2014/01/01 by Yonghua Li-Beisson, Yonghua Li‐Beisson, Rebecca L Roston +2
Economics, Econometrics and Finance · #Insurance and Financial Risk Management
paper · pdf · doi:10.1093/pcp/pcae061
Lipids are essential for plant growth, signaling, development and environmental adaptation. Plant and algal lipids are also at the core of our energy economy, as polar lipids form photosynthetic membranes while neutral storage lipids (i.e. triacylglycerols, TAGs) represent an energy-dense reservoir of reduced carbon and fuel; as such, they additionally serve as important renewable sources of food, feed, biofuel and industrial feedstocks. These benefits, which are critical to human society, underscore the importance of understanding how lipids are produced and function within plants. Recent advances in lipidomics and lipid imaging, coupled with the development of high throughput, low-cost genome sequencing tools and genome-editing techniques now enable a deeper appreciation of the role of lipids at all scales and in all their states (e.g. as membrane, storage and signaling components). This Special Issue of Plant and Cell Physiology provides a holistic view of plant and algal lipids, especially in terms of their adaptation to environmental challenges. This issue includes three review papers and 12 research articles covering areas from the regulation of lipid synthesis, enzyme structural determinants to the role of lipids in stress management and its relation to photosynthesis. Acyl-lipid biosynthesis starts in the chloroplast where de novo fatty acid synthesis occurs. The newly formed fatty acids are either used by chloroplast-located enzymes to synthesize chloroplast lipids or exported to the endoplasmic reticulum (ER) where they are assembled by ER-resident enzymes to make extra-chloroplast lipids, including TAGs. In higher plants and microalgae, TAG biosynthesis is catalyzed by two distinct acyltransferase families, i.e. the diacylglycerol:acyltransferase (DGAT) and phospholipid:diacylglycerol acyltransferase (PDAT) for the acyl-CoA-dependent and -independent pathway, respectively. Thanks to the specificities of these enzymes, a wide variety of plant oils has been found in nature. Clews et al. (2024) discuss and compare the evolution of specialized oil metabolic pathways in diverse plant species including Arabidopsis thaliana, Ricinus communis (castor bean), Linum usitatissimum L. (flax) and Elaeis guineensis (oil palm). These analyses show that numerous factors such as gene co-expressing networks, divergence in key enzymes/proteins and the subcellular protein context (i.e. within or outside of a functional interactome) all contribute to unique oil accumulation. Furthermore, the development of isotope labeling coupled with mass spectrometry imaging (Tat and Lee 2024) could further aid in the elucidation of lipid metabolism at a spatial level. In addition to the role of TAG as a storage molecule, its metabolism is critical for cellular energy balance, lipid homeostasis, cell growth and stress responses. By catalyzing the transferal of an acyl-chain from a membrane lipid (usually phosphatidylcholine) to DAG, PDAT allows the formation of a TAG molecule and therefore plays a critical role in lipid homeostasis as well as in connecting membrane lipid synthesis and growth with lipid storage. Sah et al. (2024) discuss the multifaceted roles of PDAT and TAG metabolism in cellular physiology. The divergence and similarities between PDAT from microalgae, plants and yeast are also compared. Despite its importance, our knowledge of the regulation of lipid metabolism in plants and algae remains mostly limited to transcriptional regulators. In this issue, Flyckt et al. (2024) provide new data showing that three amino acid substitutions in the DGAT 1b protein can increase soybean oil content by 2.3% and this argumentation is maintained in multiple field trials. To fill the gap in our understanding of post-translational modifications (PTMs) of plant lipid metabolism, Cannon and Horn (2024) have conducted a wide-ranging analysis of PTM proteomics (comparing S-sulfenylation, persulfidation, S-nitrosylation and S-acylation), genomics and protein structures, with a specific focus on proteins involved in plant lipid metabolism. Cysteines are widely present, and these analyses also revealed discernible patterns in lipid biochemical pathways enriched with Cys PTMs, notably involving beta-oxidation, jasmonic acid biosynthesis, fatty acid biosynthesis and wax biosynthesis. The significance of Cys-PTM in cellular physiology and metabolism, however, remains to be investigated experimentally. Nonetheless, this paper highlights the potential importance of Cys-PTMs in lipid metabolism and provides valuable insights for future investigations focusing on molecular mechanisms of Cys modifications. The chloroplast is the main powerhouse of photosynthetic cells where two major pathways occur, i.e. photosynthesis and lipid biosynthesis. Thylakoid membranes are composed of mainly galactolipids and photosynthetic complexes. How cells coordinate the biosynthesis of these two major pathways is not known. It has been reported that suppression of galactolipid biosynthesis decreased the expression of photosynthetic polypeptides. In this issue, Fujii et al. (2024) investigated this question by following gene expression patterns in galactolipid-deficient Arabidopsis seedlings during the de-etiolation process. In combination with genetic analysis, the authors propose a model in which galactolipid synthesis determines the protein homeostasis in the chloroplast through the GENOMES UNCOUPLED1 (GUN1)-mediated plastid-to-nucleus signaling pathway. In addition to lipid amount, fatty acid composition and desaturation levels play key roles in ensuring membrane fluidity and protein function. Many of the fatty acid modification enzymes, notably desaturases, which are essential to modulate fatty acid composition and therefore membrane fluidity and function, are housed within the chloroplast. In this issue, Effendi et al. (2024) report the detailed characterization of two cyanobacteria desaturases, DesC1 and DesC2. Furthermore, the authors demonstrate DesC1 and DesC2 substrate specificities and divergent functions in the two cyanobacteria species. Chloroplasts also import some unsaturated lipid species from the ER for lipid assembly. Matzner et al. (2024) report here the importance of ER-derived desaturated lipids on thylakoid lipid composition and photosynthesis. Plants and algae face a multitude of environmental challenges, most of which require lipid adjustments for efficient tolerance or signaling. Understanding the lipid mechanisms that confer tolerance is needed to engineer their resilience. Seven papers from this special issue delve into the fascinating world of stress responses, offering insights from membranes and protective wax barriers. Several of these explore the role of lipids in maintaining membrane integrity under abiotic stresses. Peng et al. (2024) demonstrate changes in galactolipids (MGDG and DGDG) in rapeseed experiencing nitrogen deficiency. Their findings suggest that the MGDG to DGDG ratio may be important for adapting chloroplast membranes to nutrient stress. Minimal levels of MGDG were also implied by Douchi et al. (2024) to be essential for recovery from desiccation, where they were retained by highly tolerant cyanobacteria Chroococcidiopsis. Interestingly, the same study showed sulfoquinovosyldiacylglycerol (SQDG) levels predominated during desiccation, suggesting a previously unrecognized function of SQDG in tolerance. Similarly, the importance of maintaining membrane fluidity for stress acclimation is underscored by Ishikawa et al. (2024). They identify unusual Δ8-unsaturated sphingolipids with hexuronic acid headgroups in the microalga Ostreococcus tauri. Expression of the Δ8 desaturase was higher at cooler temperatures, and overexpression at normal temperatures was detrimental, likely due to its unknown effect on membrane function. In addition to temperature and water stresses, all eukaryotes can experience ER stress. Such stress can be induced chemically, and Je et al. (2024) show that when sterol biosynthesis was inhibited in Chlamydomonas reinhardtii by mutation of erg5, cells were more sensitive to chemically induced ER stress. This sensitivity was reversed if steps prior to erg5 were inhibited, suggesting that specific sterols contribute to ER membrane health distinctly. van Hooren et al. (2024) demonstrate that overexpression of genes encoding Phospholipase C enhances drought tolerance in Arabidopsis, possibly through changes in shoot architecture, which points to a novel strategy for improving drought resistance via lipid modulation. Collectively, these investigations illustrate how plants strategically modify lipid synthesis and signaling pathways to fortify themselves against physical injury, water scarcity and perturbations of protein homeostasis. Finally, this issue also sheds light on the significance of lipids in forming protective barriers in plants. Papers from Lewandowska et al. (2024) and Campoli et al. (2024) showcase how wax deposition is triggered by stress. Lewandowska et al. demonstrate wound-induced wax biosynthesis in Arabidopsis leaves and show that it depends not only on jasmonic acid but also on abscisic acid (Lewandowska et al. 2024). Campoli et al. (2024), on the other hand, explore the role of a specific lipase (HvGDSL1) in barley that controls wax deposition in various organs, including the grain. Notably, they highlight the importance of waxes for maintaining hull adhesion, thereby protecting the developing embryo. In conclusion, this special issue offers a compelling exploration of plant and algal stress responses. By employing various approaches, the collection of papers illuminates the crucial role of membrane lipids, specific genes and diverse adaptation strategies in ensuring plant and algal resilience in a constantly changing environment. National Science Foundation (2241023) to Y.L.-B. and R.L.R.; The French Atomic and Alternative Energies Commission (CEA) to Y.L.-B.; ANR TOR-DYRKcontrol to Y.L.-B.; France 2030 PEPR B-BEST to Y.L.-B.; United States Department of Energy (SC0021101) to R.L.R.; National Science Foundation (1845175) to R.L.R.; University of Nebraska to R.L.R. We also thank Professor Wataru Sakamoto, former Editor-in-Chief of Plant & Cell Physiology, and Dr. Liliana M. Costa, PCP managing editor for their kind support of this special issue. The authors have no conflicts of interest to declare.