Epifluorescent microscopic evidence for maternal inheritance of chloroplast DNA

Kuroiwa, Tsuneyoshi; Kawano, Shigeyuki; Nishibayashi, Soryu; Sato, Chubun

doi:10.1038/298481a0

Cited by 195 publications

(101 citation statements)

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“…DAPI fluorescence (Fig. 7B, a, c, e, and g) confirmed previous reports (Kuroiwa et al, 1982); 1 h after cell fusion the zygote contained cell and chloroplast nuclei derived from both parents, but at 6 h it lacked the male-derived chloroplast nuclei and had a single, fused cell nucleus.…”

Section: Discussionsupporting

confidence: 75%

“…When they encounter cells of the opposite mating type, they recognize their partner, begin to agglutinate, and then fuse to become zygotes. After zygote formation, a number of events ensue, including preferential digestion of malederived chloroplast nuclei (Kuroiwa et al, 1982), nuclear fusion (Cavalier-Smith, 1970;Kuroiwa et al, 1982), flagellar degeneration, and zygospore formation (Cavalier-Smith, 1976). All functional proteins and their mRNAs directly involved in these phenomena are thought to be synthesized only after cell fusion (Kuroiwa et al, 1983;Kuroiwa, 1991).…”

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Characterization of Chlamydomonas reinhardtiiZygote-Specific cDNAs That Encode Novel Proteins Containing Ankyrin Repeats and WW Domains1

et al. 1999

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Genes that are expressed only in the young zygote are considered to be of great importance in the development of an isogamous green alga, Chlamydomonas reinhardtii. Clones representing the Zys3 gene were isolated from a cDNA library prepared using zygotes at 10 min after fertilization. Sequencing of Zys3 cDNA clones resulted in the isolation of two related molecular species. One of them encoded a protein that contained two kinds of protein-to-protein interaction motifs known as ankyrin repeats and WW domains. The other clone lacked the ankyrin repeats but was otherwise identical. These mRNA species began to accumulate simultaneously in cells beginning 10 min after fertilization, and reached maximum levels at about 4 h, after which time levels decreased markedly. Genomic DNA gel-blot analysis indicated that Zys3 was a single-copy gene. The Zys3 proteins exhibited parallel expression to the Zys3 mRNAs at first, appearing 2 h after mating, and reached maximum levels at more than 6 h, but persisted to at least 1 d. Immunocytochemical analysis revealed their localization in the endoplasmic reticulum, which suggests a role in the morphological changes of the endoplasmic reticulum or in the synthesis and transport of proteins to the Golgi apparatus or related vesicles.

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confidence: 75%

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Characterization of Chlamydomonas reinhardtiiZygote-Specific cDNAs That Encode Novel Proteins Containing Ankyrin Repeats and WW Domains1

et al. 1999

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“…These observations validate the necessity to eliminate paternal mt (cp) DNA before the destruction of mt (cp) structures. Active digestion of uniparental mt (cp) DNA has been observed in various species, including higher plants (2,21), algae (13,16), and slime mold (58,59). Also, in these cases, mt (cp) DNA molecules are digested, whereas the structures of mitochondria or chloroplasts remain apparently intact, which might be necessary to avoid the potential hazard caused by sexual recombination of mt (cp) genomes in these species.…”

Section: Discussionmentioning

confidence: 99%

“…In C. reinhardtii, 80-90 copies of the cp genome are compacted into 5-8 cp nucleoids (15). In 1982, Kuroiwa et al (16) found that mtϪ cp nucleoids disappear preferentially in young zygotes 50 min after mating. In 1998, the preferential disappearance of mtϪ cp nucleoids was observed in a living zygote (17).…”

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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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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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“…Initially, nucleoids were defined morphologically as DNA-containing foci visualized inside mitochondria (Kuroiwa, 1982;Nass et al, 1965;Stevens, 1982) or chloroplasts (Eva and Chiang, 1984;Kuroiwa et al, 1982). Later, mitochondrial nucleoids were isolated at a defined density in gradient centrifugation and appeared to retain their morphological structure in vitro (Dai et al, 2005;Miyakawa et al, 1987;Newman et al, 1996;Suzuki et al, 1982).…”

Section: Introductionmentioning

confidence: 99%

Characterization of the Structure and DNA Complexity of Mung Bean Mitochondrial Nucleoids

Hsiao

Cheng

et al. 2011

Molecules and Cells

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Electron microscopic images of mitochondrial nucleoids isolated from mung bean seedlings revealed a relatively homogeneous population of particles, each consisting of a chromatin-like structure associated with a membrane component. Association of F-actin with mitochondrial nucleoids was also observed. The mitochondrial nucleoid structure identified in situ showed heterogeneous genomic organization. After pulsed-field gel electrophoresis (PFGE), a large proportion of the mitochondrial nucleoid DNA remained in the well, whereas the rest migrated as a 50-200 kb smear zone. This PFGE migration pattern was not affected by high salt, topoisomerase I or latrunculin B treatments; however, the mobility of a fraction of the fastmoving DNA decreased conspicuously following an in-gel ethidium-enhanced UV-irradiation treatment, suggesting that molecules with intricately compact structures were present in the 50-200 kb region. Approximately 70% of the mitochondrial nucleoid DNA molecules examined via electron microscopy were open circles, supercoils, complex forms, and linear molecules with interspersed sigmashaped structures and/or loops. Increased sensitivity of mtDNA to DNase I was found after mitochondrial nucleoids were pretreated with high salt. This result indicates that some loosely bound or peripheral DNA binding proteins protected the mtDNA from DNase I degradation.

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Epifluorescent microscopic evidence for maternal inheritance of chloroplast DNA

Cited by 195 publications

References 9 publications

Characterization of Chlamydomonas reinhardtiiZygote-Specific cDNAs That Encode Novel Proteins Containing Ankyrin Repeats and WW Domains1

Characterization of Chlamydomonas reinhardtiiZygote-Specific cDNAs That Encode Novel Proteins Containing Ankyrin Repeats and WW Domains1

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

Characterization of the Structure and DNA Complexity of Mung Bean Mitochondrial Nucleoids

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