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Division of cell nuclei, mitochondria, plastids, and microbodies mediated by mitotic spindle poles in the primitive red alga Cyanidioschyzon merolae

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Abstract

To understand the cell cycle, we must understand not only mitotic division but also organelle division cycles. Plant and animal cells contain many organelles which divide randomly; therefore, it has been difficult to elucidate these organelle division cycles. We used the primitive red alga Cyanidioschyzon merolae, as it contains a single mitochondrion and plastid per cell, and organelle division can be highly synchronized by a light/dark cycle. We demonstrated that mitochondria and plastids multiplied by independent division cycles (organelle G1, S, G2 and M phases) and organelle division occurred before cell–nuclear division. Additionally, organelle division was found to be dependent on microtubules as well as cell–nuclear division. We have observed five stages of microtubule dynamics: (1) the microtubule disappears during the G1 phase; (2) α-tubulin is dispersed within the cytoplasm without forming microtubules during the S phase; (3) α-tubulin is assembled into spindle poles during the G2 phase; (4) polar microtubules are organized along the mitochondrion during prophase; and (5) mitotic spindles in cell nuclei are organized during the M phase. Microfluorometry demonstrated that the intensity peak of localization of α-tubulin changed in the order to spindle poles, mitochondria, spindle poles, and central spindle area, but total fluorescent intensity did not change remarkably throughout mitotic phases suggesting that division and separation of the cell nucleus and mitochondrion is mediated by spindle pole bodies. Inhibition of microtubule organization induced cell–nuclear division, mitochondria separation, and division of a single membrane-bound microbody, suggesting that similar to cell–nuclear division, mitochondrion separation and microbody division are dependent on microtubules.

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Abbreviations

VIMPCS:

Video-intensified microscope photon-counting system

DAPI:

4′,6-Diamidino-2-phenylindole

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Acknowledgments

This work was supported by grants from the Scientific Research on Priority Areas (no.19207004 to T.K.), the Frontier Project “Adaptation and Evolution of Extremophiles” from the Ministry of Education, Culture, Sports, Science and Technology of Japan, and by the program for the Promotion of Basic Search Activities for Innovative Biosciences (PROBRAIN, to T.K.). We have no financial relationship with the organization that sponsored this research.

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Authors and Affiliations

  1. Laboratory of Cell Biology, Department of Life Science, College of Science, Research Information Center for Extremophile, Rikkyo University, Toshima, Tokyo, 171-8501, Japan

    Yuuta Imoto, Takayuki Fujiwara, Yamato Yoshida, Haruko Kuroiwa & Tsuneyoshi Kuroiwa

  2. Institute of Molecular and Cellular Bioscience, University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo, 113-0032, Japan

    Shinichiro Maruyama

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  1. Yuuta Imoto
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  2. Takayuki Fujiwara
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  3. Yamato Yoshida
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  4. Haruko Kuroiwa
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  5. Shinichiro Maruyama
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  6. Tsuneyoshi Kuroiwa
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Correspondence to Tsuneyoshi Kuroiwa.

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Imoto, Y., Fujiwara, T., Yoshida, Y. et al. Division of cell nuclei, mitochondria, plastids, and microbodies mediated by mitotic spindle poles in the primitive red alga Cyanidioschyzon merolae . Protoplasma 241, 63–74 (2010). https://doi.org/10.1007/s00709-010-0107-y

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