Abstract
The nucleus of Cyanidioschyzon merolae has quite a limited set of components. The core and linker histones, H2A.Z, and a centromeric histone variant CenH3 are preserved, but H2A variants including H2A.X, H2A.M, and H2A.W are absent. Some proteins of the nuclear pore complex and nucleoli are also preserved, but almost all homologs of nuclear lamina and nuclear envelope proteins are lacking. The chloroplast of this species is divided by a ring, which is composed of two inner rings, the FtsZ ring and inner plastid-dividing (PD) ring, and two outer rings, the outer PD ring and dynamin ring. Identification of the PD ring components in C. merolae enabled us to elucidate the molecular mechanism behind the PD machinery. For example, a glycosyltransferase protein, plastid-dividing ring 1, acts in establishing the PD ring by forming ring-shaped polyglucan filaments. The division of mitochondria is performed by the mitochondrion-dividing (MD), FtsZ, and dynamin rings. Mda1 functions as a mediator for stably linking a dynamin. In addition, an FtsZ-associated protein, ZED, is involved in completing the inner rings of the MD machinery. Analyses of the mechanisms of mitochondrial and chloroplast division in C. merolae contribute to our understanding of the endosymbiotic process of double-membrane-bounded organelles.
References
Adams DW, Errington J (2009) Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol 7(9):642–653. https://doi.org/10.1038/nrmicro2198
Al-Haboubi T, Shumaker DK, Köser J et al (2011) Distinct association of the nuclear pore protein Nup153 with A- and B-type lamins. Nucleus 2(5):500–509. https://doi.org/10.4161/nucl.2.5.17913
Archibald JM (2015) Endosymbiosis and eukaryotic cell evolution. Curr Biol 25:R911–R921. https://doi.org/10.1016/j.cub.2015.07.055
Arimura S, Tsutsumi N (2002) A dynamin-like protein (ADL2b), rather than FtsZ, is involved in Arabidopsis mitochondrial division. Proc Natl Acad Sci U S A 99(8):5727–5731. https://doi.org/10.1073/pnas.082663299
Baum DA, Baum B (2014) An inside-out origin for the eukaryotic cell. BMC Biol 12:1. https://doi.org/10.1186/s12915-014-0076-2
Beech PL et al (2000) Mitochondrial FtsZ in a chromophyte alga. Science 287(5456):1276–1279
Berk JM, Tifft KE, Wilson KL (2013) The nuclear envelope LEM-domain protein emerin. Nucleus 4(4):298–314. https://doi.org/10.4161/nucl.25751
Bi EF, Lutkenhaus J (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354(6349):161–164. https://doi.org/10.1038/354161a0
Bleazard W et al (1999) The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat Cell Biol 1(5):298–304. https://doi.org/10.1038/13014
Burma S, Chen BP, Murphy M et al (2001) ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem 276:42462–42467. https://doi.org/10.1074/jbc.C100466200
Cavalier-Smith T (1987) The simultaneous symbiotic origin of mitochondria, chloroplasts, and microbodies. Ann N Y Acad Sci 503:55–71
Chen MS et al (1991) Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis. Nature 351(6327):583–586. https://doi.org/10.1038/351583a0
Copenhaver GP, Pikaard CS (1996) RFLP and physical mapping with an rDNA-specific endonuclease reveals that nucleolus organizer regions of Arabidopsis thaliana adjoin the telomeres on chromosomes 2 and 4. Plant J 9:259–272. https://doi.org/10.1046/j.1365-313X.1996.09020259.x
De Souza CPC, Osmani SA (2007) Mitosis, not just open or closed. Eukaryot Cell 6:1521–1527. https://doi.org/10.1128/EC.00178-07
DuBois KN et al (2012) NUP-1 is a large coiled-coil nucleoskeletal protein in trypanosomes with lamin-like functions. PLoS Biol 10(3):e1001287. https://doi.org/10.1371/journal.pbio.1001287
Elgass K, Pakay J, Ryan MT, Palmer CS (2013) Recent advances into the understanding of mitochondrial fission. Biochim Biophys Acta, Mol Cell Res 1833(1):150–161. https://doi.org/10.1016/j.bbamcr.2012.05.002
Faelber K et al (2011) Crystal structure of nucleotide-free dynamin. Nature 477(7366):556–560. https://doi.org/10.1038/nature10369
Fekkes P, Shepard KA, Yaffe MP (2000) Gag3p, an outer membrane protein required for fission of mitochondrial tubules. J Cell Biol 151(2):333–340
Ford MGJ, Jenni S, Nunnari J (2011) The crystal structure of dynamin. Nature 477(7366):561–566. https://doi.org/10.1038/nature10441
Friedman JR, Nunnari J (2014) Mitochondrial form and function. Nature 505(7483):335–343. https://doi.org/10.1038/nature12985
Fujiwara T et al (2009) Periodic gene expression patterns during the highly synchronized cell nucleus and organelle division cycles in the unicellular red alga Cyanidioschyzon merolae. DNA Res 16(1):59–72. https://doi.org/10.1093/dnares/dsn032
Fujiwara T, Tanaka K, Kuroiwa T, Hirano T (2013) Spatiotemporal dynamics of condensins I and II: evolutionary insights from the primitive redalga Cyanidioschyzon merolae. Mol Biol Cell 24(16):2515–2527. https://doi.org/10.1091/mbc.E13-04-0208
Galy V et al (2008) A role for gp210 in mitotic nuclear-envelope breakdown. J Cell Sci 121:317–328. https://doi.org/10.1242/jcs.022525
Gandre-Babbe S, van der Bliek AM (2008) The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells. Mol Biol Cell 19(6):2402–2412. https://doi.org/10.1091/mbc.E07-12-1287
Gao H, Kadirjan-Kalbach D, Froehlich JE, Osteryoung KW (2003) ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplastdivision machinery. Proc Natl Acad Sci U S A 100(7):4328–4333. https://doi.org/10.1073/pnas.0530206100
Gillham NW, Boynton JE, Hauser CR (1994) Translational regulation of gene expression in chloroplasts and mitochondria. Annu Rev Genet 28:71–93. https://doi.org/10.1146/annurev.ge.28.120194.000443
Gilson PR, Beech PL (2001) Cell division protein FtsZ: running rings around bacteria, chloroplasts and mitochondria. Res Microbiol 152(1):3–10
Glynn JM, Froehlich JE, Osteryoung KW (2008) Arabidopsis ARC6 coordinates the division machineries of the inner and outer chloroplast membranes through interaction with PDV2 in the intermembrane space. Plant Cell 20(9):2460–2470. https://doi.org/10.1105/tpc.108.061440
Glynn JM et al (2009) PARC6, a novel chloroplast division factor, influences FtsZ assembly and is required for recruitment of PDV1 during chloroplast division in Arabidopsis. Plant J 59(5):700–711. https://doi.org/10.1111/j.1365-313X.2009.03905.x
Griffin EE, Graumann J, Chan DC (2005) The WD40 protein Caf4p is a component of the mitochondrial fission machinery and recruits Dnm1p to mitochondria. J Cell Biol 170(2):237–248. https://doi.org/10.1083/jcb.200503148
Gueiros-Filho FJ, Losick R (2002) A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes Dev 16(19):2544–2556. https://doi.org/10.1101/gad.1014102
Hashimoto H (1986) Double ring structure around the constricting neck of dividing plastids of Avena sativa. Protoplasma 135(2–3):166–172
Hayashi T, Rizzuto R, Hajnoczky G, T-P S (2009) MAM: more than just a housekeeper. Trends Cell Biol 19:81–88. https://doi.org/10.1016/j.tcb.2008.12.002
Hoppins S (2014) The regulation of mitochondrial dynamics. Curr Opin Cell Biol 29:46–52. https://doi.org/10.1016/j.ceb.2014.03.005
Imoto Y et al (2013) Single-membrane-bounded peroxisome division revealed by isolation of dynamin-based machinery. Proc Natl Acad Sci U S A 110(23):9583–9588. https://doi.org/10.1073/pnas.1303483110
Ingerman E et al (2005) Dnm1 forms spirals that are structurally tailored to fit mitochondria. J Cell Biol 170(7):1021–1027. https://doi.org/10.1083/jcb.200506078
Kalashnikova AA, Rogge RA, Hansen JC (2016) Linker histone H1 and protein-protein interactions. Biochim Biophys Acta 1859(3):455–461. https://doi.org/10.1016/j.bbagrm.2015.10.004
Kato S, Imoto Y, Ohnuma M et al (2011) Aurora kinase of a red alga Cyanidioschyzon merolae is related to both mitochondrial division and mitotic spindle formation. Cytologia 76:465–472. https://doi.org/10.1508/cytologia.76.455
Kawashima T et al (2015) Diversification of histone H2A variants during plant evolution. Trends Plant Sci 20(7):419–425. https://doi.org/10.1016/j.tplants.2015.04.005
Koenig JH, Ikeda K (1989) Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J Neurosci 9(11):3844–3860
Krüger A (2012) Characterization of NE81, the first lamin-like nucleoskeleton protein in a unicellular organism. Mol Biol Cell 23(2):360–370. https://doi.org/10.1091/mbc.E11-07-0595
Kuroiwa T (1998) The primitive red algae Cyanidium caldarium and Cyanidioschyzon merolae as model system for investigating the dividing apparatus of mitochondria and plastids. BioEssays 20(4):344–354. https://doi.org/10.1002/(SICI)1521-1878(199804)20:4<344::AIDBIES11>3.0.CO;2-2
Kuroiwa T, Ohta T, Kuroiwa H, Shigeyuki K (1994) Molecular and cellular mechanisms of mitochondrial nuclear division and mitochondriokinesis. Microsc Res Tech 27(3):220–232. https://doi.org/10.1002/jemt.1070270304
Kuroiwa T et al (1995) Mitochondria-dividing ring: ultrastructural basis for the mechanism of mitochondrial division in Cyanidioschyzon merolae. Protoplasma 186:12–23
Kuroiwa T et al (1998) The division apparatus of plastids and mitochondria. Int Rev Cytol 181:1–41
Kuroiwa H, Mori T, Takahara M et al (2002) Chloroplast division machinery as revealed by immunofluorescence and electron microscopy. Planta 215(2):185–190. https://doi.org/10.1007/s00425-002-0734-4
Kuroiwa T et al (2006) Structure, function and evolution of the mitochondrial division apparatus. Biochim Biophys Acta 1763(5–6):510–521. https://doi.org/10.1016/j.bbamcr.2006.03.007
Lane N, Martin W (2010) The energetics of genome complexity. Nature 467(7318):929–934. https://doi.org/10.1038/nature09486
Lee J, Kim DH, Hwang I (2014) Specific targeting of proteins to outer envelope membranes of endosymbiotic organelles, chloroplasts, and mitochondria. Front Plant Sci. https://doi.org/10.3389/fpls.2014.00173
Liu R, Chan DC (2015) The mitochondrial fission receptor Mff selectively recruits oligomerized Drp1. Mol Biol Cell:1–27. https://doi.org/10.1091/mbc.E15-08-0591
Losón OC, Song Z, Chen H, Chan DC (2013) Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission. Mol Biol Cell 24(5):659–667. https://doi.org/10.1091/mbc.E12-10-0721
Löwe J, Amos LA (1998) Crystal structure of the bacterial cell-division protein FtsZ. Nature 391(6663):203–206. https://doi.org/10.1038/34472
Maple J et al (2004) GIANT CHLOROPLAST 1 is essential for correct plastid division in Arabidopsis. Curr Biol 14(9):776–781. https://doi.org/10.1016/j.cub.2004.04.031
Martin WF, Garg S, Zimorski V (2015) Endosymbiotic theories for eukaryote origin. Phil Trans R Soc B 370:20140330. https://doi.org/10.1098/rstb.2014.0330
Maruyama S et al (2004) The minimal eukaryotic ribosomal DNA units in the primitive red alga Cyanidioschyzon merolae. DNA Res 11(2):83–91
Maruyama S, Kuroiwa H, Miyagishima S-Y et al (2007) Centromere dynamics in the primitive red alga Cyanidioschyzon merolae. Plant J 49:1122–1129. https://doi.org/10.1111/j.1365-313X.2006.03024.x
Masuda K et al (1997) Peripheral framework of carrot cell nucleus contains a novel protein predicted to exhibit a long alpha-helical domain. Exp Cell Res 232:173–181. https://doi.org/10.1006/excr.1997.3531
Matsuanga S, Katagiri Y, Nagashima Y et al (2013) New insights into the dynamics of plant cell nuclei and chromosomes. Int Rev Cell Mol Biol 305:253–301. https://doi.org/10.1016/B978-0-12-407695-2.00006-8
Matsuzaki M et al (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428(6983):653–657. https://doi.org/10.1038/nature02398
McKeon FD, Kirschner MW, Caput D (1986) Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature 319(6053):463–468. https://doi.org/10.1038/319463a0
Mears JA et al (2011) Conformational changes in Dnm1 support a contractile mechanism for mitochondrial fission. Nat Struct Mol Biol 18(1):20–26. https://doi.org/10.1038/nsmb.1949
Meinke P, Schirmer EC (2015) LINC'ing form and function at the nuclear envelope. FEBS Lett 589:2514–2521. https://doi.org/10.1016/j.febslet.2015.06.011
Misumi O et al (2005) Cyanidioschyzon merolae genome. A tool for facilitating comparable studies on organelle biogenesis in photosynthetic eukaryotes. Plant Physiol 137(2):567–585. https://doi.org/10.1104/pp.104.053991
Mita T, Kanbe T, Tanaka K, Kuroiwa T (1986) A ring structure around the dividing plane of the Cyanidium caldarium chloroplast. Protoplasma 130(2–3):211–213
Miyagishima S-Y, Kabeya Y (2010) Chloroplast division: squeezing the photosynthetic captive. Curr Opin Microbiol 13(6):738–746. https://doi.org/10.1016/j.mib.2010.10.004
Miyagishima S-Y et al (1998) Identification of a triple ring structure involved in plastid division in the primitive red alga Cyanidioschyzon merolae. J Electron Microsc 47(3):269–272. https://doi.org/10.1093/oxfordjournals.jmicro.a023589
Miyagishima S, Itoh R, Toda K et al (1999) Real-time analyses of chloroplast and mitochondrial division and differences in the behavior of their dividing rings during contraction. Planta 207(3):343–353. https://doi.org/10.1007/s004250050491
Miyagishima S, Takahara M, Kuroiwa T (2001a) Novel filaments 5 nm in diameter constitute the cytosolic ring of the plastid division apparatus. Plant Cell 13(3):707–721
Miyagishima SY et al (2001b) Plastid division is driven by a complex mechanism that involves differential transition of the bacterial and eukaryotic division rings. Plant Cell 13(10):2257–2268. https://doi.org/10.1105/tpc.010185
Miyagishima S et al (2003) A plant-specific dynamin-related protein forms a ring at the chloroplast division site. Plant Cell Online 15(3):655–665
Miyagishima S et al (2004) Two types of FtsZ proteins in mitochondria and red-lineage chloroplasts: the duplication of FtsZ is implicated in endosymbiosis. J Mol Evol 58(3):291–303. https://doi.org/10.1007/s00239-003-2551-1
Miyagishima S, Kuwayama H, Urushihara H, Nakanishi H (2008) Evolutionary linkage between eukaryotic cytokinesis and chloroplast division by dynamin proteins. Proc Natl Acad Sci U S A 105(39):15202–15207. https://doi.org/10.1073/pnas.0802412105
Miyagishima S-Y, Kabeya Y, Sugita C et al (2014) DipM is required for peptidoglycan hydrolysis during chloroplast division. BMC Plant Biol 14:57. https://doi.org/10.1186/1471-2229-14-57.
Mori T, Kuroiwa H, Takahara M et al (2001) Visualization of an FtsZ ring in chloroplasts of Lilium longiflorum leaves. Plant Cell Physiol 42:555–559
Mozdy AD, McCaffery JM, Shaw JM (2000) Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p. J Cell Biol 151(2):367–379. https://doi.org/10.1083/jcb.151.2.367
Muñoz-Gómez SA, Slamovits CH, Dacks JB et al (2015) Ancient homology of the mitochondrial contact site and cristae organizing system points to an endosymbiotic origin of mitochondrial cristae. Curr Biol 25:1489–1495. https://doi.org/10.1016/j.cub.2015.04.006
Niemann A, Ruegg M, La Padula V et al (2005) Ganglioside-induced differentiation associated protein 1 is a regulator of the mitochondrial network: new implications for Charcot-Marie-tooth disease. J Cell Biol 170(7):1067–1078. https://doi.org/10.1083/jcb.200507087
Nishida K et al (2003) Dynamic recruitment of dynamin for final mitochondrial severance in a primitive red alga. Proc Natl Acad Sci U S A 100(4):2146–2151. https://doi.org/10.1073/pnas.0436886100
Nishida K, Yagisawa F, Kuroiwa H et al (2005) Cell cycle-regulated, microtubule-independent organelle division in Cyanidioschyzon merolae. Mol Biol Cell 16(May):2493–2502. https://doi.org/10.1091/mbc.E05-01-0068
Nishida K, Yagisawa F, Kuroiwa H et al (2007) WD40 protein Mda1 is purified with Dnm1 and forms a dividing ring for mitochondria before Dnm1 in Cyanidioschyzon merolae. Proc Natl Acad Sci U S A 104(11):4736–4741. https://doi.org/10.1073/pnas.0609364104
Nogales E, Wolf SG, Downing KH et al (1998) Structure of the alpha beta tubulin dimer by electron crystallography. Nature 393:199–203. https://doi.org/10.1038/34465
Okamura E, Sakamoto T, Sasaki T, Matsunaga S (2017) A plant ancestral polo-like kinase sheds light on the mystery of the evolutionary disappearance of polo-like kinases in the plant kingdom. Cytologia 82(3):261–266. https://doi.org/10.1508/cytologia.82.261
Olins AL, Rhodes G, Welch DB et al (2010) Lamin B receptor: multi-tasking at the nuclear envelope. Nucleus 1(1):53–70. https://doi.org/10.4161/nucl.1.1.10515
Oliva MA, Cordell SC, Löwe J (2004) Structural insights into FtsZ protofilament formation. Nat Struct Mol Biol 11(12):1243–1250. https://doi.org/10.1038/nsmb855
Osawa M, Anderson DE, Erickson HP (2008) Reconstitution of contractile FtsZ rings in liposomes. Science 320(5877):792–794. https://doi.org/10.1126/science.1154520
Osteryoung KW, Vierling E (1995) Conserved cell and organelle division. Nature 376(6540):473–474. https://doi.org/10.1038/376473b0
Palmer CS et al (2011) MiD49 and MiD51, new components of the mitochondrial fission machinery. EMBO Rep 12(6):565–573. https://doi.org/10.1038/embor.2011.54
Paull TT et al (2000) A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 10(15):886–895
Praefcke GJK, McMahon HT (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5(2):133–147. https://doi.org/10.1038/nrm1313
Roy M, Reddy PH, Iijima M, Sesaki H (2015) Mitochondrial division and fusion in metabolism. Curr Opin Cell Biol 33:111–118. https://doi.org/10.1016/j.ceb.2015.02.001
Sakamoto Y, Takagi S (2013) LITTLE NUCLEI 1 and 4 regulate nuclear morphology in Arabidopsis thaliana. Plant Cell Physiol 54(4):622–633. https://doi.org/10.1093/pcp/pct031
Schmitz AJ, Glynn JM, Olson BJSC et al (2009) Arabidopsis FtsZ2-1 and FtsZ2-2 are functionally redundant, but FtsZ-based plastid division is not essential for chloroplast partitioning or plant growth and development. Mol Plant 2(6):1211–1222. https://doi.org/10.1093/mp/ssp077
Shibata S, Matsuoka Y, Yoneda Y (2002) Nucleocytoplasmic transport of proteins and poly(A) RNA in reconstituted Tpr-less nuclei in living mammalian cells. Genes Cells 7:421–434
Shimada H et al (2004) ARC3, a chloroplast division factor, is a chimera of prokaryotic FtsZ and part of eukaryotic phosphatidylinositol-4-phosphate 5-kinase. Plant Cell Physiol 45(8):960–967. https://doi.org/10.1093/pcp/pch130
Shpetner HS, Vallee RB (1989) Identification of dynamin, a novel mechanochemical enzyme that mediates interactions between microtubules. Cell 59(3):421–432
Smirnova E, Shurland D-L, Ryazantsev SN et al (1998) A human dynamin-related protein controls the distribution of mitochondria. J Cell Biol 143(2):351–358
Smythe C, Jenkins HE, Hutchison CJ (2000) Incorporation of the nuclear pore basket protein nup153 into nuclear pore structures is dependent upon lamina assembly: evidence from cell-free extracts of Xenopus eggs. EMBO J 19:3918–3931. https://doi.org/10.1093/emboj/19.15.3918
Spang A, Saw JH, Jorgensen SL et al (2015) Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521:173–179. https://doi.org/10.1038/nature14447
Stiff T, O'Driscoll M, Rief N et al (2004) ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res 64:2390–2396
Sumiya N, Hirata A, Kawano S (2008) Multiple FtsZ ring formation and reduplicated chloroplast DNA in Nannochloris bacillaris (Chlorophyta, Trebouxiophyceae) under phosphate-enriched culture. J Phycol 44(6):1476–1489. https://doi.org/10.1111/j.1529-8817.2008.00589.x
Takahara M et al (2000) A putative mitochondrial ftsZ gene is present in the unicellular primitive red alga Cyanidioschyzon merolae. Mol Gen Genet 264(4):452–460
Tamura K, Hara-Nishimura I (2013) The molecular architecture of the plant nuclear pore complex. J Exp Bot 64(4):823–832. https://doi.org/10.1093/jxb/ers258
Tamura K, Fukao Y, Iwamoto M et al (2010) Identification and characterization of nuclear pore complex components in Arabidopsis thaliana. Plant Cell 22:4084–4097. https://doi.org/10.1105/tpc.110.079947
TerBush AD, Osteryoung KW (2012) Distinct functions of chloroplast FtsZ1 and FtsZ2 in Z-ring structure and remodeling. J Cell Biol 199(4):623–637. https://doi.org/10.1083/jcb.201205114
TerBush AD, Yoshida Y, Osteryoung KW (2013) FtsZ in chloroplast division: structure, function and evolution. Curr Opin Cell Biol 25(4):461–470. https://doi.org/10.1016/j.ceb.2013.04.006
Tieu Q, Nunnari J (2000) Mdv1p is a WD repeat protein that interacts with the dynamin-related GTPase, Dnm1p, to trigger mitochondrial division. J Cell Biol 151(2):353–365
van der Bliek AM, Meyerowitz EM (1991) Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature 351(6325):411–414. https://doi.org/10.1038/351411a0
van der Bliek AM, Shen Q, Kawajiri S (2013) Mechanisms of mitochondrial fission and fusion. Cold Spring Harb Perspect Biol 5(6):1–16. https://doi.org/10.1101/cshperspect.a011072
Vitha S, McAndrew RS, Osteryoung KW (2001) FtsZ ring formation at the chloroplast division site in plants. J Cell Biol 153:111–120
Wang H, Wang M, Wang H et al (2005) Complex H2AX phosphorylation patterns by multiple kinases including ATM and DNA-PK in human cellsexposed to ionizing radiation and treated with kinase inhibitors. J Cell Physiol 202:492–502. https://doi.org/10.1002/jcp.20141
XM X et al (2007) NUCLEAR PORE ANCHOR, the Arabidopsis homolog of Tpr/Mlp1/Mlp2/megator, is involved in mRNA export and SUMO homeostasis and affects diverse aspects of plant development. Plant Cell 19:1537–1548. https://doi.org/10.1105/tpc.106.049239
Yaffe MP (1999) The machinery of mitochondrial inheritance and behavior. Science 283(5407):1493–1497
Yagisawa F et al (2012) Mitotic inheritance of endoplasmic reticulum in the primitive red alga Cyanidioschyzon merolae. Protoplasma 249(4):1129–1135. https://doi.org/10.1007/s00709-011-0359-1
Yoon Y, Krueger EW, Oswald BJ, McNiven MA (2003) The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol Cell Biol 23(15):5409–5420
Yoshida Y, Mogi Y (2016) Reconstitution of the chloroplast FtsZ ring using the heterologous yeast system Pichia pastoris. Cytologia (Tokyo) 81(3):249–250. https://doi.org/10.1508/cytologia.81.249
Yoshida Y et al (2006) Isolated chloroplast division machinery can actively constrict after stretching. Science 313(5792):1435–1438. https://doi.org/10.1126/science.1129689
Yoshida Y, Nishida K, Kawano S, Kuroiwa T (2008) Novel dynamics of FtsZ ring before plastid abscission. Cytologia 73:197–201
Yoshida Y et al (2009) The bacterial ZapA-like protein ZED is required for mitochondrial division. Curr Biol 19(17):1491–1497. https://doi.org/10.1016/j.cub.2009.07.035
Yoshida Y et al (2010) Chloroplasts divide by contraction of a bundle of nanofilaments consisting of polyglucan. Science 329(5994):949–953. https://doi.org/10.1126/science.1190791
Yoshida Y, Miyagishima S-Y, Kuroiwa H, Kuroiwa T (2012) The plastid-dividing machinery: formation, constriction and fission. Curr Opin Plant Biol 15(6):714–721. https://doi.org/10.1016/j.pbi.2012.07.002
Yoshida Y, Fujiwara T, Imoto Y et al (2013) The kinesin-like protein TOP promotes aurora localisation and induces mitochondrial, chloroplast and nuclear division. J Cell Sci 126:2392–2400. https://doi.org/10.1242/jcs.116798
Yoshida Y, Mogi Y, TerBush AD, Osteryoung KW (2016) Chloroplast FtsZ assembles into a contractible ring via tubulin-like heteropolymerization. Nat Plants 2(7):16095. https://doi.org/10.1038/nplants.2016.95
Zaremba-Niedzwiedzka K, Caceres EF, Saw JH et al (2017) Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541:353–358. https://doi.org/10.1038/nature21031
Zhang M, Chen C, Froehlich JE et al (2015) Roles of Arabidopsis PARC6 in coordination of the chloroplast division complex and negative regulation of FtsZ assembly. Plant Physiol 170(517):01460.2015. https://doi.org/10.1104/pp.15.01460
Zhou X, Groves NR, Meier I (2015) Plant nuclear shape is independently determined by the SUN-WIP-WIT2-myosin XI-i complex and CRWN1. Nucleus 6(2):144–153. https://doi.org/10.1080/19491034.2014.1003512
Acknowledgments
This work was supported by a Human Frontier Science Program Long Term Fellowship (No. LT000356/2011-L) to Y.Y. and a grant for XFEL key technology and the X-ray Free Electron Laser Priority Strategy Program from MEXT to Sa.M. (Tokyo University of Science), MEXT/JSPS KAKENHI No. JP26291067 and JP15H05962 to Sa.M. (Tokyo University of Science), and JP15K18562 to Sh.M. (Tohoku University).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Yoshida, Y., Sakamoto, Y., Iwasaki, K., Maruyama, S., Matsunaga, S. (2017). Double-Membrane-Bounded Organelles: Recent Findings Regarding Division, Inheritance, Structure, and Evolution of the Nucleus, Mitochondria, and Chloroplasts. In: Kuroiwa, T., et al. Cyanidioschyzon merolae. Springer, Singapore. https://doi.org/10.1007/978-981-10-6101-1_14
Download citation
DOI: https://doi.org/10.1007/978-981-10-6101-1_14
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-10-6100-4
Online ISBN: 978-981-10-6101-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)