Formation of a Prespore Specific Structure From a Mitochondrion During Development of the Cellular Slime Mold Dictyostelium Discoideum

Abstract

The origin of a unique vacuole (PSV), which was specifically present in the prespore cell of the cellular slime mold Dictyostelium discoideum, was investigated electronmicroscopically. A considerable number of PSV-mitochondrion complexes was found in the intermediate fraction between a pure PSV and a pure mitochondria fractions, which were obtained by isopicnic centrifugation of cellular components of the prespore cell. Similar complexes were also observed in the differentiating prespore cells. Furthermore, the activity of succinic dehydrogenase, a typical mitochondria1 enzyme was found cytochemically to be localized in the PSV as well as in mitochondria. From these results, it was concluded that the PSV was formed from the mitochondrion through some intermediate steps.A vegetative amoeba of Dictyostelium discoideum grows and multipIies independently, feeding on bacteria. Some time after ceasing to feed, amoebae stream together to collecting points (aggregation stage). The cell aggregate thus formed initially crects itself (papilla stage), but later lies down on the substratum in the shape of a slug. The slug migrates for a period of time (migration stage), until it rises into the air to form a fruiting body composed of a mass of spores and a supporting cellular stalk (culmination stage).During culmination, the anterior (prestalk) cells of the slug differentiate into stalk cells, while the posterior (prespore) cells into spores. An electronmicroscopic study has revealed that a unique vacuole named PSV is specifically present in the cytoplasm of the prespore cells, but not in the prestalk cells (MAEDA and TAKHJCHI, 1969: HOHL andHAMAMOTO, 1969). It has also been demonstrated that the vacuole (PSV) is excreted from the prespore cell during its cytodifferentiation into the spore, and that the contents constitute the spore coat (HOHL and HAMAMOTO, 1969: MAEDA, 197 1 ).The PSV was a sole structure thus far found that showed discrete localization This paper is dedicated to Prof. Emer. Tadao Sato of Nagoya University for his seventieth birthday.

A mitochondrion as the structural basis of the formation of a cell-type-specific organelle inDictyostelium development

“…During the intermediate stage of PSV-maturation, the PSV-specific antigen (C-10) is noticed in a limited part of the mitochondria adjacent to the PSVmitochodrion complexes as well as in the lining membrane of PSVs. The PSV-mitochondrion complex is twisted at the junction and eventually they separate from each other to become the respective organelles, as previously reported (Maeda 1971b). Specialized structures such as cytoskeletons were not observed near the twisted junction between the PSV and mitochondrion.…”

“…Moreover, it has been cytochemically detected that the activity of succinic dehydrogenase, a typical mitochondrial enzyme is localized in the lining membrane of PSV as well as in mitochondria (Maeda 1971b). Based on these findings, we previously speculated that the PSV might originate from the mitochondrion through some intermediate steps (Maeda 1971b). However, it was long wrapped up in mystery whether or not the PSV is actually formed in the vacuole (M-vacuole) derived from the psp mitochondrion.…”

“…Substantial differences in fine structure have been demonstrated between the pst and psp regions of the slug (Maeda and Takeuchi 1969). Among them, the PSV (prespore-specific vacuole) is believed to be the only organelle that exists only in one of the two types of cells (Maeda andTakeuchi 1969, Hohl andHamamato 1969). The PSV is also a functionally essential structure and it is exocytosed from psp to form the spore cell wall during culmination (Hohl and Hamamoto 1969, Maeda 197 l a).…”

The necessity of mitochondrial genome DNA for normal development ofDictyosteliumcells

“…Journal of Cell Science 117 (15) In differentiating prespore cells, mitochondria exhibit a drastic structural transformation to form a sort of vacuole (Mvacuole), in which PSVs are constructed with the help of the Golgi complex (Maeda, 1971;Matsuyama and Maeda, 1998). Interestingly, during the formation of ρ ∆ cells mitochondria exhibit a marked morphological change and form unique vacuoles similar to the M-vacuole (see Fig.…”

Mitochondrial processing peptidase activity is controlled by the processing of α-MPP during development in Dictyostelium discoideum

“…Because of its unique life cycle, D. discoideum has been used as a model organism to study developmental processes. During the life cycle, mitochondria of D. discoideum exhibit marked morphological changes that appear to be closely related to the regulation of development (Ashworth et al, 1969;Cotter et al, 1969;Maeda, 1971;George et al, 1972). Mitochondrial dysfunction is caused by mutations in nuclear genes encoding mitochondrial proteins.…”