期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2016
卷号：113
期号：47
页码：E7629-E7638
DOI：10.1073/pnas.1612872113
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：SignificanceChloroplasts arose from a cyanobacterial endosymbiont, which introduced photosynthesis into eukaryotes. It is widely believed that synchronization of division in the eukaryotic host cell and in the endosymbiont was critical for the host cell to maintain the endosymbiont/chloroplast permanently. However, it is unclear how the division of the endosymbiont (the chloroplast) and host cell became synchronized. Using the unicellular red alga Cyanidioschyzon merolae, we show that the host cell enters into the metaphase only when chloroplast division has commenced. A similar phenomenon also was observed in the glaucophyte alga Cyanophora paradoxa. It thus seems likely that the acquisition of the cell-cycle checkpoint of chloroplast division played an important role in the establishment of the chloroplast in ancient algae. 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 chloroplast-division machinery by the overexpression of Filamenting temperature-sensitive (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.
