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The ultrastructural features and division of secondary plastids

  • Current Topics in Plant Research
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Abstract

Plastids in heterokonts, cryptophytes, haptophytes, dinoflagellates, chlorarachniophytes, euglenoids, and apicomplexan parasites derive from secondary symbiogenesis. These plastids are surrounded by one or two additional membranes covering the plastid-envelope double membranes. Consequently, nuclear-encoded plastid division proteins have to be targeted into the division site through the additional surrounding membranes. Electron microscopic observations suggest that the additional surrounding membranes are severed by mechanisms distinct from those for the division of the plastid envelope. In heterokonts, cryptophytes and haptophytes, the outermost surrounding membrane (epiplastid rough endoplasmic reticulum, EPrER) is studded with cytoplasmic ribosomes and connected to the rER and the outer nuclear envelope. In monoplastidic species belonging to these three groups, the EPrER and the outer nuclear envelope are directly connected to form a sac enclosing the plastid and the nucleus. This nuclear-plastid connection, referred to as the nucleus-plastid consortium (NPC), may be significant to ensure the transmission of the plastids during cell division. The plastid dividing-ring (PD-ring) is a conserved component of the division machinery for both primary and secondary plastids. Also, homologues of the bacterial cell division protein, FtsZ, may be involved in the division of secondary plastids as well as primary plastids, though in secondary plastids they have not yet been localized to the division site. It remains to be examined whether or not dynamin-like proteins and other protein components known to function in the division of primary plastids are used also in secondary plastids. The nearly completed sequencing of the nuclear genome of the diatom Thalassiosira pseudonana will give impetus to molecular and cell biological studies on the division of secondary plastids.

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References

  • Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kroger N, Lau WW, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86

    CAS  PubMed  Google Scholar 

  • Asano T, Yoshioka Y, Kurei S, Sakamoto W, Sodmergen, Machida Y (2004) A mutation of the CRUMPLED LEAF gene that encodes a protein localized in the outer envelope membrane of plastids affects the pattern of cell division, cell differentiation, and plastid division in Arabidopsis. Plant J 38:448–459

    Google Scholar 

  • Beech PL, Gilson PR (2000) FtsZ and organelle division in protists. Protist 151:11–16

    CAS  PubMed  Google Scholar 

  • Beech PL, Nheu T, Schultz T, Herbert S, Lithgow T, Gilson PR, McFadden GI (2000) Mitochondrial FtsZ in a chromophyte alga. Science 287:1276–1279

    Article  CAS  PubMed  Google Scholar 

  • Belcher JH (1969) Some remarks upon Mallomonas papillosa Harris and Bradley and M. calceolus Bradley. Nova Hedwigia 18:257–270

    Google Scholar 

  • Bhattacharya D, Medlin L (1998) Algal phylogeny and the origin of land plants. Plant Physiol 116:9–15

    Google Scholar 

  • Bleazard W, McCaffery JM, King EJ, Bale S, Mozdy A, Tieu Q, Nunnari J, Shaw JM (1999) The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat Cell Biol 1:298–304

    CAS  PubMed  Google Scholar 

  • Cavalier-Smith T (1989) The kingdom chromista. In: Green JC, Leadbeater BSC, Diver WL (eds) The chromophyte algae. Oxford University Press, New York, pp 381–407

    Google Scholar 

  • Cavalier-Smith T (2002a) The phagotrophic origin of eukaryotes and phylogenetic classification of protozoa. Int J Syst Evol Microbiol 52:297–354

    Google Scholar 

  • Cavalier-Smith T (2002b) Nucleomorphs: enslaved algal nuclei. Curr Opin Microbiol 5:612–619

    Google Scholar 

  • Cavalier-Smith T (2003) Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae). Phil Trans R Soc Lond B 358:109–134

    Article  CAS  Google Scholar 

  • Colletti KS, Tattersall EA, Pyke KA, Froelich JE, Stokes KD, Osteryoung KW (2000) A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus. Curr Biol 10:507–516

    Article  CAS  PubMed  Google Scholar 

  • Douglas SE (1998) Plastid evolution: origins, diversity, trends. Curr Opin Genet Dev 8:655–661

    CAS  PubMed  Google Scholar 

  • Douglas SE, Zauner S, Fraunholz M, Beaton M, Penny S, Deng L-T, Wu X, Reith M, Cavalier-Smith T, Maier U-G (2001) The highly reduced genome of an enslaved algal nucleus. Nature 410:1091–1096

    CAS  PubMed  Google Scholar 

  • Falciatore A, Casotti R, Leblanc C, Abrescia C, Bowler C (1999) Transformation of nonselectable reporter genes in marine diatoms. Mar Biotechnol 1:239–251

    CAS  PubMed  Google Scholar 

  • Fraunholz MJ, Moerschel E, Maier UG (1998) The chloroplast division protein FtsZ is encoded by a nucleomorph gene in cryptomonads. Mol Gen Genet 260:207–211

    Article  CAS  PubMed  Google Scholar 

  • Fulgosi H, Gerdes L, Westphal S, Glockmann C, Soll J (2002) Cell and chloroplast division requires ARTEMIS. Proc Natl Acad Sci USA 99:11501–11506

    Article  CAS  PubMed  Google Scholar 

  • Gao H, Kadirjan-Kalbach D, Froehlich JE, Osteryoung KW (2003) ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc Natl Acad Sci USA 100:4328–4333

    Article  CAS  PubMed  Google Scholar 

  • Gibbs SP (1962) Nuclear envelope-chloroplast relationships in algae. J Cell Sci 14:433–444

    CAS  Google Scholar 

  • Gibbs SP (1978) The chloroplasts of Euglena may have evolved from symbiotic green algae. Can J Bot 56:2883–2889

    Google Scholar 

  • Gibbs SP (1981) The chloroplast endoplasmic reticulum: structure, function, and evolutionary significance. Int Rev Cytol 72:49–99

    Google Scholar 

  • Gillott M, Gibbs SP (1980) The cryptomonad nucleomorph: its ultrastructure and evolutionary significance. J Phycol 16:558–568

    Article  Google Scholar 

  • Gilson PR, McFadden GI (1996) The miniaturized nuclear genome of a eukaryotic endosymbiont contains genes that overlap, genes that are cotranscribed, and the smallest known spliceosomal introns. Proc Natl Acad Sci USA 93:7737–7742

    CAS  PubMed  Google Scholar 

  • Gilson PR, McFadden GI (2002) Jam packed genomes—a preliminary, comparative analysis of nucleomorphs. Genetica 115:13–28

    CAS  PubMed  Google Scholar 

  • Greenwood AD (1974) The cryptophyta in relation to phylogeny and photosynthesis. No. 32. In: Sanders JV, Goodchild DJ (eds) 8th International Conference on Electron Microscopy, Australian Academy of Science, Canberra

  • Greenwood AD, Griffiths HB, Santore UJ (1977) Chloroplasts and cell compartments in Cryptophyceae. Br Phycol J 12:119

    Google Scholar 

  • Gu X, Verma DP (1996) Phragmoplastin, a dynamin-like protein associated with cell plate formation in plants. EMBO J 15:695–704

    CAS  PubMed  Google Scholar 

  • Hales KG, Fuller MT (1997) Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell 90:121–129

    CAS  PubMed  Google Scholar 

  • Hashimoto H (1986) Double ring structure around the constricting neck of dividing plastids of Avena sativa. Protoplasma 135:166–172

    Article  Google Scholar 

  • Hashimoto H (1997) Electron-opaque annular structure girdling the constricting isthmus of the dividing chloroplasts of Heterosigma akashiwo (Raphidophyceae, Chromophyta). Protoplasma 197:210–216

    Article  Google Scholar 

  • Hashimoto H (2003) Plastid division: its origins and evolution. Int Rev Cytol 222:63–98

    PubMed  Google Scholar 

  • Hibberd DJ, Norris RE (1984) Cytology and ultrastructure of Chlorarachnion reptans (Chlorarachniophyta division nova, Chlorarachniophyceae classis nova). J Phycol 20:310–330

    Article  Google Scholar 

  • Hinshaw JE (2000) Dynamin and its role in membrane fission. Annu Rev Cell Dev Biol 16:483–519

    CAS  PubMed  Google Scholar 

  • van den Hoek C, Mann DG, Jahns HM (1995) Algae: an introduction to phycology. Cambridge University Press, New York

    Google Scholar 

  • Hong ZL, Geisler-Lee CJ, Zhang ZM, Verma DPS (2003) Phragmoplastin dynamics: multiple forms, microtubule association and their roles in cell plate formation in plants. Plant Mol Biol 53:297–312

    CAS  PubMed  Google Scholar 

  • Hopkins J, Fowler R, Krishna S, Wilson I, Mitchell G, Bannister L (1999) The plastid in Plasmodium falciparum asexual blood stages: a three-dimensional ultrastructural analysis. Protist 150:283–292

    CAS  PubMed  Google Scholar 

  • Iino M, Hashimoto H (2003) Intermediate features of cyanelle division of Cyanophora paradoxa (Glaucocystophyta) between cyanobacterial and plastid division. J Phycol 39:561–569

    Article  Google Scholar 

  • Ishida K, Cavalier-Smith T, Green BR (2000) Endomembrane structure and the chloroplast protein targeting pathway in Heterosigma akashiwo (Raphidophyceae, Chromista). J Phycol 36:1135–1144

    CAS  Google Scholar 

  • Itoh R, Fujiwara M, Nagata N, Yoshida S (2001) A chloroplast protein homologous to the eubacterial topological specificity factor MinE plays a role in chloroplast division. Plant Physiol 127:1644–1655

    CAS  PubMed  Google Scholar 

  • Jin J Kim YA, Kim SJ, Lee SH, Kim DH, Cheong GW, Hwang I (2001) A new dynamin-like protein, ADL6, is involved in trafficking from the trans-Golgi network to the central vacuole in Arabidopsis. Plant Cell 13:1511–1525

    Google Scholar 

  • Keeling P (2004) A brief history of plastids and their hosts. Protist 155:3–7

    CAS  PubMed  Google Scholar 

  • Kiefel BR, Gilson PR, Beech PL (2004) Diverse eukaryotes have retained mitochondrial homologues of the bacterial division protein FtsZ. Protist 155:105–115

    CAS  PubMed  Google Scholar 

  • Koch A, Thiemann M, Grabenbauer M, Yoon Y, McNiven MA, Schrader M (2003) Dynamin-like protein 1 is involved in peroxysomal fission. J Biol Chem 278:8597–8605

    CAS  PubMed  Google Scholar 

  • Kochs G, Haener M, Aebi U, Haller O (2002) Self-assembly of human MxA GTPase into highly ordered dynamin-like oligomers. J Biol Chem 277:14172–14176

    CAS  PubMed  Google Scholar 

  • Kuroiwa T, Sakai A, Takahashi H, Toda K, Itoh R (1998) The division apparatus of plastid and mitochondria. Int Rev Cytol 181:1–41

    CAS  PubMed  Google Scholar 

  • Labrousse AM, Zappaterra MD, Rube DA, van Bliek AM (1999) C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol Cell 4:815–826

    CAS  PubMed  Google Scholar 

  • Li X, Gould SJ (2003) The dynamin-like GTPase DLP1 is essential for peroxysome division and is recruited to peroxysomes in part by PEX11. J Biol Chem 278:17012–17020

    CAS  PubMed  Google Scholar 

  • Löffelhardt W, Bohnert HJ, Bryant DA (1997) The cyanelles of Cyanophora paradoxa. Crit Rev Plant Sci 16:393–413

    Google Scholar 

  • Ludwig M, Gibbs SP (1985) DNA is present in the nucleomorphs of cryptomonads: further evidence that the chloroplast evolved from a eukaryotic endosymbiont. Protoplasma 127:9–20

    Article  Google Scholar 

  • Ludwig M, Gibbs SP (1989) Evidence that the nucleomorphs of Chlorarachnion reptans (Chlorarachniophyceae) are vestigial nuclei: morphology, division and DNA-DAPI fluorescence. J Phycol 25:385–394

    Google Scholar 

  • Lutkenhaus J, Addinall SG (1997) Bacterial cell division and the Z ring. Annu Rev Biochem 66:93–116

    CAS  PubMed  Google Scholar 

  • Maier UG, Douglas SE, Cavalier-Smith T (2000) The nucleomorph genomes of cryptophytes and chlorarachniophytes. Protist 151:103–109

    CAS  PubMed  Google Scholar 

  • Maple J, Fujiwara MT, Kitahata N, Lawson T, Baker NR, Yoshida S, Moller SG (2004) GIANT CHLOROPLAST 1 is essential for correct plastid division in Arabodopsis. Curr Biol 14:776–781

    CAS  PubMed  Google Scholar 

  • Margolin W (2000) Themes and variations in prokaryotic cell division. FEMS Microbiol Rev 24:531–548

    Google Scholar 

  • Marks B, Stowel MHB, Vallis Y, Mills IG, Gibson A, Hopkins CR, McMahon HT (2001) GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410:231–235

    CAS  PubMed  Google Scholar 

  • Matsuzaki M, Misumi O, Shin-I T, Maruyama S, Takahara M, Miyagishima S, Mori T, Nishida K, Yagisawa F, Nishida K, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, Minoda A, Sano M, Nomoto H, Oishi K, Hayashi H, Ohta N, Nishizawa S, Haga S, Miura S, Morishita T, Kabeya Y, Terasawa K, Suzuki Y, Ishii Y, Asakawa S, Takano H, Ohta N, Kuroiwa H, Tanaka K, Shimizu N, Sugano S, Sato N, Nozaki H, Ogasawara N, Kohara Y, Kuroiwa T (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657

    Article  CAS  PubMed  Google Scholar 

  • McAndrew RS, Froehlich JE, Vitha S, Stokes KD, Osteryoung KW (2001) Colocalization of plastid division proteins in the chloroplast stromal compartment establishes a new functional relationship between FtsZ1 and FtsZ2 in higher plants. Plant Physiol 127:1656–1666

    CAS  PubMed  Google Scholar 

  • McFadden GI, Gilson PR, Douglas SE (1994) The photosynthetic endosymbiont in cryptomonad cells produces both chloroplast and cytoplasmic-type ribosomes. J Cell Sci 107:649–657

    CAS  PubMed  Google Scholar 

  • McKerracher L, Gibbs SP (1982) Cell and nucleomorph division in the alga Cryptomonas. Can J Bot 60:2440–2452

    Google Scholar 

  • Mita T, Kuroiwa T (1988) Division of plastids by a plastid-dividing ring in Cyandium caldarium. Protoplasma Suppl 1:133–152

    Google Scholar 

  • Mita T, Kanbe T, Tanaka K, Kuroiwa T (1986) A ring structure around the dividing plane of the Cyanidium caldarium chloroplast. Protoplasma 130:211–213

    Article  Google Scholar 

  • Miyagishima S, Takahara M, Kuroiwa T (2001a) Novel filaments 5 nm in diameter constitute the cytosolic ring of the plastid division apparatus. Plant Cell 13:707–721

    Google Scholar 

  • Miyagishima S, Takahara M, Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T (2001b) Plastid division is driven by a complex mechanism that involves differential transition of the bacterial and eukaryotic division rings. Plant Cell 13:2257–2268

    Google Scholar 

  • Miyagishima S, Nishida K, Kuroiwa T (2003a) An evolutionary puzzle: chloroplast and mitochondrial division rings. Trends Plant Sci 8:432–438

    CAS  PubMed  Google Scholar 

  • Miyagishima S, Nishida K, Mori T, Matsuzaki M, Higashiyama T, Kuroiwa H, Kuroiwa T (2003b) A plant-specific dynamin-related protein forms a ring at the chloroplast division site. Plant Cell 15:655–665

    Google Scholar 

  • Miyagishima S, Nozaki H, Nishida K, Nishida K, Matsuzaki M, Kuroiwa T (2004) Two types of FtsZ proteins in mitochondrial and red-lineage chloroplasts: the duplication of FtsZ is implicated in endosymbiosis. J Mol Evol 58:291–303

    CAS  PubMed  Google Scholar 

  • Moestrup Ø (1982) Flagellar structure in algae: a review, with new observations particularly on the Chrysophyceae, Phaeophyceae (Fucophyceae), Euglenophyceae, and Rickertia. Phycologia 21:427–528

    Google Scholar 

  • Moestrup Ø, Sengco M (2001) Ultrastructural studies on Bigelowiella natans, gen. et sp. nov., a chlorarachniophyte flagellate. J Phycol 37:624–646

    Article  Google Scholar 

  • Mori T, Kuroiwa H, Takahara M, Miyagishima S, Kuroiwa T (2001) Visualization of an FtsZ-ring in chloroplasts of Lilium longiflorum leaves. Plant Cell Physiol 42:555–559

    CAS  PubMed  Google Scholar 

  • Morrall S, Greenwood AD (1982) Ultrastructure of nucleomorph division in species of Cryptophyceae and its evolutionary implications. J Cell Sci 54:311–328

    Google Scholar 

  • Nishida K, Takahara M, Miyagishima S, Kuroiwa H, Matsuzaki M, Kuroiwa T (2003) Dynamic recruitment of dynamin for final mitochondrial severance in a primitive red alga. Proc Natl Acad Sci USA 100:2146–2151

    CAS  PubMed  Google Scholar 

  • Nozaki H, Matsuzaki M, Takahara M, Misumi O, Kuroiwa H, Hasegawa M, Shin-I T, Kohara Y Ogasawara N, Kuroiwa T (2003) The phylogenetic position of red algae revealed by multiple nuclear genes from mitochondrial-containing eukaryotes and an alternative hypothesis on the origin of plastids. J Mol Evol 56:485–497

    CAS  PubMed  Google Scholar 

  • Osteryoung KW, McAndrew RS (2001) The plastid division machine. Annu Rev Plant Physiol Plant Mol Biol 52:315–333

    CAS  PubMed  Google Scholar 

  • Osteryoung KW, Nunnari J (2003) The division of endosymbiotic organelles. Science 302:1698–1704

    CAS  PubMed  Google Scholar 

  • Osteryoung KW, Vierling E (1995) Conserved cell and organelle division. Nature 376:473–474

    CAS  PubMed  Google Scholar 

  • Osteryoung KW, Stokes KD, Rutherford SM, Percival AL, Lee WY (1998) Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ. Plant Cell 10:1991–2004

    CAS  PubMed  Google Scholar 

  • Palmer JD (2003) The symbiotic birth and spread of plastids: how many times and whodunit? J Phycol 39:4–11

    Article  CAS  Google Scholar 

  • Praefcke GJK, McMahon HT (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5:133–147

    CAS  PubMed  Google Scholar 

  • Pyke KA (1999) Plastid division and development. Plant Cell 11:549–556

    Google Scholar 

  • Pyke KA, Leech RM (1994) A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol 104:201–207

    Google Scholar 

  • RayChaudhuri D, Park JT (1992) Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein. Nature 359:251–254

    Google Scholar 

  • Raynaud C, Cassier-Chauvat C, Perennes C, Bergounioux C (2004) An Arabidopsis homolog of the bacterial cell division inhibitor SulA is involved in plastid division. Plant Cell 16:1801–1811

    Google Scholar 

  • Robertson EJ, Rutherford SM, Leech RM (1996) Characterization of chloroplast division using the Arabidopsis mutant arc5. Plant Physiol 112:149–159

    Google Scholar 

  • Schmid A-MM (2003) Endobacteria in the diatom Pinnularia (Bacillariophyceae). I. “Scattered ct-nucleoids” explained: DAPI-DNA complexes stem from exoplastidial bacteria boring into the chloroplasts. J Phycol 39:122–138

    Article  Google Scholar 

  • Schwartzbach SD, Osafune T, Löffelhardt W (1998) Protein import into cyanelles and complex chloroplasts. Plant Mol Biol 38:247–263

    Google Scholar 

  • Shimada H, Koizumi M, Kuroki K, Mochizuki M, Fujimoto H, Ohta H, Masuda T, Takamiya K, (2004) ARC3, a chloroplast division factor, is a chimera of prokaryotic FtsZ and part of eukaryotic phosphatidylinositol-4-phosphate 5-kinase. Plant Cell Physiol 45:960–967

    Google Scholar 

  • Strepp R, Scholz S, Kruse S, Speth V, Reski R (1998) Plant molecular gene knockout reveals a role in plastid division for the homolog of the bacterial cell division protein FtsZ, an ancestral tubulin. Proc Natl Acad Sci USA 95:4368–4373

    CAS  PubMed  Google Scholar 

  • Striepen B, Crawford MJ, Shaw MK, Tilney LG, Seeber F, Roos DS (2000) The plastid of Toxoplasma gondii is divided by association with the centrosomes. J Cell Biol 151:1423–1434

    CAS  PubMed  Google Scholar 

  • Takahara M, Takahashi H, Matsunaga S, Miyagishima S, Sakai A, Kawano S, Kuroiwa T (1999) Two types of ftsZ genes isolated from the unicellular primitive red alga Galdieria sulphuraria. Plant Cell Physiol 40:784–791

    Google Scholar 

  • Takahara M, Takahashi H, Matsunaga S, Miyagishima S, Sakai A, Kawano S, Kuroiwa T (2000) A putative mitochondrial ftsZ gene is encoded in the unicellular primitive red alga Cyanidioschyzon merolae. Mol Gen Genet 264:452–460

    CAS  PubMed  Google Scholar 

  • Taylor FJR (1974) Implications and extensions of the serial endosymbiosis theory of the origin of eukaryotes. Taxon 23:229–258

    Google Scholar 

  • Vaughan S, Wickstead B, Gull K, Addinall SG (2004) Molecular evolution of FtsZ protein sequences encoded within the genomes of Archea, Bacteria, and Eukaryota. J Mol Evol 58:19–39

    CAS  PubMed  Google Scholar 

  • Vitha S, McAndrew RS, Osteryoung KW (2001) FtsZ ring formation at the chloroplast division site in plants. J Cell Biol 153:111–119

    CAS  PubMed  Google Scholar 

  • Vitha S, Froehlich JE, Koksharova O, Pyke KA, van Erp H, Osteryoung KW (2003) ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 15:1918–1933

    CAS  PubMed  Google Scholar 

  • Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D (2004) A molecular timing for the origin of photosynthetic eukaryotes. Mol Biol Evol 21:809–818

    CAS  PubMed  Google Scholar 

  • Zaslavskaia LA, Lippmeier JC, Grossman AR, Apt KE (2000) Transformation of the diatom Phaeodactylum tricornutum (Bacillariophyceae) with a variety of selectable marker and reporter genes. J Phycol 36:379–386

    CAS  Google Scholar 

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Hashimoto, H. The ultrastructural features and division of secondary plastids. J Plant Res 118, 163–172 (2005). https://doi.org/10.1007/s10265-005-0214-6

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