A symposium entitled “Molecular mechanism of cytoplasmic inheritance — 101 years of challenges —”was held at the 74th meeting of the Botanic Society of Japan in 2010 to commemorate 101th anniversary of the discovery of cytoplasmic inheritance. This symposium was co-supported by Journal of Plant Research and Japanese Society of Plant Morphology. Researchers studying various eukaryotes including slime molds, green algae, higher plants, and animals were invited to create an opportunity to overview the history and frontiers of researches in this field and to discuss the molecular mechanisms and significance of cytoplasmic inheritance during the evolution of eukaryotes.

View full abstract

The direct evidence of the digestion of paternal mitochondrial DNA (mtDNA) have been found in the true slime mold. This was the first report on the selective digestion of mtDNA inside the zygote, and would be the striking mechanism of maternal inheritance of mitochondria. Moreover, two mitochondrial nuclease activities have been detected in this organism as candidates for the nucleases responsible for selective digestion of mtDNA. In the true slime mold, an additional feature is concerned in the uniparental inheritance of mitochondria. Although mitochondria are believed to be inherited from maternal lineage in nearly all eukaryotes, the mating types of the true slime mold Physarum polycephalum is not restricted to two: there are three mating loci matA, matB, and matC, and these loci have 15, 15, and 3 alleles, respectively. Interestingly, the transmission patterns of mtDNA is determined by the matA locus, in a hierarchical fashion (matA hierarchy) as follows: matA7 > matA2 > matA11 > matA12 > matA15/matA16> matA1 > matA6. The strain possessing higher status of matA would be the mtDNA donor in crosses. Furthermore, we have found that some crosses showed biparental inheritance of mitochondria. This review describes the phenomenon of hierarchical transmission of mtDNA in the true slime mold, and discusses the presumed molecular mechanism of maternal and biparental inheritance.

View full abstract

Chloroplast (cp) and mitochondrial (mt) genomes are inherited almost exclusively from one parent in diverse taxa of plants and animals. Uniparental inheritance of mt/cp genomes was long thought to be the passive outcome of the fact that eggs contain multiple numbers of organelles whereas the contributions from male gametes are limited. However, the process is likely to be more dynamic because uniparental inheritance occurs in organisms that produce gametes of identical sizes (isogamous). In Chlamydomonas reinhardtii, uniparental inheritance of cp/mt genomes is achieved by a series of mating type-controlled events that actively eliminate mating type minus (mt-) cpDNA within 60 min after mating. How Chlamydomonas selectively degrades mt- cpDNA has long fascinated researchers and is the subject of this review.

View full abstract

Chloroplast and mitochondrial DNA (mtDNA) is inherited exclusively from the female parent in the plant and animal kingdoms. In isogamous green algae of the genus Chlamydomonas, however, chloroplast DNA (cpDNA) is inherited maternally while mtDNA is inherited paternally. To study the paternal inheritance of mtDNA in Chlamydomonas, markers were constructed to distinguish mtDNA origins, diploid cells were constructed, and genetic, molecular biological and microscopic analyses of mt+ and mt- mtDNA in zygotes were conducted. Here, the literature on mitochondrial inheritance in Chlamydomonas is reviewed.

View full abstract

The earliest studies of plastid transmission were showed maternal transmission in Mirabilis jalapa and biparental transmission in Pelargonium zonale. Two mechanisms have been proposed for maternal inheritance, “physical exclusion of the organelle” and the more likely possibility “digestion of organellar DNA” in generative/sperm cells. The replication or digestion of organellar DNA in young generative cells just after pollen mitosis I is a critical point to determine the mode of cytoplasmic inheritance. This review describes the complexity and diversity of cytoplasmic inheritance in angiosperms.

View full abstract

Two modes of mitochondrial (mtDNA) inheritance, i.e., maternal inheritance and rapid segregation between generations, have been proposed as the characteristic modes of mtDNA transmission in most animals. The occurrence of maternal inheritance of mtDNA has been known for a long time, but direct experimental evidence has been lacking. After the development and widespread applications of sensitive detection techniques, such as polymerase chain reaction (PCR), researchers reported paternal (biparental) inheritance of mtDNA in several species. In the case of intraspecific hybrid mice, sperm mtDNA was detected until the early pronuclear stage, but was not detected after 2-cell stage. By contrast, in the case of interspecific hybrid mice, paternal mtDNA was detected throughout the developmental period, from pronuclear to neonatal stages. However, the leakage of paternal mtDNA was limited to the progeny of the first generation of an interspecific cross and did not occur in the progeny of any other generation from subsequent backcrosses. These observations suggest that maternal inheritance of mtDNA is strictly preserved in mice.
   Rapid segregation is the other unique mode of mtDNA transmission. It is unclear why mtDNA sequence variants rapidly segregate through generations, and only 1 variant is fixed in an individual despite the high copy number of mtDNA in somatic cells (10^3-4). To address this question, investigators have proposed the mitochondrial genetic bottleneck that results from the reduction in the number of mtDNA molecules per germ cell. However, in our study, mtDNA copy numbers of female germ cells at several developmental stages was not reduced to the extent that was previously speculated. Therefore, the mitochondrial bottleneck is not generated because of a drastic decline in the mtDNA copy number, but because of a small effective number of segregation units of mtDNA in mouse germ cells.

View full abstract

[in Japanese]

View full abstract

Pollen development in angiosperms starts in anthers within buds formed by conversion from vegetative growth to reproductive growth, and results in double fertilization at which one sperm cell fuses to an egg cell and the other sperm cell fuses to a central cell including two polar nuclei. During this process, there are drastic cellular changes such as production of haploid cells by meiosis in pollen mother cells, differentiation of the generative cell and the vegetative cell by an unequal (asymmetric) cell division in microspores and growth of pollen tubes. However, it is generally difficult to observe the inner structure under an ordinary light microscope because the pollen mother cells possess callosic cell wall, and microspores and pollen grains further have a thick exine consisting of insoluble sporopollenin. Therefore, the observation has usually been conducted on sectioned samples as in the case with electron microscopy. In order to make the observation easy, we tried to isolate protoplasts free from cell wall and exine in Lilium longiflorum. As a result, pollen mother cell protoplasts, microspore protoplasts, pollen protoplasts and generative cell protoplasts could be obtained in large quantities. On the other hand, biochemical research suggested several specific proteins appeared during pollen development. Using specific antibodies raised against the specific antigens, immunofluorescence studies on isolated protoplasts first revealed dynamics of the specific proteins during pollen development.

View full abstract

Chloroplasts originated more than 1 billion years ago when a cyanobacterial cell became an endosymbiont in a eukaryotic cell. Reminiscent of their free-living ancestors, chloroplasts replicate by binary fission, but the division is controlled by the eukaryotic host cell. Recent studies have shown that chloroplast division is performed by a macromolecular protein complex at the division site, encompassing both the inside and the outside of the two envelope membranes. The division complex has retained certain components of the cyanobacterial division complex and several other components that have been developed by the host cell. On the basis of the information about the division complex, we are beginning to understand how the division complex evolved, and how eukaryotic host cells regulate chloroplast division during proliferation and differentiation. In this review, we summarize the recent rapid progress in our understanding of the chloroplast division machinery and its regulation.

View full abstract

The ASYMMETRIC LEAVES2 (AS2) gene is involved in leaf development along adaxial-abaxial, medial-lateral and proximal-distal axes in Arabidopsis. The AS2 gene belongs to the AS2/LATERAL ORGAN BOUNDARIES (LOB) family. There are 42 members of the AS2/LOB family in the Arabidopsis genome. Many recent studies revealed that AS2/LOB family genes are involved in various physiological processes including the regulation of development and metabolism in plants. The approximately 100 amino acid AS2/LOB-domain, which defines this family, is highly conserved. Conserved regions include the C-motif, an internal region containing an invariant glycine residue, and a leucine-zipper-like motif, in the case of class I proteins. The conserved AS2/LOB-domain of AS2 cannot be functionally replaced by those of other members of the family. AS2 acts in a same pathway as that of AS1, which is an ortholog of ROUGH SHEATH2 of maize and PHANTASTICA of snapdragon. Recent molecular genetic studies for the role of AS2 provided important information. The regulation of gene expression and leaf development by AS2 is genetically linked with the regulations based on chromatin level, post-transcriptional level, protein metabolism and cell proliferation. These novel insights contribute to a better understanding of the role of AS2/LOB family genes for plant morphogenesis and physiological responses.

View full abstract

During mitosis, chromosomes show dynamic movements. The orchestration of chromosome dynamics mediated by various molecules is required for stable transmission of genetic information. The failure of chromosome separation directly induces aneuploidy with imbalance of genetic information. Because aneuploidy, an abnormal number of chromosomes, and chromosome instability is found in most solid tumors, the mechanisms of chromosome dynamics are well studied in animals, specifically as therapeutic target. However, it remains to be unclear the mechanisms of chromosome dynamics with mitotic kinases in plants. The authors identified and analyzed Aurora kinases as mitotic kinases, which regulate chromosome dynamics during mitosis, in Arabidopsis thaliana and Nicotiana tabacum. In this review, I summarize the recent finding of the regulatory mechanisms of chromosome dynamics in animals and in plants, and discuss future perspectives.

View full abstract