More membranes, more proteins: complex protein import mechanisms into secondary plastids

Abstract

Plastids are found across the tree of life in a tremendous diversity of life forms. Surprisingly they are not limited to photosynthetic organisms but also found in numerous predators and parasites. An important reason for the pervasiveness of plastids has been their ability to move laterally and to jump from one branch of the tree of life to the next through secondary endosymbiosis. Eukaryotic algae have entered endosymbiotic relationships with other eukaryotes on multiple independent occasions. The descendants of these endosymbiotic events now carry complex plastids, organelles that are bound by three or even four membranes. As in all endosymbiotic organelles most of the symbiont's genes have been transferred to the host and their protein products have to be imported into the organelle. As four membranes might suggest, this is a complex process. The emerging mechanisms display a series of translocons that mirror the divergent ancestry of the membranes they cross. This review is written from the viewpoint of a parasite biologist and seeks to provide a brief overview of plastid evolution in particular for readers not already familiar with plant and algal biology and then focuses on recent molecular discoveries using genetically tractable Apicomplexa and diatoms.

Figure 1

(A) Diagramatic representation of the complex evolutionary process that gave rise to present day primary and secondary plastids. A cyanobacterium was engulfed by a heterotrophic eukaryote giving rise to the plastids of red and green algae (including land plants) and glaucophytes. In a second endosymbiotic event an alga was taken up by another eukaryote (note that this occurred multiple independent times). The resulting complex plastids are surrounded by four (and sometimes three) membranes. (B) Schematic tree of eukaryotic life highlighting the three major secondary endosymbiotic events that are thought to be responsible for present day complex plastids (*note that we excluded multiple events in dinoflagellates for simplicity). The relationships shown here are based on phylogenetic analyses summarized by Keeling and colleagues (Keeling et al. 2005). The ancestor of present day chromalveolates acquired their plastid through endosymbiotic uptake of a red alga. Diversification and adaptation to different ecological niches led to subsequent loss of photosynthesis (as in Apicomplexa) or loss of entire plastids (as in ciliates or oomycetes). Plastids of euglenids and chlorarachniophytes were acquired by two independent endosymbiotic events involving green algae.

Figure 2

(A) Schematic depiction of cellular morphology and the trafficking routes to the plastid for a selection of plastid containing organisms. Arrows indicate the path taken by nuclear/nucleomorph encoded proteins to reach their final destination in the plastid. (A, D) The green algae Chlorella and the red alga Cyanidioschyzon: nuclear encoded plastid proteins are synthesized in the cytosol and transported across the two plastid membrane with the help of Tic-Toc translocons. Engulfment of a red or green plastid by a heterotrophic eukaryote gave rise to organisms with multiple membrane bound secondary plastids. Secondary symbiosis gave rise to two main green lineages, chlorarachniophytes (B) euglenids (C). The main secondary red lineage has a common origin and includes cryptomonads (E), diatoms (F) and Apicomplexa (G). A remnant of the algal nucleus, the nucleomorph (Nm) resides between the second and third outermost compartments in chlorarachniophytes and cryptomonads (B , E). Note that in cryptomonads and diatoms the plastid resides within the endoplasmic reticulum (E, F). N, nucleus, G, Golgi, P, plastid, ER, endoplasmic reticulum. H. Schematic outline of a molecular model of the plastid protein import machinery based on results from Apicomplexa and diatoms. Note that not all elements have been experimentally validated (several such points are highlighted by a question mark). The pathway taken by apicomplexan proteins from the ER to the apicoplast remains highly speculative. Cargo proteins are shown as grey lines, proteins destined for degradation as dashed lines. Please refer to Table 1 for further detailed reference on specific proteins.