Expression of the Nucleus-Encoded Chloroplast Division Genes and Proteins Regulated by the Algal Cell Cycle

Expression of the Nucleus-Encoded Chloroplast Division Genes and Proteins Regulated by the Algal Cell Cycle
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DOI:
10.1093/molbev/mss102
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发表时间:
2012-10-01
影响因子:
10.7
通讯作者:
Kabeya, Yukihiro
Kabeya, Yukihiro
中科院分区:
生物学1区
文献类型:
--
作者:
Miyagishima, Shin-ya;Suzuki, Kenji;Kabeya, Yukihiro

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叶绿体是由蓝藻内共生体进化而来的,它们的连续性通过叶绿体分裂来维持,叶绿体分裂是通过在分裂部位收缩环状分裂复合体来实现的。人们认为,内共生和宿主细胞分裂事件的同步是建立持久的内共生关系的关键步骤,例如在现有藻类中常见的内共生关系。在大多数藻类中,叶绿体在寄主细胞分裂周期的特定时期分裂一次。为了了解藻类细胞叶绿体分裂的时间规律和系统是如何进化的,我们研究了含有蓝藻初级内共生来源的叶绿体(绿藻、红藻、绿藻和链藻)的藻类细胞周期中叶绿体分裂基因和蛋白质的表达。结果表明,蓝藻和真核寄主的核编码叶绿体分裂基因和蛋白,除FtsZ外,均在S期特异表达。在这种蓝藻中,FtsZ在整个细胞周期中持续表达,而核编码的Mind和Mine的表达以及FtsZ环的形成受细胞周期各阶段的调控。与核编码的分裂基因相比,叶绿体编码的分裂基因的表达不受宿主细胞周期的调控。Mine和Mind的内生基因从叶绿体到核基因组的转移在不同的谱系中多次独立发生,而核编码的Mind和Mind的表达受本研究所研究的所有谱系中细胞周期的调节。这些结果表明,藻类细胞周期中叶绿体分裂的时机受到细胞周期调控的部分而非全部叶绿体分裂基因表达的制约。此外,研究还表明,内生共生基因转移后不久,每个分裂相关基因的调控就建立起来了,并且这一事件在不同的基因和不同的谱系中独立发生了多次。
Chloroplasts have evolved from a cyanobacterial endosymbiont and their continuity has been maintained by chloroplast division, which is performed by the constriction of a ring-like division complex at the division site. It is believed that the synchronization of the endosymbiotic and host cell division events was a critical step in establishing a permanent endosymbiotic relationship, such as is commonly seen in existing algae. In the majority of algal species, chloroplasts divide once per specific period of the host cell division cycle. In order to understand both the regulation of the timing of chloroplast division in algal cells and how the system evolved, we examined the expression of chloroplast division genes and proteins in the cell cycle of algae containing chloroplasts of cyanobacterial primary endosymbiotic origin (glaucophyte, red, green, and streptophyte algae). The results show that the nucleus-encoded chloroplast division genes and proteins of both cyanobacterial and eukaryotic host origin are expressed specifically during the S phase, except for FtsZ in one graucophyte alga. In this glaucophyte alga, FtsZ is persistently expressed throughout the cell cycle, whereas the expression of the nucleus-encoded MinD and MinE as well as FtsZ ring formation are regulated by the phases of the cell cycle. In contrast to the nucleus-encoded division genes, it has been shown that the expression of chloroplast-encoded division genes is not regulated by the host cell cycle. The endosymbiotic gene transfer of minE and minD from the chloroplast to the nuclear genome occurred independently on multiple occasions in distinct lineages, whereas the expression of nucleus-encoded MIND and MINE is regulated by the cell cycle in all lineages examined in this study. These results suggest that the timing of chloroplast division in algal cell cycle is restricted by the cell cycle-regulated expression of some but not all of the chloroplast division genes. In addition, it is suggested that the regulation of each division-related gene was established shortly after the endosymbiotic gene transfer, and this event occurred multiple times independently in distinct genes and in distinct lineages.