Lipid transport required to make lipids of photosynthetic membranes

Abstract

Photosynthetic membranes provide much of the usable energy for life on earth. To produce photosynthetic membrane lipids, multiple transport steps are required, including fatty acid export from the chloroplast stroma to the endoplasmic reticulum, and lipid transport from the endoplasmic reticulum to the chloroplast envelope membranes. Transport of hydrophobic molecules through aqueous space is energetically unfavorable and must be catalyzed by dedicated enzymes, frequently on specialized membrane structures. Here, we review photosynthetic membrane lipid transport to the chloroplast in the context of photosynthetic membrane lipid synthesis. We independently consider the identity of transported lipids, the proteinaceous transport components, and membrane structures which may allow efficient transport. Recent advances in lipid transport of chloroplasts, bacteria, and other systems strongly suggest that lipid transport is achieved by multiple mechanisms which include membrane contact sites with specialized protein machinery. This machinery is likely to include the TGD1, 2, 3 complex with the TGD5 and TGD4/LPTD1 systems, and may also include a number of proteins with domains similar to other membrane contact site lipid-binding proteins. Importantly, the likelihood of membrane contact sites does not preclude lipid transport by other mechanisms including vectorial acylation and vesicle transport. Substantial progress is needed to fully understand all photosynthetic membrane lipid transport processes and how they are integrated.

Reorganization of Acyl Flux through the Lipid Metabolic Network in Oil-Accumulating Tobacco Leaves

“…All other membrane lipids initially accumulated little radiolabel, but slowly increased over time. This is consistent with the redistribution of nascent fatty acids from PC to other lipids through acyl editing (Bates et al, 2007;Bates, 2016) and the conversion of MGDG to DGDG within the plastid (Kelly and Dörmann, 2004;Hurlock et al, 2014;LaBrant et al, 2018).…”

“…Third, the reduction in eukaryotic galactolipid synthesis of the HO line may also be due to reduced turnover of PC to produce the PC-derived substrate for galactolipid synthesis, or to the commandeering of that PC-derived substrate for TAG biosynthesis. The identity of the eukaryotic pathway substrate that is transferred from the ER to the plastid is not clear, and leading candidates include PC, PC-derived PA, and/or DAG (Hurlock et al, 2014;LaBrant et al, 2018;Karki et al, 2019). If PC-derived DAG is the substrate that is transferred from the ER to the chloroplast for galactolipid synthesis, then the overexpressed AtDGAT1 may compete for the PC-derived DAG substrate in the ER and reduce its transfer to the chloroplast for eukaryotic galactolipid synthesis.…”

“…Plant leaves have two parallel metabolic pathways of glycerol-3-phosphate (G3P) acylation to produce membrane glycerolipids, and these have been characterized biochemically and genetically over the past 50 years, and reviewed extensively (e.g. Roughan and Slack, 1982;Ohlrogge and Browse, 1995;Li-Beisson et al, 2013;Hurlock et al, 2014;Allen et al, 2015;LaBrant et al, 2018;Hölzl and Dörmann, 2019). In brief, plants synthesize fatty acids while esterified to acyl carrier proteins (ACPs) in the plastid.…”

“…that is transported from the ER to the plastid is unclear-it could be PC, or the PC-derived intermediates PA or DAG (Hurlock et al, 2014;Maréchal and Bastien, 2014;LaBrant et al, 2018;Karki et al, 2019).…”

Arabidopsis TRM5 encodes a nuclear-localised bifunctional tRNA guanine and inosine-N1-methyltransferase that is important for growth

“…, we could observe only one event of protein downregulation due to decreased transcript level: the lipid transfer protein (AT2G45180) which is involved in lipid transport in chloroplasts. Lipid transport is crucial in the formation of photosynthetic membranes in plants(63). As several lipids are important functional components of thylakoidal protein complexes involved in photosynthesis, the impacted lipid transport and lipid synthesis revealed by the GO term analysis may contribute to the observed dysregulation of photosynthesis-related genes.…”