How do plastids and mitochondria divide?

Abstract Plastids and mitochondria are thought to have originated from free-living cyanobacterial and alpha-proteobacterial ancestors, respectively, via endosymbiosis. Their evolutionary origins dictate that these organelles do not multiply de novo but through the division of pre-existing plastids and mitochondria. Over the past three decades, studies have shown that plastid and mitochondrial division are performed by contractile ring-shaped structures, broadly termed the plastid and mitochondrial-division machineries. Interestingly, the division machineries are hybrid forms of the bacterial cell division system and eukaryotic membrane fission system. The structure and function of the plastid and mitochondrial-division machineries are similar to each other, implying that the division machineries evolved in parallel since their establishment in primitive eukaryotes. Compared with our knowledge of their structures, our understanding of the mechanical details of how these division machineries function is still quite limited. Here, we review and compare the structural frameworks of the plastid and mitochondrial-division machineries in both lower and higher eukaryotes. Then, we highlight fundamental issues that need to be resolved to reveal the underlying mechanisms of plastid and mitochondrial division. Finally, we highlight related studies that point to an exciting future for the field. plastid division, mitochondrial division, endosymbiosis, PDR1, MDR1, endosymbiotic-organelle-dividing machinery Introduction Binary fission is one of the fundamental characteristics of living organisms, as it is required to maintain species and to multiply cells (Fig. 1). The principle also applies to eukaryotic organelles that are descended from endosymbiotic bacterial ancestors, namely plastids (chloroplasts) and mitochondria, which contain their own genomic DNA and are not generated de novo in eukaryotic cells [1–6]. Proliferation of these organelles is executed by ring-shaped cellular machineries termed the plastid-division machinery and the mitochondrial-division machinery (Fig. 2) [7–15]. After assembly of the division machinery at the midpoint of each organelle, the circumference of the machinery monotonically decreases. As a result, the machinery constricts the organellar membranes at the division site until finally, fission occurs. Fig. 1. View largeDownload slide Plastid and mitochondrial division. Time-lapse images of plastid and mitochondrial proliferation by binary division in unicellular red alga Cyanidioschyzon merolae. The C. merolae cells contain only one plastid and one mitochondrion per cell. Plastids (red) are visualized by autofluorescence and mitochondria (green) are visualized with sfGFP-tagged mitochondrial-EF-tu. Scale bar, 1 μm. Fig. 1. View largeDownload slide Plastid and mitochondrial division. Time-lapse images of plastid and mitochondrial proliferation by binary division in unicellular red alga Cyanidioschyzon merolae. The C. merolae cells contain only one plastid and one mitochondrion per cell. Plastids (red) are visualized by autofluorescence and mitochondria (green) are visualized with sfGFP-tagged mitochondrial-EF-tu. Scale bar, 1 μm. Fig. 2. View largeDownload slide The division machinery of plastids and mitochondria. (a) Immunofluorescence images of PDR1 (upper) and MDR1 (bottom). Scale bars, 1 μm. (b and c) Immuno-EM images of an isolated plastid-division machinery (b) and an isolated mitochondrial-division machinery (c). Scale bars, 200 nm. Images were reproduced and modified with permission from Refs. [47,51,55]. Fig. 2. View largeDownload slide The division machinery of plastids and mitochondria. (a) Immunofluorescence images of PDR1 (upper) and MDR1 (bottom). Scale bars, 1 μm. (b and c) Immuno-EM images of an isolated plastid-division machinery (b) and an isolated mitochondrial-division machinery (c). Scale bars, 200 nm. Images were reproduced and modified with permission from Refs. [47,51,55]. The mode of plastid and mitochondrial division was long unclear; however, the discovery of the Plastid-Dividing (PD) ring and the Mitochondrion-Dividing (MD) ring, which were identified as electron-dense specialized structures at the plastid and mitochondrial-division sites in primitive red algae, opened the way to investigate the proliferation mechanisms of these organelles [7,16–18]. A series of electron microscopy (EM) studies made significant contributions to delineating the behavior of the plastid- and mitochondrial-division machineries [7,19]. Later, several genes involved in plastid or mitochondrial division were identified in multiple lineages of eukaryotes [9–12,20]. Now, we know that both plastids and mitochondria divide under the regulation of supramolecular complexes comprising a dynamic trio of rings—the PD/MD ring, FtsZ ring and dynamin ring—which span the plastid or mitochondrial double membrane (Fig. 3) [9,10,15]. Fig 3. View largeDownload slide Schematic representations of the division machinery of plastids and mitochondria in C. merolae. IEM, inner-envelope membrane; OEM, outer-envelope membrane; IM, inner membrane; OM, outer membrane. The middle PD ring, the inner MD ring and Mda1 are omitted from this representation. Modified from Refs. [37,55]. Fig 3. View largeDownload slide Schematic representations of the division machinery of plastids and mitochondria in C. merolae. IEM, inner-envelope membrane; OEM, outer-envelope membrane; IM, inner membrane; OM, outer membrane. The middle PD ring, the inner MD ring and Mda1 are omitted from this representation. Modified from Refs. [37,55]. However, the mechanical details of plastid and mitochondrial division are still not fully understood. In particular, the kinetics and dynamics of the division machineries are almost completely unknown. This review summarizes the components responsible for the division of these organelles and categorizes the underlying processes, highlighting gaps in our understanding of each. We also highlight several examples of studies using high-resolution imaging approaches that may provide clues to these unanswered questions. We hope that viewing the current understanding of the mechanisms of plastid and mitochondrial division through this lens will trigger a break in the deadlock of the field. Compositions of the division machineries The FtsZ ring The FtsZ gene was originally identified from Escherichia coli mutants as encoding the key division protein in bacteria [21,22]. Bacterial FtsZ assembles a ring structure at the midpoint of the cell and plays a central role in bacterial cell division [22,23]. The core structure of the FtsZ protein includes two functional domains, a GTP-binding at the amino (N)-terminal and a GTPase-activating domain at the carboxy (C)-terminal. The FtsZ proteins polymerize head-to-tail to form directional protofilaments [24,25]. Recent studies of bacterial FtsZ proteins usin (...truncated)