The Metabolite Transporters of the Plastid Envelope: An Update

Abstract

The engulfment of a photoautotrophic cyanobacterium by a primitive mitochondria-bearing eukaryote traces back to more than 1.2 billion years ago. This single endosymbiotic event not only provided the early petroalgae with the metabolic capacity to perform oxygenic photosynthesis, but also introduced a plethora of other metabolic routes ranging from fatty acids and amino acids biosynthesis, nitrogen and sulfur assimilation to secondary compounds synthesis. This implicated the integration and coordination of the newly acquired metabolic entity with the host metabolism. The interface between the host cytosol and the plastidic stroma became of crucial importance in sorting precursors and products between the plastid and other cellular compartments. The plastid envelope membranes fulfill different tasks: they perform important metabolic functions, as they are involved in the synthesis of carotenoids, chlorophylls, and galactolipids. In addition, since most genes of cyanobacterial origin have been transferred to the nucleus, plastidial proteins encoded by nuclear genes are post-translationally transported across the envelopes through the TIC–TOC import machinery. Most importantly, chloroplasts supply the photoautotrophic cell with photosynthates in form of reduced carbon. The innermost bilayer of the plastidic envelope represents the permeability barrier for the metabolites involved in the carbon cycle and is literally stuffed with transporter proteins facilitating their transfer. The intracellular metabolite transporters consist of polytopic proteins containing membrane spans usually in the number of four or more α-helices. Phylogenetic analyses revealed that connecting the plastid with the host metabolism was mainly a process driven by the host cell. In Arabidopsis, 58% of the metabolite transporters are of host origin, whereas only 12% are attributable to the cyanobacterial endosymbiont. This review focuses on the metabolite transporters of the inner envelope membrane of plastids, in particular the electrochemical potential-driven class of transporters. Recent advances in elucidating the plastidial complement of metabolite transporters are provided, with an update on phylogenetic relationship of selected proteins.

The SnRK1 Kinase as Central Mediator of Energy Signaling between Different Organelles

“…In addition to effects on amino acid degradation, these findings point to a role of bZIP63 in coordinating subcellular metabolism. The malate shuttle across the chloroplast envelope is essential for the transport of 2-oxoglutarate and Glu between cytosol and chloroplast (Facchinelli and Weber, 2011), and thereby automatically also affects mitochondrial metabolism. Hence, it is interesting to speculate that SnRK1 coordinates the subcellular C/N balance not only by phosphorylating NR, Suc-P synthase, or F2KP, but also via transcriptional control mediated by bZIP63 leading to allocation of organic and amino acids between multiple compartments.…”

Signaling pathway in development of Camellia oleifera nurse seedling grafting union

“…At the same time, DHAP is converted into phosphoglycerate (PGA) in the presence of TPI and GAPDH (Ikemoto et al 2003). PGA is converted into phosphoenolpyruvate (PEP) with entering into second metabolism (Facchinelli and Weber 2011). Calcium can increase the second metabolism, to produce the chlorogenic acid (Ngadze et al 2014), such as cinnamic acid and coumaric acid (Clifford et al 2003).…”

The basic genetic toolkit to move in with your photosynthetic partner

“…It has been suggested that the diverse plastid-localized antiporters of the nucleotide-sugar/triose phosphate translocator (NST) family, which are essential to mobilize different carbon compounds (e.g., phosphorylated 3-, 5-, and 6-carbon sugars) across the plastid inner membrane, evolved from a "generalist" transporter selected from the host endomembrane system to extract carbohydrates from the endosymbiont (Weber et al, 2006;Facchinelli and Weber, 2011) (Figure 1B). Interestingly, alternative solutions may have evolved to take advantage of the endosymbiont photosynthates and different membrane transporters have been recruited to translocate metabolites from the photosynthetic compartment.…”

“…Other plastid-localized transporters that regulate the export and import of diverse metabolites, such as 2-oxoglutarate, glucose-6-P, ribose-5-P, pyruvate, and tetrahydrofolate, evolved from proteins encoded in the host genome. The evidence suggests that a basic set of metabolite membrane transporters has been fundamental to highjack photosynthetic endosymbionts and initiate the metabolic integration (Tyra et al, 2007;Facchinelli and Weber, 2011).…”