Direct Evidence for Homologous Recombination in Mussel (Mytilus galloprovincialis) Mitochondrial DNA

Ladoukakis, Emmanuel D.; Ζούρος, Ε.

doi:10.1093/oxfordjournals.molbev.a003904

Cited by 192 publications

(156 citation statements)

References 60 publications

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“…Homologous recombination is well studied in chloroplasts, and cpDNA transformation is performed taking advantage of this activity (55,56). Furthermore, direct evidence for homologous recombination in animal mtDNA was recently reported (57). These observations validate the necessity to eliminate paternal mt (cp) DNA before the destruction of mt (cp) structures.…”

Section: Discussionmentioning

confidence: 78%

Active digestion of sperm mitochondrial DNA in single living sperm revealed by optical tweezers

Nishimura

Yoshinari

Naruse

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

144

104

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In almost all eukaryotes, mitochondrial (mt) genes are transmitted to progeny mainly from the maternal parent. The most popular explanation for this phenomenon is simple dilution of paternal mtDNA, because the paternal gametes (sperm) are much smaller than maternal gametes (egg) and contribute a limited amount of mitochondria to the progeny. Recently, this simple explanation has been challenged in several reports that describe the active digestion of sperm mtDNA, down-regulation of mtDNA replication in sperm, and proteolysis of mitochondria triggered by ubiquitination. In this investigation, we visualized mt nucleoids in living sperm by using highly sensitive SYBR green I vital staining. The ability to visualize mt nucleoids allowed us to clarify that the elimination of sperm mtDNA upon fertilization is achieved through two steps: (i) gradual decrease of mt nucleoid numbers during spermatogenesis and (ii) rapid digestion of sperm mtDNA just after fertilization. One notable point is that the digestion of mtDNA is achieved before the complete destruction of mitochondrial structures, which may be necessary to avoid the diffusion and transmission of potentially deleterious sperm mtDNA to the progeny. maternal inheritance ͉ medaka ͉ mtDNA M itochondria and chloroplasts contain their own genomes, which are believed to be vestiges of their bacterial ancestors (1). Mitochondrial (mt) and chloroplast (cp) genes are inherited in non-Mendelian fashion. A variety of patterns and mechanisms have been observed for the transmission of these genes, but in almost all eukaryotes, they are inherited mainly from the maternal parent (2-4).Generally, the maternal inheritance of mt (cp) DNA is thought to be a result of the dilution of the paternal contribution, because the paternal gametes (sperm) are much smaller than maternal gametes (egg) and contribute only a limited amount of cytoplasm to the progeny. In animals, a mature sperm carries Ϸ100 copies of mtDNA, which might be necessary to maintain the integrity of mitochondrial activity (5). In contrast, the animal oocyte contains Ϸ10 5 to 10 8 copies of mtDNA, exceeding that of sperm by a factor of at least 10 3 (3, 6). Therefore, the paternal contribution of mtDNA or cpDNA would be diluted beyond the limits of detection by using conventional restriction enzyme analysis (7).This simple explanation, however, has been challenged by many findings (8). For example, there have been several fairly unsuccessful attempts to detect leaky transmission of paternal mtDNA by repetitive backcross experiments using lepidopteran insects (9). On the contrary, in mussels (Mtylus), paternal mtDNA can be transmitted to male progeny at a remarkably high frequency, even though paternal mtDNAs are transmitted by sperm (10-12). A more striking example was found in the unicellular alga Chlamydomonas reinhardtii. In C. reinhardtii, despite the fact that mtϩ (female) and mtϪ (male) gametes contribute equal amounts of cytoplasm to the progeny, cpDNA is transmitted only from the mtϩ parent. One biochemical stud...

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Section: Discussionmentioning

confidence: 78%

Active digestion of sperm mitochondrial DNA in single living sperm revealed by optical tweezers

Nishimura

Yoshinari

Naruse

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

144

104

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“…Both events have been documented to occur in mammals (Gyllensten et al, 1991;Schwartz and Vissing, 2002;Ladoukakis and Eyre-Walker, 2004;Zhao et al, 2004), birds (Kvist et al, 2003), fish (Magoulas and Zouros, 1993;Guo et al, 2006;Ciborowski et al, 2007), mollusks (Ladoukakis and Zouros, 2001), amphibians (Ujvari et al, 2007), arthropods (Meusel and Moritz, 1993;Gantenbein et al, 2005;Arunkumar et al, 2006;Sherengul et al, 2006;Fontaine et al, 2007) and nematodes (Lunt and Hyman, 1997;Armstrong et al, 2007). What is more, gender-associated and tissue-specific transmission of both paternal and maternal mtDNA ('doubly uniparental inheritance' (DUI)) appears to be the norm in some bivalves (Breton et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Lost in the zygote: the dilution of paternal mtDNA upon fertilization

Wolff¹,

Gemmell²

2008

Heredity

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The mechanisms by which paternal inheritance of mitochondrial DNA (mtDNA) (paternal leakage) and, subsequently, recombination of mtDNA are prevented vary in a speciesspecific manner with one mechanism in common: paternally derived mtDNA is assumed to be vastly outnumbered by maternal mtDNA in the zygote. To date, this dilution effect has only been described for two mammalian species, human and mouse. Here, we estimate the mtDNA content of chinook salmon oocytes to evaluate the dilution effect operating in another vertebrate; the first such study outside a mammalian system. Employing real-time PCR, we determined the mtDNA content of chinook salmon oocytes to be 3.2 Â 10 9 ± 1.0 Â 10 9 , and recently, we determined the mtDNA content of chinook salmon sperm to be 5.73 ± 2.28 per gamete. Accordingly, the ratio of paternal-to-maternal mtDNA if paternal leakage occurs is estimated to be 1:5.5 Â 10 8 . This contribution of paternal mtDNA to the overall mtDNA pool in salmon zygotes is three to five orders of magnitude smaller than those revealed for the mammalian system, strongly suggesting that paternal inheritance of mtDNA per offspring will be much less likely in this system than in mammals.

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“…The finding that DUI is present in divergent groups of bivalve leads to the hypothesis that doubly uniparental inheritance emerged early in the bivalve and should represent an ancestral character in the group. Occasionally, the paternal route is invaded by the maternal lineage (Hoeh et al, 1997;Saavedra et al, 1997), producing a heterogeneous pool transmitted by males, so that recombination, like gene conversion, could eventually happen (Ladoukakis & Zouros, 2001), as has been shown in M. galloprovincialis. Another event that may happen is the complete replacement of the M lineage by the F, so that the M becomes the same as the F, an event called the "masculinization of the F".…”

Section: Discussionmentioning

confidence: 99%

No evidence of doubly uniparental inheritance in the brown mussel Perna perna from the RFLP analyses of the mitochondrial 16S rDNA

Weber

Hildebrand

2009

Braz. J. Aquat. Sci. Technol.

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The doubly uniparental mode of inheritance, characteristic of the Mytilidae, consists of an F-type mitochondrial lineage transmitted only through females and an M-type lineage present only in male gonads and therefore transmitted only through males. In this work, we search for evidence of two mitochondrial lineages in Perna perna by studying the same 16S rRNA region that allowed for the discovery of doubly uniparental inheritance in the Mytilus group and in one venerid clam. The region was screened for substitutions using eight restriction enzymes to analyze two kinds of tissues (somatic and gonadal) from 20 males and 20 females from the south of Brazil. A restriction map was constructed after confirming restriction sites with sequence analysis. After amplification with the same primers used in previous studies, a fragment of 517 bp was obtained, which was 10 bp shorter than the one from Mytilus species. No variation was found among individuals or between sexes or kinds of tissue (gonadal and somatic). The absence of variation in this region was confirmed by sequence analysis, and this result left us unable to reject the hypothesis of common maternal mitochondrial inheritance. The 16S rDNA sequence obtained for Perna perna was aligned with twenty-three representative sequences from fifteen mytilid species available in GenBank, and a neighborjoining tree was constructed. The phylogenetic analysis showed all Perna species clustered together in a single branch, which was supported 100% by bootstrap analysis and was more closely related to the branch of the Mytilus group than the other representative genera of the Mytilidae.

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Direct Evidence for Homologous Recombination in Mussel (Mytilus galloprovincialis) Mitochondrial DNA

Cited by 192 publications

References 60 publications

Active digestion of sperm mitochondrial DNA in single living sperm revealed by optical tweezers

Active digestion of sperm mitochondrial DNA in single living sperm revealed by optical tweezers

Lost in the zygote: the dilution of paternal mtDNA upon fertilization

No evidence of doubly uniparental inheritance in the brown mussel Perna perna from the RFLP analyses of the mitochondrial 16S rDNA

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