Fatty Acid and Lipid Transport in Plant Cells

FAX1, a novel membrane protein in the inner envelope of chloroplasts, mediates FA export. The discovery and analysis of membrane transporters allows future development of models for transport mechanisms of lipophilic compounds. The flow of FAs from plastids to their final cellular destination in lipid molecules is controlled by membrane-intrinsic and membrane-attached proteins. Plant membrane transporters for FAs and lipid derivatives represent essential components in growth, development, and plant performance. Fatty acids (FAs) and lipids are essential — not only as membrane constituents but also for growth and development. In plants and algae, FAs are synthesized in plastids and to a large extent transported to the endoplasmic reticulum for modification and lipid assembly. Subsequently, lipophilic compounds are distributed within the cell, and thus are transported across most membrane systems. Membrane-intrinsic transporters and proteins for cellular FA/lipid transfer therefore represent key components for delivery and dissemination. In addition to highlighting their role in lipid homeostasis and plant performance, different transport mechanisms for land plants and green algae – in the model systems Arabidopsis thaliana, Chlamydomonas reinhardtii – are compared, thereby providing a current perspective on protein-mediated FA and lipid trafficking in photosynthetic cells. Fatty acids (FAs) and lipids are essential — not only as membrane constituents but also for growth and development. In plants and algae, FAs are synthesized in plastids and to a large extent transported to the endoplasmic reticulum for modification and lipid assembly. Subsequently, lipophilic compounds are distributed within the cell, and thus are transported across most membrane systems. Membrane-intrinsic transporters and proteins for cellular FA/lipid transfer therefore represent key components for delivery and dissemination. In addition to highlighting their role in lipid homeostasis and plant performance, different transport mechanisms for land plants and green algae – in the model systems Arabidopsis thaliana, Chlamydomonas reinhardtii – are compared, thereby providing a current perspective on protein-mediated FA and lipid trafficking in photosynthetic cells. small (10 kDa) conserved ACBPs are implicated in the storage and intracellular distribution of acyl-CoA esters or lipids in eukaryotes. In Arabidopsis, six ACBP proteins with acyl-CoA binding domains exist, and three of them – ACBP4, 5, and 6 – are localized in the cytosol. Only At-ACBP6 represents a 'classical' 10 kDa ACBP, whereas At-ACBP1–3 are about 38–39 kDa, and At-ACBP4 and 5, with additional kelch motif domains, are about 71–73 kDa in size. Thus, ACBP1–5 represent plant-specific proteins. Whereas ACBP3 is targeted to the extracellular space, ACBP1 and 2 contain ankyrin repeats and have a transmembrane domain that attaches them to the ER and plasma membrane. plant ABC transporter ATPases constitute a large membrane-protein family with at least 130 members in Arabidopsis and belong to the ABC Superfamily 3.A.1 (Transporter Classification Database, TCDB: www.tcdb.org). The generalized transport reactions for ABC-type uptake and efflux systems are: (i) solute (out) + ATP → solute (in) + ADP + Pi; and (ii) substrate (in) + ATP → substrate (out) + ADP + Pi, respectively. An ABC transporter complex consists of two transmembrane and two nucleotide-binding domains, which can either be assembled by one or two polypeptide chains of the full- and half-size ABC transporters, respectively. Prokaryotic-type ABC transporter complexes are assembled by four separate subunits plus two or more additional substrate-binding proteins (e.g., the TGD1–3 complex in the chloroplast IE). Proteins in the A, D, and G subfamilies in animals and plants are predominantly involved in transport of lipophilic molecules. starting with LC (C16–18) FAs synthesized in plastids, the eukaryotic pathway of lipid synthesis in plants occurs at the ER where elongation, acyl editing, and lipid assembly take place. Because the ER sn2-acyltransferase has high specificity for C18 FAs, eukaryotic DAG backbones in plant glycerolipids mainly contain C18 acyl chains at the sn2 position. Owing to their endosymbiotic origin, plastids have retained the so-called prokaryotic lipid synthesis pathway, mainly producing plastid-intrinsic galactolipids and PG. The plastid sn2-acyltransferase has an exclusive preference for C16 FAs, thus 'prokaryotic' plastid-produced DAG backbones always have C16 acyl chains at sn2, thereby enabling discrimination of lipid origin. Note that the sn1-acyltransferases in both compartments prefer C18 FAs. LACS enzymes are plant long-chain fatty acid:CoA ligases (AMP-forming) and belong to the IUBMB enzyme class EC 6.2.1.3. LACS or FACS (fatty acid CoA synthetase) are ubiquitously present in pro- and eukaryotic organisms and catalyze the reaction: ATP + (long-chain) fatty acid + CoA → AMP + diphosphate + acyl-CoA (KEGG database: www.genome.jp/kegg/kegg1.html). Owing to their function in FA activation by formation of a thioester with CoA, they play an important role in the so-called process of vectorial acylation. LC FAs have an alkyl chain length of C16–18, whereas VLC FAs have 20 or more carbon atoms (C≥20). the coupling of FA transport across a lipid bilayer membrane – either passive diffusion or transmembrane flip most likely mediated by a membrane-intrinsic protein – with subsequent ATP-dependent FA activation by a LACS/FACS enzyme and delivery for metabolism. Because in this latter step thioester bounds are formed, the process is also referred to as vectorial esterification.