Department of Genomics, Faculty of Biotechnology, University of Wrocław, ul. Przybyszewskiego 63/77, Wrocław 51-148, Poland.
Biol Direct. 2013 Jul 11;8:18. doi: 10.1186/1745-6150-8-18.
It is commonly assumed that a heterotrophic ancestor of the supergroup Archaeplastida/Plantae engulfed a cyanobacterium that was transformed into a primary plastid; however, it is still unclear how nuclear-encoded proteins initially were imported into the new organelle. Most proteins targeted to primary plastids carry a transit peptide and are transported post-translationally using Toc and Tic translocons. There are, however, several proteins with N-terminal signal peptides that are directed to higher plant plastids in vesicles derived from the endomembrane system (ES). The existence of these proteins inspired a hypothesis that all nuclear-encoded, plastid-targeted proteins initially carried signal peptides and were targeted to the ancestral primary plastid via the host ES.
We present the first phylogenetic analyses of Arabidopsis thaliana α-carbonic anhydrase (CAH1), Oryza sativa nucleotide pyrophosphatase/phosphodiesterase (NPP1), and two O. sativa α-amylases (αAmy3, αAmy7), proteins that are directed to higher plant primary plastids via the ES. We also investigated protein disulfide isomerase (RB60) from the green alga Chlamydomonas reinhardtii because of its peculiar dual post- and co-translational targeting to both the plastid and ES. Our analyses show that these proteins all are of eukaryotic rather than cyanobacterial origin, and that their non-plastid homologs are equipped with signal peptides responsible for co-translational import into the host ES. Our results indicate that vesicular trafficking of proteins to primary plastids evolved long after the cyanobacterial endosymbiosis (possibly only in higher plants) to permit their glycosylation and/or transport to more than one cellular compartment.
The proteins we analyzed are not relics of ES-mediated protein targeting to the ancestral primary plastid. Available data indicate that Toc- and Tic-based translocation dominated protein import into primary plastids from the beginning. Only a handful of host proteins, which already were targeted through the ES, later were adapted to reach the plastid via the vesicular trafficking. They represent a derived class of higher plant plastid-targeted proteins with an unusual evolutionary history.
人们普遍认为，超组古菌/植物的异养祖先吞噬了一个被转化为原始质体的蓝细菌；然而，核编码蛋白最初是如何被导入新细胞器的仍不清楚。大多数靶向原始质体的蛋白质都带有转运肽，并通过Toc 和 Tic 转运体进行翻译后转运。然而，有几个具有 N 端信号肽的蛋白质被定向到来自内膜系统（ES）的小泡中的高等植物质体。这些蛋白质的存在激发了一个假说，即所有核编码的、靶向质体的蛋白质最初都带有信号肽，并通过宿主 ES 靶向到原始的初级质体。
我们首次对拟南芥 α-碳酸酐酶（CAH1）、水稻核苷酸焦磷酸酶/磷酸二酯酶（NPP1）和两个水稻 α-淀粉酶（αAmy3、αAmy7）进行了系统发育分析，这些蛋白质通过 ES 被定向到高等植物的初级质体。我们还研究了绿藻莱茵衣藻的蛋白质二硫键异构酶（RB60），因为它具有奇特的双重翻译后和共翻译靶向到质体和 ES 的特性。我们的分析表明，这些蛋白质都具有真核生物而不是蓝细菌的起源，并且它们的非质体同源物都带有信号肽，负责共翻译导入宿主 ES。我们的结果表明，质体蛋白的囊泡运输是在蓝细菌内共生之后很久才进化而来的（可能只在高等植物中），以允许它们的糖基化和/或运输到不止一个细胞区室。
我们分析的蛋白质不是 ES 介导的靶向原始初级质体的蛋白质的遗迹。现有数据表明，Toc 和 Tic 为基础的转运从一开始就主导了蛋白质向初级质体的输入。只有少数已经通过 ES 靶向的宿主蛋白后来被适应通过囊泡运输到达质体。它们代表了一类具有不寻常进化历史的高等植物质体靶向蛋白的衍生类。
