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Review
. 2013 Feb;1833(2):341-51.
doi: 10.1016/j.bbamcr.2012.06.028. Epub 2012 Jun 28.

Intra-plastid protein trafficking: how plant cells adapted prokaryotic mechanisms to the eukaryotic condition

Jose M Celedon  1 , Kenneth Cline
Affiliations
Review

Intra-plastid protein trafficking: how plant cells adapted prokaryotic mechanisms to the eukaryotic condition

Jose M Celedon et al. Biochim Biophys Acta. 2013 Feb.

Abstract

Protein trafficking and localization in plastids involve a complex interplay between ancient (prokaryotic) and novel (eukaryotic) translocases and targeting machineries. During evolution, ancient systems acquired new functions and novel translocation machineries were developed to facilitate the correct localization of nuclear encoded proteins targeted to the chloroplast. Because of its post-translational nature, targeting and integration of membrane proteins posed the biggest challenge to the organelle to avoid aggregation in the aqueous compartments. Soluble proteins faced a different kind of problem since some had to be transported across three membranes to reach their destination. Early studies suggested that chloroplasts addressed these issues by adapting ancient-prokaryotic machineries and integrating them with novel-eukaryotic systems, a process called 'conservative sorting'. In the last decade, detailed biochemical, genetic, and structural studies have unraveled the mechanisms of protein targeting and localization in chloroplasts, suggesting a highly integrated scheme where ancient and novel systems collaborate at different stages of the process. In this review we focus on the differences and similarities between chloroplast ancestral translocases and their prokaryotic relatives to highlight known modifications that adapted them to the eukaryotic situation. This article is part of a Special Issue entitled: Protein Import and Quality Control in Mitochondria and Plastids.

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Figures

Figure 1
Figure 1. Trafficking pathways of chloroplast proteins
Most plastid proteins are encoded on nuclear genes and synthesized in the cytosol as precursor proteins with N-terminal transit peptides that govern import through the Toc and Tic translocases into the stroma and are removed by a stromal processing protease. Thylakoid lumen-resident proteins and some thylakoid membrane proteins are targeted by hydrophobic signal peptides that are removed by a lumen-facing signal peptidase following translocation. Multispanning membrane proteins are targeted by uncleaved hydrophobic transmembrane domains (TMD). The ancestral (conserved from the endosymbiont) thylakoid translocases are the cpSRP/Alb3, cpTat, and cpSecA1/cpSecY1E1. A second recently described and divergent Sec translocase, cpSecA2/cpSecY2E2 is located in the plastid envelope. For presentation purposes, the cp prefix is not shown. A relatively small number of plastid proteins are encoded on plastid genes and many of these are co-translationally integrated into the thylakoid membrane and assembled into photosynthetic complexes. An hypothesized, but experimentally supported, membrane flow from the inner envelope membrane to the thylakoids (see section 3.3) may be involved in thylakoid biogenesis. In this and subsequent figures, translocases conserved from the endosymbiont are colored orange and those invented in eukaryotes or not conserved colored blue.
Figure 2
Figure 2. Comparison of the post-translational Sec pathways in the thylakoids and the prokaryote E.coli.
The basic translocase consists of an hourglass shaped channel made up of SecY and SecE. Polypeptides traverse the Sec channel in an unfolded conformation. The SecA ATPase functions as a reciprocating translocation motor to feed polypeptide substrates through the channel. The E. coli Sec channel also contains the non-essential component SecG. E. coli also contains an additional non-essential complex called SecDFyajC, which seems to mediate the involvement of the protonmotive force in translocation, and a chaperone called SecB that maintains the precursor protein in transport competent conformation. The additional components are not conserved among prokaryotes.
Figure 3
Figure 3. Steps of the Twin arginine translocation (Tat) pathway in thylakoid membranes of plant chloroplasts
(A) Steps for binding, Tha4assembly, and translocation. The three components of the cpTat system, cpTatC, Hcf106, and Tha4, are organized in two complexes in the membrane. cpTatC and Hcf106 form a receptor complex that binds the twin arginine signal peptide. cpTatC binds the RR motif of the signal peptide through its N-terminus and first stromal loop. Hcf106 also makes contact with the signal peptide. For purposes of illustration only one receptor unit is shown with one cpTatC (in blue and depicted with its six TMDs) and one Hcf106 (in yellow). The signal peptide and the proton gradient trigger assembly of Tha4 (in orange), which may polymerize to form a transport active homo-oligomer. Functional analysis indicates that a Tha4 oligomer of ~26 protomers is required for transport of the OE17 precursor protein. The precursor is translocated by still an unknown mechanism and the signal peptide cleaved by the lumen-facing signal peptidase (scissors). After precursor protein translocation, Tha4 dissociates into, apparently, tetramers. (B) The characterized receptor complex may contain eight cpTatC-Hcf106 heterodimers (depicted here as blue cylinders that each represent cpTatC-Hcf106 hetero-dimer). Binding stoichiometry studies suggest that a fully saturated receptor complex contains ~ eight precursor proteins. In addition, when Tha4 is in sufficient abundance, all precursor bound sites are independently activated for transport. This suggests that a fully saturated and Tha4 assembled cpTat translocase would be > 2 megadaltons.
Figure 3
Figure 3. Steps of the Twin arginine translocation (Tat) pathway in thylakoid membranes of plant chloroplasts
(A) Steps for binding, Tha4assembly, and translocation. The three components of the cpTat system, cpTatC, Hcf106, and Tha4, are organized in two complexes in the membrane. cpTatC and Hcf106 form a receptor complex that binds the twin arginine signal peptide. cpTatC binds the RR motif of the signal peptide through its N-terminus and first stromal loop. Hcf106 also makes contact with the signal peptide. For purposes of illustration only one receptor unit is shown with one cpTatC (in blue and depicted with its six TMDs) and one Hcf106 (in yellow). The signal peptide and the proton gradient trigger assembly of Tha4 (in orange), which may polymerize to form a transport active homo-oligomer. Functional analysis indicates that a Tha4 oligomer of ~26 protomers is required for transport of the OE17 precursor protein. The precursor is translocated by still an unknown mechanism and the signal peptide cleaved by the lumen-facing signal peptidase (scissors). After precursor protein translocation, Tha4 dissociates into, apparently, tetramers. (B) The characterized receptor complex may contain eight cpTatC-Hcf106 heterodimers (depicted here as blue cylinders that each represent cpTatC-Hcf106 hetero-dimer). Binding stoichiometry studies suggest that a fully saturated receptor complex contains ~ eight precursor proteins. In addition, when Tha4 is in sufficient abundance, all precursor bound sites are independently activated for transport. This suggests that a fully saturated and Tha4 assembled cpTat translocase would be > 2 megadaltons.
Figure 4
Figure 4. The chloroplast post-translational Signal Recognition Particle (cpSRP) pathway and its comparison to the E. coli co-translational SRP pathways
(A) The cpSRP system is the best example of a modification that adapts the prokaryotic machinery to the eukaryotic situation. The cpSRP system lacks the nearly ubiquitous RNA moiety of SRPs (colored blue in Fig 4-B) but contains a novel cpSRP43 protein. Combined activities of both proteins allow the chloroplast system to bind imported LHC proteins and maintain them soluble and integration competent. cpSRP54 binds hydrophobic domains as do other SRP54 proteins. However, cpSRP43 appears to be responsible for the novel post-translational mode of action; it binds a novel hydrophilic motif that is found only on LHC antenna proteins; it maintains LHCP in a dis-aggregated state, and it targets the cpSRP-LHCP to the integrase Alb3 via the Alb3 C-terminus (colored red). (B) The E. coli SRP has been shown to co-translationally target to several different translocase and integrase configurations. It remains to be determined if such versatility is characteristic of cpSRP.
Figure 5
Figure 5. Speculative model for integration of multispanning membrane proteins by cpSecA2/cpSecY2E2 during the protein import by the Toc and Tic system
Precursor proteins directed to the chloroplast are imported across the outer and inner envelope by the Toc-Tic translocases. In a speculative model, Toc-Tic could work together with the cpSec2 system to perform a ‘pseudo’ co-translational integration of membrane proteins. This model is based on the observation that Tic40 begins integration during import across Toc-Tic (see section 3.3).
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