Skip to main content
SpringerLink
Log in

Cellular Structure of Cyanidioschyzon merolae: A Minimum Set of Organelles

  • Chapter
  • First Online:
Cyanidioschyzon merolae

Abstract

The cell of the unicellular red alga Cyanidioschyzon merolae is composed of a very small number of membranous organelles: one cell nucleus, one mitochondrion, one chloroplast (plastid), a simple-shaped ER, one Golgi body with two cisternae, a few vacuoles (lysosomes), and one peroxisome. During the last two decades, numerous electron and fluorescence microscopic studies, combined with synchronous culture, have demonstrated spatial organization and morphological information of these organelles in each cell cycle phase of C. merolae cells. These explorations have revealed that the timing and manner of the organelle behaviors are strictly determined by the progression of the cell division cycle. In addition, the simplicity of the cell structure assists researchers to directly address the biological processes in each organelle. Concurrently, given the completely sequenced genome and various genetic technologies, the simple composition of C. merolae cells provides considerable opportunities to clarify long-standing biological questions, including cell cycle regulation, organelle biogenesis, and various types of metabolic pathways.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Institutional subscriptions

References

  • Fujiwara T, Misumi O, Tashiro K, Yoshida Y, Nishida K, Yagisawa F, Imamura S, Yoshida M, Mori T, Tanaka K, Kuroiwa H, Kuroiwa T (2009) Periodic gene expression patterns during the highly synchronized cell nucleus and organelle division cycles in the unicellular red alga Cyanidioschyzon merolae. DNA Res 16:59–72

    Google Scholar 

  • Fujiwara T, Kuroiwa H, Yagisawa F, Ohnuma M, Yoshida Y, Yoshida M, Nishida K, Misumi O, Watanabe S, Tanaka K et al (2010a) The coiled-coil protein VIG1 is essential for tethering vacuoles to mitochondria during vacuole inheritance of Cyanidioschyzon merolae. Plant Cell 22:772–781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujiwara T, Yagisawa F, Ohnuma M, Yoshida Y, Yoshida M, Nishida K, Misumi O, Kuroiwa H, Kuroiwa T (2010b) The vacuole binding to mitochondria by VIG1 contributes an equal inheritance of the vacuoles in Cyanidioschyzon merolae. Cytologia 75:189–194

    Article  CAS  Google Scholar 

  • Fujiwara T, Tanaka K, Kuroiwa T, Hirano T (2013) Spatiotemporal dynamics of condensins I and II: evolutionary insights from the primitive red alga Cyanidioschyzon merolae. Mol Biol Cell 24:2515–2527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujiwara T, Kanesaki Y, Hirooka S, Era A, Sumiya N, Yoshikawa H, Tanaka K, Miyagishima SY (2015) A nitrogen source-dependent inducible and repressible gene expression system in the red alga Cyanidioschyzon merolae. Front Plant Sci 6:657

    PubMed  PubMed Central  Google Scholar 

  • Hirooka S, Misumi O, Yoshida M, Mori T, Nishida K, Yagisawa F, Yoshida Y, Fujiwara T, Kuroiwa H, Kuroiwa T (2009) Expression of the Cyanidioschyzon merolae stromal ascorbate peroxidase in Arabidopsis thaliana enhances thermotolerance. Plant Cell Rep 28:1881–1893

    Article  CAS  PubMed  Google Scholar 

  • Imamura S, Kanesaki Y, Ohnuma M, Inouye T, Sekine Y, Fujiwara T, Kuroiwa T, Tanaka K (2009) R2R3-type MYB transcription factor, CmMYB1, is a central nitrogen assimilation regulator in Cyanidioschyzon merolae. Proc Nat Acad Sci 106:12548–12553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Imamura S, Terashita M, Ohnuma M, Maruyama S, Minoda A, Weber AP, Inouye T, Sekine Y, Fujita Y, Omata T et al (2010) Nitrate assimilatory genes and their transcriptional regulation in a unicellular red alga Cyanidioschyzon merolae: genetic evidence for nitrite reduction by a sulfite reductase-like enzyme. Plant Cell Phys 51:707–717

    Article  CAS  Google Scholar 

  • Imamura S, Kawase Y, Kobayashi I, Sone T, Era A, Miyagishima SY, Shimojima M, Ohta H, Tanaka K (2015) Target of rapamycin (TOR) plays a critical role in triacylglycerol accumulation in microalgae. Plant Mol Biol 89:309–318

    Article  CAS  PubMed  Google Scholar 

  • Imoto Y, Fujiwara T, Yoshida Y, Kuroiwa H, Maruyama S, Kuroiwa T (2010) Division of cell nuclei, mitochondria, plastids, and microbodies mediated by mitotic spindle poles in the primitive red alga Cyanidioschyzon merolae. Protoplasma 241:63–74

    Article  PubMed  Google Scholar 

  • Imoto Y, Yoshida Y, Yagisawa F, Kuroiwa H, Kuroiwa T (2011) The cell cycle, including the mitotic cycle and organelle division cycles, as revealed by cytological observations. J Elect Micro 60(suppl 1):S117–S136

    Google Scholar 

  • Imoto Y, Kuroiwa H, Ohnuma M, Kawano S, Kuroiwa T (2012) Identification of peroxisome-dividing ring in Cyanidioschyzon merolae based on organelle partner hypothesis. Cytologia 77:515–522

    Article  Google Scholar 

  • Imoto Y, Kuroiwa H, Yoshida Y, Ohnuma M, Fujiwara T, Yoshida M, Nishida K, Yagisawa F, Hirooka S, Miyagishima S et al (2013) Single-membrane–bounded peroxisome division revealed by isolation of dynamin-based machinery. Proc Nat Acad Sci 110:9583–9588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanesaki Y, Imamura S, Minoda A, Tanaka K (2012) External light conditions and internal cell cycle phases coordinate accumulation of chloroplast and mitochondrial transcripts in the red alga Cyanidioschyzon merolae. DNA Res 19:289–303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi T, Takahara M, Miyagishima SY, Kuroiwa H, Sasaki N, Ohta N, Matsuzaki M, Kuroiwa T (2002) Detection and localization of a chloroplast-encoded HU-like protein that organizes chloroplast nucleoids. Plant Cell 14:1579–1589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi Y, Kanesaki Y, Tanaka A, Kuroiwa H, Kuroiwa T, Tanaka K (2009) Tetrapyrrole signal as a cell-cycle coordinator from organelle to nuclear DNA replication in plant cells. Proc Nat Acad Sci 106:803–807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi Y, Imamura S, Hanaoka M, Tanaka K (2011) A tetrapyrrole-regulated ubiquitin ligase controls algal nuclear DNA replication. Nat Cell Biol 13:483–487

    Article  CAS  PubMed  Google Scholar 

  • 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 20:344–354

    Article  Google Scholar 

  • Kuroiwa T, Suzuki K, Kuroiwa H (1993) Mitochondrial division by an electron-dense ring in Cyanidioschyzon merolae. Protoplasma 175:173–177

    Article  Google Scholar 

  • Kuroiwa T, Kawazu T, Takahashi H, Suzuki K, Ohta N, Kuroiwa H (1994) Comparison of ultrastructures between the ultra-small eukaryote Cyanidioschyzon merolae and Cyanidium caldarium. 341. Cytologia 59:149–158

    Article  Google Scholar 

  • Kuroiwa T, Misumi O, Nishida K, Yagisawa F, Yoshida Y, Fujiwara T, Kuroiwa H (2008) Vesicle, mitochondrial, and plastid division machineries with emphasis on dynamin and electron-dense rings. Int Rev Cell Mol Biol 271:97–152

    Article  CAS  PubMed  Google Scholar 

  • Kuroiwa T, Ohnuma M, Imoto Y, Misumi O, Fujiwara T, Miyagishima SY, Sumiya N, Kuroiwa H (2012) Lipid droplets of bacteria, algae and fungi and a relationship between their contents and genome sizes as revealed by BODIPY and DAPI staining. Cytologia 77:289–299

    Article  Google Scholar 

  • Maruyama S, Kuroiwa H, Miyagishima SY, Tanaka K, Kuroiwa T (2007) Centromere dynamics in the primitive red alga Cyanidioschyzon merolae. The Plant J 49:1122–1129

    Article  CAS  PubMed  Google Scholar 

  • Matsuzaki M, Misumi O, Shin-i T, Maruyama S, Takahara M, Miyagishima SY, Mori T, Nishida K, Yagisawa F, Nishida K et al (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657

    Article  CAS  PubMed  Google Scholar 

  • Minoda A, Sakagami R, Yagisawa F, Kuroiwa T, Tanaka K (2004) Improvement of culture conditions and evidence for nuclear transformation by homologous recombination in a red alga, Cyanidioschyzon merolae 10D. Plant Cell Phys 45:667–671

    Article  CAS  Google Scholar 

  • Misumi O, Sakajiri T, Hirooka S, Kuroiwa H, Kuroiwa T (2008) Cytological studies of metal ion tolerance in the red algae Cyanidioschyzon merolae. Cytologia 73:437–443

    Article  CAS  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 M, Itoh R, Toda K, Takahashi H, Kuroiwa H, Kuroiwa T (1998) Visualization of the microbody division in Cyanidioschyzon merolae with the fluorochrome brilliant sulfoflavin. Protoplasma 201:115–119

    Article  Google Scholar 

  • Miyagishima SY, Itoh R, Aita S, Kuroiwa H, Kuroiwa T (1999a) Isolation of dividing chloroplasts with intact plastid-dividing rings from a synchronous culture of the unicellular red alga Cyanidioschyzon merolae. Planta 209:371–375

    Article  CAS  PubMed  Google Scholar 

  • Miyagishima SY, Itoh R, Toda K, Kuroiwa H, Kuroiwa T (1999b) Real-time analyses of chloroplast and mitochondrial division and differences in the behavior of their dividing rings during contraction. Planta 207:343–353

    Article  CAS  Google Scholar 

  • Miyagishima SY, Itoh R, Toda K, Kuroiwa H, Nishimura M, Kuroiwa T (1999c) Microbody proliferation and segregation cycle in the single-microbody alga Cyanidioschyzon merolae. Planta 208:326–336

    Article  CAS  Google Scholar 

  • Miyagishima SY, Kuroiwa H, Kuroiwa T (2001a) The timing and manner of disassembly of the apparatuses for chloroplast and mitochondrial division in the red alga Cyanidioschyzon merolae. Planta 212:517–528

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyagishima SY, Fujiwara T, Sumiya N, Hirooka S, Nakano A, Kabeya Y, Nakamura M (2014) Translation-independent circadian control of the cell cycle in a unicellular photosynthetic eukaryote. Nat Commun 5

    Google Scholar 

  • Mori N, Moriyama T, Toyoshima M, Sato N (2016) Construction of global acyl lipid metabolic map by comparative genomics and subcellular localization analysis in the red alga Cyanidioschyzon merolae. Front Plant Sci 7

    Google Scholar 

  • Moriyama T, Sakurai K, Sekine K, Sato N (2014) Subcellular distribution of central carbohydrate metabolism pathways in the red alga Cyanidioschyzon merolae. Planta 240:585–598

    Article  CAS  PubMed  Google Scholar 

  • Nishida K, Takahara M, Miyagishima S-y, Kuroiwa H, Matsuzaki M, Kuroiwa T (2003) Dynamic recruitment of dynamin for final mitochondrial severance in a primitive red alga. Proc Nat Acad Sci 100(4):2146–2151

    Google Scholar 

  • Nishida K, Yagisawa F, Kuroiwa H, Nagata T, Kuroiwa T (2005) Cell cycle-regulated, microtubule-independent organelle division in Cyanidioschyzon merolae. Mol Biol Cell 16:2493–2502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nozaki H, Takano H, Misumi O, Terasawa K, Matsuzaki M, Maruyama S, Nishida K, Yagisawa F, Yoshida Y, Fujiwara T et al (2007) A 100%-complete sequence reveals unusually simple genomic features in the hot-spring red alga Cyanidioschyzon merolae. BMC Biol 5(1)

    Google Scholar 

  • Ohnuma M, Yokoyama T, Inouye T, Sekine Y, Tanaka K (2008) Polyethylene glycol (PEG)-mediated transient gene expression in a red alga, Cyanidioschyzon merolae 10D. Plant Cell Phys 49:117–120

    Article  CAS  Google Scholar 

  • Ohta N, Sato N, Kuroiwa T (1998) Structure and organization of the mitochondrial genome of the unicellular red alga Cyanidioschyzon merolae deduced from the complete nucleotide sequence. Nuc Acids Res 26:5190–5198

    Article  CAS  Google Scholar 

  • Ohta N, Matsuzaki M, Misumi O, Miyagishima SY, Nozaki H, Tanaka K, Shin-I T, Kohara Y, Kuroiwa T (2003) Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res, 10: 67–77

    Google Scholar 

  • Sakajiri T, Asano K, Hirooka S, Ohnuma M, Misumi O, Yoshida M, Fujiwara T, Doi H, Kuroiwa T (2010) The overexpression of Cyanidioschyzon merolae S-adenosylmethionine Synthetase enhances salt tolerance in transgenic Arabidopsis thaliana. Cytologia 75:341–352

    Article  CAS  Google Scholar 

  • Sumiya N, Fujiwara T, Kobayashi Y, Misumi O, Miyagishima SY (2014) Development of a heat-shock inducible gene expression system in the red alga Cyanidioschyzon merolae. PLoS One 9:e111261

    Article  PubMed  PubMed Central  Google Scholar 

  • Sumiya N, Kawase Y, Hayakawa J, Matsuda M, Nakamura M, Era A, Tanaka K, Kondo A, Hasunuma T et al (2015) Expression of cyanobacterial acyl-ACP reductase elevates the triacylglycerol level in the red alga Cyanidioschyzon merolae. Plant Cell Phys 56:1962–1980

    Article  CAS  Google Scholar 

  • Sumiya N, Fujiwara T, Era A, Miyagishima SY (2016) Chloroplast division checkpoint in eukaryotic algae. Proc Nat Acad Sci 113:E7629–E7638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki K, Ehara T, Osafune T, Kuroiwa H, Kawano S, Kuroiwa T (1994) Behavior of mitochondria, chloroplasts and their nuclei during the mitotic cycle in the ultramicroalga Cyanidioschyzon merolae. Eur J Cell Biol 63:280–288

    CAS  PubMed  Google Scholar 

  • Takahara M, Kuroiwa H, Miyagishima SY, Mori T, Kuroiwa T (2001) Localization of the mitochondrial FtsZ protein in a dividing mitochondrion. Cytologia 66:421–425

    Article  Google Scholar 

  • Takayama Y, Inui Y, Sekiguchi Y, Kobayashi A, Oroguchi T, Yamamoto M, Matsunaga S, Nakasako M (2015) Coherent X-ray diffraction imaging of chloroplasts from Cyanidioschyzon merolae by using X-ray free electron laser. Plant Cell Phys 56:1272–1286

    Article  CAS  Google Scholar 

  • Yagisawa F, Nishida K, Kuroiwa H, Nagata T, Kuroiwa T (2007) Identification and mitotic partitioning strategies of vacuoles in the unicellular red alga Cyanidioschyzon merolae. Planta 226:1017–1029

    Article  CAS  PubMed  Google Scholar 

  • Yagisawa F, Nishida K, Yoshida M, Ohnuma M, Shimada T, Fujiwara T, Yoshida Y, Misumi O, Kuroiwa H, Kuroiwa T (2009) Identification of novel proteins in isolated polyphosphate vacuoles in the primitive red alga Cyanidioschyzon merolae. The Plant J 60:882–893

    Article  CAS  PubMed  Google Scholar 

  • Yagisawa F, Fujiwara T, Kuroiwa H, Nishida K, Imoto Y, Kuroiwa T (2012) Mitotic inheritance of endoplasmic reticulum in the primitive red alga Cyanidioschyzon merolae. Protoplasma 249:1129–1135

    Article  CAS  PubMed  Google Scholar 

  • Yagisawa F, Fujiwara T, Ohnuma M, Kuroiwa H, Nishida K, Imoto Y, Yoshida Y, Kuroiwa T (2013) Golgi inheritance in the primitive red alga, Cyanidioschyzon merolae. Protoplasma 250:943–948

    Article  PubMed  Google Scholar 

  • Yoshida Y, Kuroiwa H, Misumi O, Nishida K, Yagisawa F, Fujiwara T, Nanamiya H, Kawamura F, Kuroiwa T (2006) Isolated chloroplast division machinery can actively constrict after stretching. Science 313:1435–1438

    Article  CAS  PubMed  Google Scholar 

  • Yoshida Y, Kuroiwa H, Hirooka S, Fujiwara T, Ohnuma M, Yoshida M, Misumi O, Kawano S, Kuroiwa T (2009) The bacterial ZapA-like protein ZED is required for mitochondrial division. Curr Biol 19:1491–1497

    Article  CAS  PubMed  Google Scholar 

  • Yoshida Y, Kuroiwa H, Misumi O, Yoshida M, Ohnuma M, Fujiwara T, Yagisawa F, Hirooka S, Imoto Y, Matsuhita K, Kawano S, Kuroiwa T (2010) Chloroplasts divide by contraction of a bundle of nanofilaments consisting of polyglucan. Science 329:949–953

    Article  CAS  PubMed  Google Scholar 

  • Yoshida M, Yoshida Y, Fujiwara T, Misumi O, Kuroiwa H, Kuroiwa T (2011) Proteomic comparison between interphase and metaphase of isolated chloroplasts of Cyanidioschyzon merolae (Cyanidiophyceae, Rhodophyta). Phycol Res 59:1–15

    Article  CAS  Google Scholar 

  • Yoshida Y, Miyagishima SY, Kuroiwa H, Kuroiwa T (2012) The plastid-dividing machinery: formation, constriction and fission. Curr Opi Pant Biol 15:714–721

    Article  CAS  Google Scholar 

  • Yoshida Y, Fujiwara T, Imoto Y, Yoshida M, Ohnuma M, Hirooka S, Misumi O, Kuroiwa H, Kuroiwa T (2013) The kinesin-like protein TOP promotes aurora localisation and induces mitochondrial, chloroplast and nuclear division. J Cell Sci 126:2392–2400

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Organelle Homeostasis, Medical Institute of Bioregulation, Kyushu University, 3-1-1 Maidashi, Higashiku, Fukuoka, 812-0053, Japan

    Yuuta Imoto

  2. Laboratory for Single Cell Gene Dynamics, Quantitative Biology Center, RIKEN, Furuedai, Suita, Osaka, 565-0874, Japan

    Yamato Yoshida

Authors
  1. Yuuta Imoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yamato Yoshida
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuuta Imoto .

Editor information

Editors and Affiliations

  1. Faculty of Science Department of Chemical and Biological Sciences, Japan Women’s University, Tokyo, Japan

    Tsuneyoshi Kuroiwa

  2. Department of Cell Genetics, National Institute of Genetics, Shizuoka, Japan

    Shinya Miyagishima

  3. Department of Applied Biological Science, Faculty of Science and Technology, Tokyo University of Science, Chiba, Japan

    Sachihiro Matsunaga

  4. Department of Life Sciences Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, Japan

    Naoki Sato

  5. Department of Biological Sciences Graduate School of Science, University of Tokyo, Tokyo, Japan

    Hisayoshi Nozaki

  6. Laboratory for Chemistry and Life Science Institute of Innovative Research, Tokyo Institute of Technology, Kanagawa, Japan

    Kan Tanaka

  7. Graduate School of Science and Technology for Innovation Faculty of Science, Department of Biological Science and Chemistry, Yamaguchi University, Yamaguchi, Japan

    Osami Misumi

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Imoto, Y., Yoshida, Y. (2017). Cellular Structure of Cyanidioschyzon merolae: A Minimum Set of Organelles. In: Kuroiwa, T., et al. Cyanidioschyzon merolae. Springer, Singapore. https://doi.org/10.1007/978-981-10-6101-1_2

Download citation

Publish with us

Policies and ethics

Search

Navigation