An mt+ gamete-specific nuclease that targets mt− chloroplasts during sexual reproduction in C. reinhardtii

Nishimura, Yoshiki; Misumi, Osami; Kato, Ko; Inada, Noriko; Higashiyama, Tetsuya; Momoyama, Yu; Kuroiwa, Tsuneyoshi

doi:10.1101/gad.979902

Cited by 75 publications

(69 citation statements)

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“…A Mn 21 -dependent nuclease activity was shown to be activated in mitochondria upon formation of the zygote and suggested to play a role in selective mtDNA degradation (Moriyama et al 2005). In C. reinhardtii, a Ca 21 -dependent nuclease activity specifically expressed in mt 1 gametes was identified and proposed to digest mt À chloroplast DNA in the zygote (Nishimura et al 2002). However, the responsible genes have not yet been identified.…”

Section: Discussionmentioning

confidence: 99%

Thea2Mating-Type Locus Geneslga2andrga2Direct Uniparental Mitochondrial DNA (mtDNA) Inheritance and Constrain mtDNA Recombination During Sexual Development ofUstilago maydis

Fedler

Luh

Stelter³

et al. 2009

Genetics

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Uniparental inheritance of mitochondria dominates among sexual eukaryotes. However, little is known about the mechanisms and genetic determinants. We have investigated the role of the plant pathogen Ustilago maydis genes lga2 and rga2 in uniparental mitochondrial DNA (mtDNA) inheritance during sexual development. The lga2 and rga2 genes are specific to the a2 mating-type locus and encode small mitochondrial proteins. On the basis of identified sequence polymorphisms due to variable intron numbers in mitochondrial genotypes, we could demonstrate that lga2 and rga2 decisively influence mtDNA inheritance in matings between a1 and a2 strains. Deletion of lga2 favored biparental inheritance and generation of recombinant mtDNA molecules in combinations in which inheritance of mtDNA of the a2 partner dominated. Conversely, deletion of rga2 resulted in predominant loss of a2-specific mtDNA and favored inheritance of the a1 mtDNA. Furthermore, expression of rga2 in the a1 partner protected the associated mtDNA from elimination. Our results indicate that Lga2 in conjunction with Rga2 directs uniparental mtDNA inheritance by mediating loss of the a1-associated mtDNA. This study shows for the first time an interplay of mitochondrial proteins in regulating uniparental mtDNA inheritance.

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Section: Discussionmentioning

confidence: 99%

Thea2Mating-Type Locus Geneslga2andrga2Direct Uniparental Mitochondrial DNA (mtDNA) Inheritance and Constrain mtDNA Recombination During Sexual Development ofUstilago maydis

Fedler

Luh

Stelter³

et al. 2009

Genetics

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confidence: 99%

“…Single zygotes with or without mtϪ cp nucleoids were then collected by optical tweezers and analyzed by highly sensitive nested PCR, confirming that mtϪ cpDNA is actively digested during this rapid disappearance of mtϪ cp nucleoids (18). It is now believed that maternal inheritance in C. reinhardtii is achieved through active processes, including the rapid digestion of mtϪ cpDNA, protection of mtϩ cpDNA, and amplification of mtϩ cpDNA (19,20).The cytological analysis of mt (cp) nucleoids has been a powerful strategy to determine the sexual transmission of mt (cp) DNA not only in C. reinhardtii but also in higher plants (21), ferns, mosses, fungi, and algae (2). In animals, however, studies on mt nucleoids are rare (22,23).…”

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confidence: 99%

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.

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147

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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“…In the unicellular green algae Chlamydomonas, the chloroplast DNA (cpDNA) of one parent 6 disappears immediately after mating, before the fusion of the sexual pronucleus (Sager and Lane, 1972). Nishimura et al (2002) separated the sexual chloroplasts from zygotes in Chlamydomonas immediately after mating. They detected gradually increasing Ca 2+ -dependent nuclease activity during the disappearance of cpDNA, but only in male derived chloroplasts.…”

Section: Introductionmentioning

confidence: 99%

The sperm mitochondria-specific translocator has a key role in maternal mitochondrial inheritance

Hayashida

Omagari

Masuda

et al. 2005

Cell Biology International

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AbstrctThe mechanism of maternal mitochondrial inheritance in animals involves the selective elimination of sperm mitochondria by the elimination factor of the egg and the sperm mitochondria-specific factor. In vitro fertilization using sperm from congenic mice incorporating heterogeneous mitochondrial DNA (mtDNA) showed that the number of PCR positives of sperm mtDNA in two-cell embryos was significantly increased following sperm incubation with anti-tpis, anti-Tom22 and anti-Tom40 antibodies. The treatment of fertilized eggs with EGTA and endonuclease inhibitors increased the sperm mtDNA levels. We conclude that the elimination factor, which is probably an endonuclease, is selectively received by the tpis protein of the sperm mitochondrial outer membrane within the egg. It is then transported into the sperm mitochondria by Tom22 and Tom40, where it destroys the sperm mtDNA, establishing the maternal inheritance of mtDNA.3

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An mt⁺ gamete-specific nuclease that targets mt⁻ chloroplasts during sexual reproduction in C. reinhardtii

Cited by 75 publications

References 68 publications

Thea2Mating-Type Locus Geneslga2andrga2Direct Uniparental Mitochondrial DNA (mtDNA) Inheritance and Constrain mtDNA Recombination During Sexual Development ofUstilago maydis

Thea2Mating-Type Locus Geneslga2andrga2Direct Uniparental Mitochondrial DNA (mtDNA) Inheritance and Constrain mtDNA Recombination During Sexual Development ofUstilago maydis

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

The sperm mitochondria-specific translocator has a key role in maternal mitochondrial inheritance

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