Sommer Maik S, Gould Sven B, Lehmann Petra, Gruber Ansgar, Przyborski Jude M, Maier Uwe-G
Laboratory for Cell Biology, Philipps-University of Marburg, Marburg, Germany.
Mol Biol Evol. 2007 Apr;24(4):918-28. doi: 10.1093/molbev/msm008. Epub 2007 Jan 22.
Phototrophic chromalveolates possess plastids surrounded by either 3 or 4 membranes, revealing their secondary endosymbiotic origin from an engulfed eukaryotic alga. In cryptophytes, a member of the chromalveolates, the organelle is embedded within a designated region of the host's rough endoplasmic reticulum (RER). Its eukaryotic compartments other than the plastid were reduced to the mere remains of its former cytosol, the periplastid compartment (PPC, PP space), and its nucleus, the nucleomorph, separated from the RER by its former plasma membrane, the periplast membrane (PPM). In the nucleomorph genome of the cryptophyte Guillardia theta, we identified several genes sharing homology with components of the ER-associated degradation (ERAD) machinery of yeast and higher eukaryotes, namely ORF201 and ORF477, homologs of membrane-bound proteins, Der1p (Degradation in the ER protein 1) and the RING-finger ubiquitin ligase Hrd1, and a truncated version of Udf1, a cofactor of Cdc48, a lumenal ATPase. Exemplarily, studies on the Der1-homolog ORF201 showed that this protein partially rescued a yeast deletion mutant, indicating the existence of a functional PPC-specific ERAD-like system in cryptophytes. With the noninvestigated exception of haptophytes a phylogenetically and mechanistically related system is apparently present in all chromalveolates with 4 membrane-bound plastids because amongst others, PPC-specific Derlins (Der1-like proteins), CDC48 and its cofactor Ufd1 were identified in the nuclear genomes of diatoms and apicomplexa. These proteins are equipped with the required topogenic signals to direct them into the periplastid compartment of their secondary symbionts. Based on our findings, we suggest that all chromalveolates with 4 membrane-bound plastids express an ERAD-derived machinery in the PPM of their secondary plastid, coexisting physically and systematically adjacent to the host's own ERAD system. We propose herewith that this system was functionally adapted to mediate transport of nucleus-encoded PPC/plastid preproteins from the RER into the periplastid space.
光合色素泡虫类具有由3层或4层膜包围的质体，这揭示了它们源自被吞噬的真核藻类的次生内共生起源。在色素泡虫类的成员隐藻中，该细胞器嵌入宿主糙面内质网（RER）的特定区域内。除质体外，其真核区室已缩减为其前胞质溶胶的残余部分，即周质体区室（PPC，PP空间），以及其细胞核，即核质体，它通过其前质膜，即周质膜（PPM）与RER分隔开。在隐藻Guillardia theta的核质体基因组中，我们鉴定出了几个与酵母和高等真核生物的内质网相关降解（ERAD）机制的组分具有同源性的基因，即ORF201和ORF477，它们是膜结合蛋白Der1p（内质网降解蛋白1）和环状泛素连接酶Hrd1的同源物，以及Udf1的截短版本，Udf1是腔ATP酶Cdc48的辅助因子。例如，对Der1同源物ORF201的研究表明，该蛋白部分挽救了酵母缺失突变体，这表明隐藻中存在功能性的PPC特异性ERAD样系统。除了未研究的定鞭藻外，在所有具有4个膜结合质体的色素泡虫类中显然都存在一个在系统发育和机制上相关的系统，因为除其他外，在硅藻和顶复门的核基因组中鉴定出了PPC特异性Derlins（Der1样蛋白）、CDC48及其辅助因子Ufd1。这些蛋白配备了所需的拓扑信号，以将它们引导至其次生共生体的周质体区室。基于我们的发现，我们认为所有具有4个膜结合质体的色素泡虫类在其次生质体的PPM中表达一种源自ERAD的机制，在物理和系统上与宿主自身的ERAD系统相邻共存。我们在此提出，该系统在功能上经过调整，以介导核编码的PPC/质体前体蛋白从RER转运到周质体空间。
