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Localization of the Mitochondrial Ftsz Protein in a Dividing Mitochondrion Mitochondria Are Ubiquitous Organelles That Play Crit

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Localization of the Mitochondrial Ftsz Protein in a Dividing Mitochondrion Mitochondria Are Ubiquitous Organelles That Play Crit C2001 The Japan Mendel Society Cytologia 66: 421-425, 2001 Localization of the Mitochondrial FtsZ Protein in a Dividing Mitochondrion Manabu Takahara*, Haruko Kuroiwa, Shin-ya Miyagishima, Toshiyuki Mori and Tsuneyoshi Kuroiwa Department of Biological Sciences, Graduate School of Science, University of Tokyo, Hongo, Tokyo 113-0033, Japan Accepted November 2, 2001 Summary FtsZ protein is essential for bacterial cell division, and is also involved in plastid and mitochondrial division. However, little is known of the function of FtsZ in the mitochondrial division process. Here, using electron microscopy, we revealed that the mitochondrial FtsZ (CmFtsZ 1) local- izes at the constricted isthmus of a dividing mitochondrion on the inner (matrix-side) surface of the mitochondrion. These results strongly suggest that the mitochondrial FtsZ acts as a ring structure on the inner surface of mitochondria. Key words Cyanidionschyzon merolae, FtsZ, FtsZ ring, mitochondria, mitochondrion-dividing ring (MD ring) . Mitochondria are ubiquitous organelles that play critical roles in respiration and ATP synthesis in almost all eukaryotic cells. Mitochondria are thought to have originated from a-proteobacteria through an endosymbiont event. Like bacteria, they multiply by the binary fission of pre-existing mitochondria. Although the role of mitochondria in respiration and ATP production is well under- stood, little is known about the proliferation of mitochondria in cells. In plastids, which also arose from prokaryotic endosymbionts, the ring structure that appears at the constricted isthmus of a dividing plastid (the plastid-dividing ring or PD ring) has been iden- tified as the plastid division apparatus (Mita et al. 1986). The PD ring is widespread among plants and algae, and consists of an outer (cytosolic) ring and an inner (stromal) ring in most species. A similar structure has been identified at the constricted neck of mitochondria (the mitochondrion-di- viding ring or MD ring) in primitive red algae (Kuroiwa et al. 1993). The MD ring also consists of an outer (cytosolic) ring and an inner (matrix-side) ring, although the inner MD ring is rarely ob- served clearly. However, the molecular mechanisms of these rings remain uncertain. On the other hand, bacterial cell division is a well-studied process, and many of the genes in- volved in the bacterial cell division process have been identified (de Boer et al. 1990, Rothfield and Justice 1997, Bramhill 1997, Lutkenhaus and Addinall 1997). The best characterized is ftsZ, which is considered to play the most crucial role. Homologues of ftsZ are present in almost all prokaryotic genomes sequenced to date, suggesting that ftsZ is almost universally conserved in prokaryotes (Erickson 1997). During the cell-division cycle, the FtsZ protein forms a bacterial contractile ring (known as the 'FtsZ ring' or 'Z ring') on the inner surface of the cytoplasmic membrane, at the midpoint of the cell (Bi and Lutkenhaus 1991). FtsZ is structurally and evolutionarily related to eu- karyotic tubulins, and it is presumed to be an evolutionary progenitor of tubulin (Erickson 1995, Lowe and Amos 1998, Nogales et al. 1998). FtsZ homologues are also involved in plastid division (Osteryoung et al. 1998, Strepp et al. 1998). Recently, mitochondrial homologues of FtsZ were discovered in the primitive red alga Cyani- dioschyzon merolae (Takahara et al. 2000) and the chromophyte alga Mallomonas splendes (Beech * Corresponding author . 422 Manabu Takahara et al. Cytologia 66 et al. 2000). These FtsZs are nuclear-encoded, closely related to the FtsZs of ƒ¿-proteobacteria , the ancestor of mitochondria, and localized to mitochondria. However, the localization of mitochondrial FtsZ is not clear. Here, we studied the localization of the mitochondrial FtsZ of the primitive red alga C . mero- lae (CmFtsZ 1) by electron microscopy. We found that CmFtsZ 1 localizes on the inner (matrix-side) surface at the constricted isthmus of a dividing mitochondrion. These results strongly suggest that mitochondrial FtsZ plays a role in the mitochondrial division process by forming a ring structure on the inner surface of mitochondria. Materials and methods Cell culture C. merolae strain 10D-14 was used throughout this study. This strain was originally provided by Prof. G. Pinto of the University of Naples, and was then isolated by Dr . K. Toda of the Universi- ty of Tokyo (Toda et al. 1998). C. merolae cells were cultured in Allen's medium (Allen 1959) . Synchronization of C. merolae cultures was performed essentially as described previously (Suzuki et al. 1994). Electron microscopy For ultrastructural observations, C. merolae cells were rapidly frozen in liquid propane , fixed with 1% OsO4, and embedded in Spurr's resin (Spurr 1969) . Thin sections were observed with a JEM-1200EX electron microscope (JEOL, Tokyo, Japan). For immunogold electron microscopy, the cells were rapidly frozen in liquid propane , freeze- substituted in acetone with 1% OsO4, and embedded in LR White resin (The London Resin Co ., London, UK). As a first antibody, mouse antiserum against CmFtsZ 1 was used at a dilution of 1 : 100. As a second antibody, goat anti-mouse IgG conjugated to 10-nm gold particles (British Bio- Cell International, Cardiff, UK) was used at a dilution of 1 : 80. After double staining with uranyl acetate and lead citrate, samples were examined by electron microscopy. Results A C. merolae cell has a single mitochondrion, which is concave, like a red blood cell , and lies between the cell nucleus and the chloroplast (Suzuki et al. 1994) . Fig. 1A shows a cell containing a dividing mitochondrion and a dividing chloroplast, cut perpendicular to the plane of division, dur- ing organelle division in C. merolae. In the front view, the mitochondrion appears rod-shaped and forms a V-shape as it divides. The MD ring (outer MD ring) is observed on the outer (cytosolic) surface of the mitochondrial envelope at the constricted neck of the mitochondrion . When immuno- electron microscopy was performed using C. merolae cells at the stage of division corresponding to that in Fig. 1A, immuno-gold particles were seen on the inner (matrix-side) surface of the constrict- ed edge of the mitochondrion (Fig. 1B). The topological relation of particles and the MD ring is similar to that of particles and the PD ring observed using electron microscopy (Miyagishima et al . 2001). The gold particles seemed to pair with the MD ring . These results indicate that CmFtsZ 1 lo- calizes in a ring structure on the inner surface of the constricted edge of the mitochondria. No parti- cles were observed on the MD ring and the PD ring (Fig. 1B), suggesting that CmFtsZ 1 is not locat- ed on the MD ring and the PD ring. Discussion Here, we provide the first evidence that mitochondrial FtsZ localizes at the constricted isthmus 2001 Mitochondrial FtsZ Protein in a Dividing Mitochondrion 423 Fig. 1. Localization and structure of the mitochondrial FtsZ (CmFtsZ 1) in C. merolae. A) Electron micrograph of C. merolae cells with dividing mitochondria. The MD ring (arrow) is observed on the outer (cytosolic) surface of the mitochondrial envelope at the constricted neck of the mitochondrion. B) Immunoelectron micrographs showing the localization of CmFtsZ 1 at the constricted neck of dividing mitochondrion. Arrows show the MD ring, and arrowheads show the gold particles using anti-CmFtsZ 1 antibodies. The doublearrow shows the outer PD ring. mt, mitochondrion; cp, chloroplast. Scale bar= 500 nm (A) and 100 nm (B). of a dividing mitochondrion, suggesting that the mitochondrial FtsZ forms a ring on the inner sur- face of the mitochondrion. In a previous study, Beech et al. (2000) showed that a mitochondrial FtsZ (MsFtsZ-mt) was always associated with mitochondria. Although anti-MsFtsZ-mt labels have been observed at the midpoint in some mitochondria, it has not previously been determined whether mitochondrial FtsZ forms a ring. The data in this study indicate that mitochondrial FtsZ is not located on the outer MD ring. Like the PD ring, the MD ring is observed as a double ring: the outer MD ring, which is the main component of the MD ring, on the cytoplasmic side of the mitochondrion, and the inner MD ring in the mitochondrial matrix beneath the inner membrane. The inner MD ring is rarely observed clear- ly, since it is probably thin and weak. Therefore, we cannot conclude from these results whether mi- tochondrial FtsZ is located on the inner MD ring. However, no FtsZ rings (or filaments) have been observed in vivo using electron microscopy. Therefore, we assume that the mitochondrial FtsZ ring is also distinct from the inner MD ring. In bacteria, FtsZ mediates cell division by forming a bacterial contractile ring (FtsZ ring) be- neath the cytoplasmic membrane at the leading edge of the cell division site (Bi and Lutkenhaus 1991). In addition, recent studies have revealed that plastid FtsZs localize to rings at the plastid midpoint (Vitha et al. 2001, Mori et al. 2001). Mori et al. (2001) showed that a plastid FtsZ is local- ized on the stromal side of constricting chloroplasts. Therefore, we presume that the location and structure of FtsZ are generally universal among bacteria, plastids, and mitochondria; FtsZ forms a ring on the inner surface of the cell or organelle at the division site. It is presumed that mitochondrial FtsZ is present in a limited number of organisms, since there are no mitochondrial ftsZ homologues in the entire genomes of S. cerevisiae (Goffeau et al. 1996), C. elegans (The C. elegans Sequencing Consortium 1998), and A. thaliana (The Arabidopsis 424 Manabu Takahara et al. Cytologia 66 Genome Initiative 2000) or in the extensive EST databases for humans and animals. The absence of mitochondrial FtsZ in animals, fungi, and higher plants raises 2 questions. Where in the evolution of eukaryotes did mitochondria lose their FtsZ, and how do mitochondria lacking FtsZ divide? In regard to the second question, the key proteins are dynamins.
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