Specific location of sperm mitochondria in mussel <i>Mytilus galloprovincialis</i> zygotes stained by MitoTracker

Obata, Masahiro; Komaru, Akira

doi:10.1111/j.1440-169x.2005.00801.x

Cited by 43 publications

(46 citation statements)

References 27 publications

(28 reference statements)

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“…As mentioned earlier, the strategy of searching for sex-biased heteroplasmy of mitochondrial gene sequences as a means for detecting DUI has been successfully employed in other bivalve species (e.g., Boyle & Etter, 2013; Vargas et al, 2015; Dégletagne, Abele & Held, 2016). DUI can also be detected by in vivo localization of male mitochondria in embryos: an aggregate pattern of M-type mitochondria only into the male germline during early embryonic stages is typical of DUI species (Cao, Kenchington & Zouros, 2004; Obata & Komaru, 2005; Cogswell, Kenchington & Zouros, 2006; Milani, Ghiselli & Passamonti, 2012). The percentage of nucleotide divergence between the F and M cox1 sequences for both of these species, i.e., 33.4% for S. plana and 13% for Y. hyperborea , is within the range of what has been found for other bivalves with DUI (e.g., 8% in the veneroid Artica islandica (Dégletagne, Abele & Held, 2016), 17% in the nuculanoid Ledella sublevis (Boyle & Etter, 2013); 24% in the mytiloid Mytilus edulis (Breton et al, 2006),and 50% in the unionoid Inversidens japanensis (Doucet-Beaupré et al, 2010)).…”

Section: Discussionmentioning

confidence: 99%

Pursuing the quest for better understanding the taxonomic distribution of the system of doubly uniparental inheritance of mtDNA

Gusman

Lecomte

Stewart

et al. 2016

PeerJ

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There is only one exception to strict maternal inheritance of mitochondrial DNA (mtDNA) in the animal kingdom: a system named doubly uniparental inheritance (DUI), which is found in several bivalve species. Why and how such a radically different system of mitochondrial transmission evolved in bivalve remains obscure. Obtaining a more complete taxonomic distribution of DUI in the Bivalvia may help to better understand its origin and function. In this study we provide evidence for the presence of sex-linked heteroplasmy (thus the possible presence of DUI) in two bivalve species, i.e., the nuculanoid Yoldia hyperborea(Gould, 1841)and the veneroid Scrobicularia plana(Da Costa,1778), increasing the number of families in which DUI has been found by two. An update on the taxonomic distribution of DUI in the Bivalvia is also presented.

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Section: Discussionmentioning

confidence: 99%

Pursuing the quest for better understanding the taxonomic distribution of the system of doubly uniparental inheritance of mtDNA

Gusman

Lecomte

Stewart

et al. 2016

PeerJ

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“…The sex bias appears to be controlled by the nuclear genome of the females which can be accordingly subdivided in three classes: those producing predominantly males, those producing predominantly females, and those producing females and males at intermediate frequencies. 2) In embryos of DUI species the distribution of sperm mitochondria follows two different patterns: aggregated or dispersed (Cao et al 2004; Obata and Komaru 2005; Cogswell et al 2006; Milani et al 2011, 2012). In Mytilus , it was possible to correlate the pattern type to the sex of the embryo: male-biased offsprings showed a prevalence of aggregated patterns, while female-biased offsprings a prevalence of dispersed patterns.…”

Section: Introductionmentioning

confidence: 99%

Paternally Transmitted Mitochondria Express a New Gene of Potential Viral Origin

Milani

Ghiselli

Maurizii

et al. 2014

Genome Biology and Evolution

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Mitochondrial ORFans (open reading frames having no detectable homology and with unknown function) were discovered in bivalve molluscs with doubly uniparental inheritance (DUI) of mitochondria. In these animals, two mitochondrial lineages are present, one transmitted through eggs (F-type), the other through sperm (M-type), each showing a specific ORFan. In this study, we used in situ hybridization and immunocytochemistry to provide evidence for the expression of Ruditapes philippinarum male-specific ORFan (orf21): both the transcript and the protein (RPHM21) were localized in spermatogenic cells and mature spermatozoa; the protein was localized in sperm mitochondria and nuclei, and in early embryos. Also, in silico analyses of orf21 flanking region and RPHM21 structure supported its derivation from viral sequence endogenization. We propose that RPHM21 prevents the recognition of M-type mitochondria by the degradation machinery, allowing their survival in the zygote. The process might involve a mechanism similar to that of Modulators of Immune Recognition, viral proteins involved in the immune recognition pathway, to which RPHM21 showed structural similarities. A viral origin of RPHM21 may also support a developmental role, because some integrated viral elements are involved in development and sperm differentiation of their host. Mitochondrial ORFans could be responsible for or participate in the DUI mechanism and their viral origin could explain the acquired capability of M-type mitochondria to avoid degradation and invade the germ line, that is what viruses do best: to elude host immune system and proliferate.

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“…This observation suggests that fertilized eggs showing the dispersed sperm mitochondrial pattern develop into female embryos and eggs with the aggregation develop into males. It has been sug-gested that the aggregated mitochondria are finally delivered into the primordial germ cells in male embryos (18), thus accounting for the paternal transmission of the M genome. Similar observations have been made in another species with DUI, the clam Ruditapes philippinarum (19,20).…”

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confidence: 99%

Proteomic Analysis of Eggs from Mytilus edulis Females Differing in Mitochondrial DNA Transmission Mode

Diz

Dudley

Cogswell

et al. 2013

Molecular & Cellular Proteomics

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Many bivalves have an unusual mechanism of mitochondrial DNA (mtDNA) inheritance called doubly uniparental inheritance (DUI) in which distinctly different genomes are inherited through the female (F genome) and male (M genome) lineages. In fertilized eggs that will develop into male embryos, the sperm mitochondria remain in an aggregation, which is believed to be delivered to the primordial germ cells and passed to the next generation through the sperm. In fertilized eggs that will develop into female embryos, the sperm mitochondria are dispersed throughout the developing embryo and make little if any contribution to the next generation. The frequency of embryos with the aggregated or dispersed mitochondrial type varies among females. Previous models of DUI have predicted that maternal nuclear factors cause molecular differences among unfertilized eggs from females producing embryos with predominantly dispersed or aggregated mitochondria. We test this hypothesis using females of each of the two types from a natural population. We have found small, yet detectable, differences of the predicted type at the proteome level. We also provide evidence that eggs of females giving the dispersed pattern have consistently lower expression for different proteasome subunits than eggs of females giving the aggregated pattern. These results, combined with those of an earlier study in which we used hatchery lines of Mytilus, and with a transcriptomic study in a clam that has the DUI system of mtDNA transmission, reinforce the hypothesis that the ubiquitinproteasome system plays a key role in the mechanism of DUI and sex determination in bivalves. We also report that eggs of females giving the dispersed pattern have higher expression for arginine kinase and enolase, enzymes involved in energy production, whereas ferritin, which is involved in iron homeostasis, has lower expression. We discuss these results in the context of genetic models for DUI and suggest experimental methods for further understanding the role of these proteins in DUI. Proteomics has made a rapid progress when applied to model species where genomic databases are well developed, but recent reviews have pointed to the growing interest in applying proteomics to nonmodel species in areas such as evolutionary ecology (1), aquatic toxicology (2), aquatic pollution (3), aquaculture (4), and marine biology (5). In the marine mussel genus Mytilus, an unusual system of mtDNA inheritance occurs characterized by the presence of two mitochondrial genomes (called F and M) one of which is inherited maternally and the other paternally (6 -9). This phenomenon, called doubly uniparental inheritance of mtDNA (DUI), 1 suggests a connection between mtDNA inheritance and sex determination. DUI also occurs in other species belonging to three bivalve orders (10, 11). Since the 1990s, DUI has been under intensive investigation, but the molecular mechanism for DUI and how it relates to sex determination, is still to be elucidated (for review, see 12-15).Cytological studies of fertilize...

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Specific location of sperm mitochondria in mussel Mytilus galloprovincialis zygotes stained by MitoTracker

Cited by 43 publications

References 27 publications

Pursuing the quest for better understanding the taxonomic distribution of the system of doubly uniparental inheritance of mtDNA

Pursuing the quest for better understanding the taxonomic distribution of the system of doubly uniparental inheritance of mtDNA

Paternally Transmitted Mitochondria Express a New Gene of Potential Viral Origin

Proteomic Analysis of Eggs from Mytilus edulis Females Differing in Mitochondrial DNA Transmission Mode

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