
• Format: Article
• Language: English
• Subjects: Amino Acid Sequence; Analysis; Animals; Antibodies; Bivalvia; Bivalvia - cytology; Bivalvia - genetics; Bivalvia - growth & development; Cell cycle; Cell migration; Cell proliferation; Cytoplasm; Dynamic tests; Embryonic development; Environmental science; Females; Gene expression; Gene Expression Regulation, Developmental; Genes; Genes, Mitochondrial; Genetic aspects; Genetic Markers; Genomes; Geology; Germ cells; Gonads - cytology; Gonads - growth & development; Gonads - metabolism; Homology; Inheritance Patterns; Insects; Localization; Male; Males; Mitochondria; Mitochondria - genetics; Mitochondrial DNA; Models, Molecular; Molecular Sequence Data; Mollusca; Organogenesis - genetics; Physiological aspects; Progeny; Proteins; Ruditapes philippinarum; Sequence Alignment; Spermatogenesis; Spermatogenesis - genetics; Spermatozoa; Spermatozoa - cytology; Spermatozoa - growth & development; Spermatozoa - metabolism; Stem cells; Transcription
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0137468

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.