Evolutionary linkage between eukaryotic cytokinesis and chloroplast division by dynamin proteins

Miyagishima, Shin-ya; Kuwayama, Hidekazu; Urushihara, Hideko; Nakanishi, Hiromitsu

doi:10.1073/pnas.0802412105

Cited by 74 publications

(106 citation statements)

References 36 publications

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“…This revealed that the cytokinetic dynamins were monophyletic (LMN: 88% bootstrap support), and represented a sister group to the chloroplast division dynamins (PQR: 43% bootstrap support). The last common ancestor of amoebozoans and archaeplastids therefore had a class C cytokinetic dynamin (LMN) (22) that persists essentially unchanged in many lineages, as well as another class C dynamin of unknown sequence (???) (Fig.…”

Section: Entire Ancestral Dynamin Variants Are Preserved In Extant Spmentioning

confidence: 99%

Ancient dynamin segments capture early stages of host–mitochondrial integration

Purkanti

Thattai

2015

Proc. Natl. Acad. Sci. U.S.A.

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Eukaryotic cells use dynamins-mechano-chemical GTPases-to drive the division of endosymbiotic organelles. Here we probe early steps of mitochondrial and chloroplast endosymbiosis by tracing the evolution of dynamins. We develop a parsimony-based phylogenetic method for protein sequence reconstruction, with deep time resolution. Using this, we demonstrate that dynamins diversify through the punctuated transformation of sequence segments on the scale of secondary-structural elements. We find examples of segments that have remained essentially unchanged from the 1.8-billion-y-old last eukaryotic common ancestor to the present day. Stitching these together, we reconstruct three ancestral dynamins: The first is nearly identical to the ubiquitous mitochondrial division dynamins of extant eukaryotes, the second is partially preserved in the myxovirus-resistance-like dynamins of metazoans, and the third gives rise to the cytokinetic dynamins of amoebozoans and plants and to chloroplast division dynamins. The reconstructed sequences, combined with evolutionary models and published functional data, suggest that the ancestral mitochondrial division dynamin also mediated vesicle scission. This bifunctional protein duplicated into specialized mitochondrial and vesicle variants at least three independent times-in alveolates, green algae, and the ancestor of fungi and metazoans-accompanied by the loss of the ancient prokaryotic mitochondrial division protein FtsZ. Remarkably, many extant species that retain FtsZ also retain the predicted ancestral bifunctional dynamin. The mitochondrial division apparatus of such organisms, including amoebozoans, red algae, and stramenopiles, seems preserved in a nearprimordial form.eukaryote evolution | mitochondria | vesicles | dynamin | FtsZ E ukaryotes arose through the acquisition of mitochondria by an archaeal host cell about 2 billion y ago (1, 2), a watershed moment in the evolution of the modern compartmentalized cell plan (3). A second transformative endosymbiotic event, the acquisition of a cyanobacterium by a eukaryotic host to form chloroplasts, gave rise to the photosynthetic eukaryotic lineages (4). As the endosymbionts became integrated with their hosts, their growth and division became regulated by host-cellular machinery (5). Proteins of the dynamin superfamily were central to this process: Mitochondria and chloroplasts originally divided using a constricting ring of the prokaryotic cytoskeletal protein FtsZ, but dynamins have been recruited to these roles in all extant eukaryotes (6, 7). By reconstructing the evolutionary history of dynamins, we can probe the process of endosymbiont integration.The dynamin superfamily is diverse (8, 9), and different dynamin variants remodel membranes at different cellular locations (Table S1 and primary references therein). A major class of dynamins is essential for mitochondrial and peroxisomal division. Another large group drives the scission of clathrin-coated vesicles in organisms such as fungi and alveolates. A related group, the socal...

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Section: Entire Ancestral Dynamin Variants Are Preserved In Extant Spmentioning

confidence: 99%

Ancient dynamin segments capture early stages of host–mitochondrial integration

Purkanti

Thattai

2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Finally, DYNAMIN-RELATED PROTEIN5B (DRP5B; also known as ARC5), a member of the dynamin family of self-assembling proteins, is recruited by PDV1 and PDV2 to chloroplasts to complete chloroplast division (Miyagishima et al, 2006). DRP5B is specific to plants and algae and is thought to have evolved from a dynamin-related protein involved in eukaryotic cytokinesis (Miyagishima et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Phosphatidylinositol 4-Phosphate Negatively Regulates Chloroplast Division in Arabidopsis

2015

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Chloroplast division is performed by the constriction of envelope membranes at the division site. Although constriction of a ring-like protein complex has been shown to be involved in chloroplast division, it remains unknown how membrane lipids participate in the process. Here, we show that phosphoinositides with unknown function in envelope membranes are involved in the regulation of chloroplast division in Arabidopsis thaliana. PLASTID DIVISION1 (PDV1) and PDV2 proteins interacted specifically with phosphatidylinositol 4-phosphate (PI4P). Inhibition of phosphatidylinositol 4-kinase (PI4K) decreased the level of PI4P in chloroplasts and accelerated chloroplast division. Knockout of PI4Kb2 expression or downregulation of PI4Ka1 expression resulted in decreased levels of PI4P in chloroplasts and increased chloroplast numbers. PI4Ka1 is the main contributor to PI4P synthesis in chloroplasts, and the effect of PI4K inhibition was largely abolished in the pdv1 mutant. Overexpression of DYNAMIN-RELATED PROTEIN5B (DRP5B), another component of the chloroplast division machinery, which is recruited to chloroplasts by PDV1 and PDV2, enhanced the effect of PI4K inhibition, whereas overexpression of PDV1 and PDV2 had additive effects. The amount of DRP5B that associated with chloroplasts increased upon PI4K inhibition. These findings suggest that PI4P is a regulator of chloroplast division in a PDV1-and DRP5B-dependent manner.

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“…Because the Dnm1 is continuously expressed throughout the cell cycle, including organelle division cycles in C. merolae (27,28), an unknown factor that can recruit Dnm1 molecules to the division sites may play a role for the key regulator in the divisions of peroxisome and mitochondrion. Although the dynamin family members are phylogenetically grouped according to their functions, Dnm1 is grouped in the same subclade of DRP3s, which have dual functions (29,30). Thus, serial control of peroxisomal division and mitochondrial division by the same dynamin might be conserved among virtually all eukaryotes.…”

Section: Function Of the Pod Machinery And Comparisons Between The Podmentioning

confidence: 99%

Single-membrane–bounded peroxisome division revealed by isolation of dynamin-based machinery

Imoto

Kuroiwa

Yoshida

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Peroxisomes (microbodies) are ubiquitous single-membrane-bounded organelles and fulfill essential roles in the cellular metabolism. They are found in virtually all eukaryotic cells and basically multiply by division. However, the mechanochemical machinery involved in peroxisome division remains elusive. Here, we first identified the peroxisome-dividing (POD) machinery. We isolated the POD machinery from Cyanidioschyzon merolae, a unicellular red alga containing a single peroxisome. Peroxisomal division in C. merolae can be highly synchronized by light/dark cycles and the microtubuledisrupting agent oryzalin. By proteomic analysis based on the complete genome sequence of C. merolae, we identified a dynamin-related protein 3 (DRP3) ortholog, CmDnm1 (Dnm1), that predominantly accumulated with catalase in the dividing-peroxisome fraction. Immunofluorescence microscopy demonstrated that Dnm1 formed a ring at the division site of the peroxisome. The outlines of the isolated dynamin rings were dimly observed by phasecontrast microscopy and clearly stained for Dnm1. Electron microscopy revealed that the POD machinery was formed at the cytoplasmic side of the equator. Immunoelectron microscopy showed that the POD machinery consisted of an outer dynamin-based ring and an inner filamentous ring. Down-regulation of Dnm1 impaired peroxisomal division. Surprisingly, the same Dnm1 serially controlled peroxisomal division after mitochondrial division. Because genetic deficiencies of Dnm1 orthologs in multiperoxisomal organisms inhibited both mitochondrial and peroxisomal proliferation, it is thought that peroxisomal division by contraction of a dynaminbased machinery is universal among eukaryotes. These findings are useful for understanding the fundamental systems in eukaryotic cells.

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Evolutionary linkage between eukaryotic cytokinesis and chloroplast division by dynamin proteins

Cited by 74 publications

References 36 publications

Ancient dynamin segments capture early stages of host–mitochondrial integration

Ancient dynamin segments capture early stages of host–mitochondrial integration

Phosphatidylinositol 4-Phosphate Negatively Regulates Chloroplast Division in Arabidopsis

Single-membrane–bounded peroxisome division revealed by isolation of dynamin-based machinery

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