Chloroplast division checkpoint in eukaryotic algae

Nobuko Sumiya, Takayuki Fujiwara, Atsuko Era, Shin Ya Miyagishima

Research output: Contribution to journalArticle

19 Citations (Scopus)

Abstract

Chloroplasts evolved from a cyanobacterial endosymbiont. It is believed that the synchronization of endosymbiotic and host cell division, as is commonly seen in existing algae, was a critical step in establishing the permanent organelle. Algal cells typically contain one or only a small number of chloroplasts that divide once per host cell cycle. This division is based partly on the S-phase-specific expression of nucleus-encoded proteins that constitute the chloroplast-division machinery. In this study, using the red alga Cyanidioschyzon merolae, we show that cell-cycle progression is arrested at the prophase when chloroplast division is blocked before the formation of the chloroplastdivision machinery by the overexpression of Filamenting temperaturesensitive (Fts) Z2-1 (Fts72-1), but the cell cycle progresses when chloroplast division is blocked during division-site constriction by the overexpression of either FtsZ2-1 or a dominant-negative form of dynamin-related protein 5B (DRP5B). In the cells arrested in the prophase, the increase in the cyclin B level and the migration of cyclin-dependent kinase B (CDKB) were blocked. These results suggest that chloroplast division restricts host cell-cycle progression so that the cell cycle progresses to the metaphase only when chloroplast division has commenced. Thus, chloroplast division and host cell-cycle progression are synchronized by an interactive restriction that takes place between the nucleus and the chloroplast. In addition, we observed a similar pattern of cell-cycle arrest upon the blockage of chloroplast division in the glaucophyte alga Cyanophora paradoxa, raising the possibility that the chloroplast division checkpoint contributed to the establishment of the permanent organelle.

Original languageEnglish
Pages (from-to)E7629-E7638
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number47
DOIs
Publication statusPublished - 2016 Nov 22
Externally publishedYes

Fingerprint

Chloroplasts
Cell Cycle
Prophase
Organelles
Cyanophora
Chloroplast Proteins
Dynamins
Cyclin B
Rhodophyta
Cyclin-Dependent Kinases
Metaphase
Cell Cycle Checkpoints
S Phase
Constriction
Cell Division

Keywords

  • Algal cell cycle
  • Chloroplast division
  • Cyanidioschyzon merolae
  • Cyanophora paradoxa

ASJC Scopus subject areas

  • General

Cite this

Chloroplast division checkpoint in eukaryotic algae. / Sumiya, Nobuko; Fujiwara, Takayuki; Era, Atsuko; Miyagishima, Shin Ya.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, No. 47, 22.11.2016, p. E7629-E7638.

Research output: Contribution to journalArticle

Sumiya, Nobuko ; Fujiwara, Takayuki ; Era, Atsuko ; Miyagishima, Shin Ya. / Chloroplast division checkpoint in eukaryotic algae. In: Proceedings of the National Academy of Sciences of the United States of America. 2016 ; Vol. 113, No. 47. pp. E7629-E7638.
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