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Evolutionary Linkage Between Eukaryotic Cytokinesis and Chloroplast Division by Dynamin Proteins

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Evolutionary Linkage Between Eukaryotic Cytokinesis and Chloroplast Division by Dynamin Proteins Evolutionary linkage between eukaryotic cytokinesis and chloroplast division by dynamin proteins Shin-ya Miyagishima*†, Hidekazu Kuwayama‡, Hideko Urushihara‡, and Hiromitsu Nakanishi* *Initiative Research Program, Advanced Science Institute, RIKEN, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan; and ‡Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennoudai, Tsukuba, Ibaraki 305-8572, Japan Edited by Lynn Margulis, University of Massachusetts, Amherst, MA, and approved August 12, 2008 (received for review March 11, 2008) Chloroplasts have evolved from a cyanobacterial endosymbiont activity, such as transport vesicle budding, organelle division, and been retained for more than 1 billion years by coordinated cytokinesis, and pathogen resistance (10). In some cases, two or chloroplast division in multiplying eukaryotic cells. Chloroplast more functions have been assigned to the same protein (10). division is performed by ring structures at the division site, en- Among the dynamin family, chloroplast division proteins spe- compassing both the inside and the outside of the two envelopes. cifically localize at the chloroplast division site (7–9), and A part of the division machinery is derived from the cyanobacterial mutations specifically inhibit chloroplast division (8, 11), sug- cytokinetic activity based on the FtsZ protein. In contrast, other gesting that the proteins function exclusively in chloroplast parts of the division machinery involve proteins specific to eu- division in extant plants and algae. However, given that the karyotes, including a member of the dynamin family. Each member dynamin family already existed in eukaryotes before the emer- of the dynamin family is involved in the division or fusion of a gence of chloroplasts (4, 5, 10), the dynamin proteins involved in distinct eukaryotic membrane system. To gain insight into the kind chloroplast division probably are derived from those involved in of ancestral dynamin protein and eukaryotic membrane activity eukaryotic membrane systems other than that in the chloroplast. that evolved to regulate chloroplast division, we investigated the Understanding the eukaryotic membrane fission/fusion machin- functions of the dynamin proteins that are most closely related to ery, which has evolved into the division mechanism of organelles, chloroplast division proteins. These proteins in the amoeba Dic- should provide important insights into the question of how host tyostelium discoideum and Arabidopsis thaliana localize at the cells have regulated the division of endosymbionts to establish a sites of cell division, where they are involved in cytokinesis. Our permanent endosymbiotic relationship. It has been suggested results suggest that the dynamin for chloroplast division is derived that synchronization of the host–endosymbiont cell cycle and from that involved in eukaryotic cytokinesis. Therefore, the chlo- cosegregation are critical steps (12, 13), but it is not known how roplast division machinery is a mixture of bacterial and eukary- the synchronization was established in ancestral algae. otic cytokinesis components, with the latter a key factor in the In this study, we found that previously uncharacterized mem- synchronization of endosymbiotic cell division with host cell divi- bers of the dynamin family in plants and nonphotosynthetic sion, thus helping to establish the permanent endosymbiotic protists share a common ancestor with the plant-specific chlo- relationship. roplast division dynamin proteins. Our results show that these proteins of amoeba and plants are involved in eukaryotic cyto- kinesis. These results suggest that the dynamin used in chloro- t is widely believed that chloroplasts arose from a bacterial plast division is derived from that involved in eukaryotic cyto- endosymbiont related to extant cyanobacteria (1, 2). Although I kinesis. Application of cytokinetic dynamin to endosymbiont cell most of their genes have either been lost or transferred to the division may have enabled the synchronization of host– host nuclear genome, chloroplasts retain several features similar endosymbiont cell division such that each daughter cell can to cyanobacteria. Chloroplasts contain nucleoids and ribosomes, inherit an endosymbiont after cytokinesis. and they are not synthesized de novo (1, 2). Chloroplasts multiply by division, as do cyanobacteria (3). However, the chloroplast Results genome does not contain sufficient information for carrying out Phylogenetic Relationships in the Dynamin Family. To address the division, indicating that the host eukaryotic cell genome regu- questions of the type of dynamin family member that evolved lates the division of chloroplasts (3). into the chloroplast division protein and the membrane activity Chloroplast division is performed by the constriction of a in which the ancestor of the chloroplast division dynamin was division apparatus (ring) encircling the division site around the involved, we conducted phylogenetic analyses of the dynamin two envelope membranes (3–6). The division apparatus includes family. In these phylogenetic analyses, we included both previ- a plastid-dividing ring of unknown composition, FtsZ, and one ously characterized and uncharacterized members of the dy- of the dynamin family of proteins (4–6). FtsZ and its associated namin family of Plantae, Opisthokonta (fungi and animals), factors are descended from the cyanobacterial endosymbiont, Amoebozoa, Heterolobosea, Chromista (a stramenopile), and posttranslationally targeted into chloroplasts (4). In contrast, the Alveolata (ciliates). Because the dynamin family has a diverse dynamin family of GTPases is specific to eukaryotes, and the range of functions (10), it is expected that the evolutionary rates chloroplast division dynamin is recruited to the cytosolic side of vary with the specific functions. To avoid the generation of an the chloroplast division site (7–9). This suggests that the chlo- incorrect tree, which is commonly a problem with rapidly roplast division machinery is derived from both endosymbiotic evolving sequences (long-branch attraction artifacts), we con- (bacterial) and host (eukaryotic) cells. The cyanobacteria-descended components of the chloroplast division machinery evolved from the cell division machinery of Author contributions: S.-y.M., H.K., H.U., and H.N. designed research; S.-y.M., H.K., and H.N. the cyanobacterial endosymbiont (4, 5). In contrast, there is little performed research; S.-y.M. and H.K. analyzed data; and S.-y.M. wrote the paper. information about the origin of chloroplast division dynamin The authors declare no conflict of interest. proteins. The dynamin family of GTPase proteins self-assemble This article is a PNAS Direct Submission. into rings or spirals on the surface of eukaryotic membranes, †To whom correspondence should be addressed. E-mail: [email protected]. where they play roles in membrane fission or fusion (10). There This article contains supporting information online at www.pnas.org/cgi/content/full/ are divergencies in the dynamin family, and the function of each 0802412105/DCSupplemental. member has been assigned to a distinct eukaryotic membrane © 2008 by The National Academy of Sciences of the USA 15202–15207 ͉ PNAS ͉ September 30, 2008 ͉ vol. 105 ͉ no. 39 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0802412105 Downloaded by guest on October 2, 2021 Fig. 1. Phylogenetic relationships in the dynamin family of proteins. The tree shown is the maximum-likelihood tree constructed by the PhyML program based on alignment of 567 amino acid residues of 78 dynamin family proteins. The numbers at the nodes are local bootstrap values calculated using PhyML and ProtML analyses. Bootstrap values Ͼ80% are shown, and dashes indicate Ͻ80% support. Branch lengths are proportional to the number of amino acid substitutions, which are indicated by the scale bar below the tree. The tree includes the dynamin family of proteins of Plantae Arabidopsis thaliana (At), Oryza sativa (Os or locus ID start from Os), Chlamydomonas reinhardtii (Cr), Ostreococcus lucimarinus (Ot), Cyanidioschyzon merolae (Cm), Stramenopile Thalassiosira pseudonana (Tp), Amoebozoa Dictyostelium discoideum (Dd), Fig. 2. DlpA, DlpB, and DlpC are involved in cytokinesis in D. discoideum. (A) Heterolobosea Naegleria gruberi (Ng) Alveolata Tetrahymena thermophila The ⌬dlpA, ⌬dlpB, and ⌬dlpC mutant amoeba cells (observed using phase- (Tt), Paramecium tetraurelia (Pt), Opisthokonta Saccharomyces cerevisiae (Sc), contrast microscopy) are multinucleated (nuclei are shown with blue fluores- Schizosaccharomyces pombe (Sp), Homo sapiens (Hs), Drosophila melano- cence by DAPI staining) and larger than the wild-type (WT) cells. (B) Time gaster (Dm), and Caenorhabditis elegans (Ce). course of dlpA, dlpB, and dlpC mRNA and DlpA protein levels during spore germination and cell culture mRNA were detected by semiquantitative RT-PCR cycB (encoding G2/M-specific cyclin B). The expression level indicates the structed phylogenetic trees by maximum-likelihood methods frequency of cells in M phase. TFIIS (encoding transcription elongation factor using amino acid sequences [ProtML (14) and PhyML (15)]. IIS) was used as an internal control. The DlpA protein was detected by The phylogenetic analyses showed a distant relationship be- anti-DlpA antibodies, which specifically detect DlpA, as shown at the Left. The tween chloroplast division DRP5B proteins (grouped in green in lowermost bands of Ponceau S staining show the same amount of total Fig. 1; originally
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