Regulation of Plant Lipid Metabolism

A special issue of Metabolites (ISSN 2218-1989). This special issue belongs to the section "Lipid Metabolism".

Deadline for manuscript submissions: closed (15 June 2021) | Viewed by 14650

Special Issue Editors

1. The Roy J. Carver Department of Biochemistry, Biophysics and Molecular Biology, Iowa State University, Ames, IA 50011, USA
2. Center for Metabolic Biology, Iowa State University, Ames, IA 50011, USA
Interests: biochemistry; molecular biology; regulation of plant lipid metabolism
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Guest Editor
1. Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA, USA
2. Center for Metabolic Biology, Iowa State University, Ames, IA 50011, USA
Interests: genetics; plant biology; plant biochemistry; cuticular lipids; abiotic stress

Special Issue Information

Dear Colleagues,

Lipids are important components of all biological systems, providing the molecular framework for many biological functions, including structural, protective, signaling, and energy storage. Foremost among these functionalities is the hydrophobic nature of lipids, which is the physical driving force for the sequestration of water-immiscible molecules from water-miscible molecules. This physical separation is the molecular driving force for many of these biological processes. For example, the membrane as an impermeable barrier sequesters biological processes at both the intracellular and intercellular levels. Moreover, this membrane barrier provides the medium for constraining biological processes to two dimensions. Additionally, lipids are also associated with many signaling or mediator processes that manifest regulatory control on dynamic processes and protection against environmental stressors, and these are inevitably associated with the hydrophobic nature of these molecules. Nonetheless, despite the relatively simple physical property that is at the core of the functionality of lipids, biological systems have evolved an ability to generate many thousands of different lipid molecules with distinct functions.

The distinctive evolutionary trajectory of plants manifests complex regulatory mechanisms at different levels of regulation (e.g., gene regulatory networks, signaling networks, feedback, and feed-forward regulation) that facilitate unique spatial and temporal patterns of lipid metabolism as these organisms respond to different developmental, genetic and environmental cues. Furthermore, plant metabolic processes generate unique complex lipophilic polymers that act as extracellular barriers (e.g., cutin and suberin). Exclusively in plants, lipid metabolism coordinates and integrates processes that occur in several subcellular compartments, some of which appear to be redundant. This is primarily associated with the evolutionary history of plastids (e.g., chloroplasts) and mitochondria as evolutionary products of ancient endosymbiotic events. Additionally, plant systems not only assemble lipids as structural components of membranes, but these lipid molecules are metabolic intermediates in the assembly of more complex lipid molecules—for example, acyl-chain desaturases that utilize complex membrane lipids as substrates. This Special Issue of Metabolites will be dedicated to publishing current advances in dissecting the dynamic metabolic and genetic networks that regulate lipid metabolic processes in response to diverse cues, and that occur uniquely in plant systems.

Dr. Basil Nikolau
Dr. Marna D Yandeau-Nelson
Guest Editor

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Published Papers (5 papers)

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Research

13 pages, 1998 KiB  
Article
Co-Expression of Lipid Transporters Simultaneously Enhances Oil and Starch Accumulation in the Green Microalga Chlamydomonas reinhardtii under Nitrogen Starvation
by Ru Chen, Yasuyo Yamaoka, Yanbin Feng, Zhanyou Chi, Song Xue and Fantao Kong
Metabolites 2023, 13(1), 115; https://doi.org/10.3390/metabo13010115 - 10 Jan 2023
Cited by 12 | Viewed by 2649
Abstract
Lipid transporters synergistically contribute to oil accumulation under normal conditions in microalgae; however, their effects on lipid metabolism under stress conditions are unknown. Here, we examined the effect of the co-expression of lipid transporters, fatty acid transporters, (FAX1 and FAX2) and ABC transporter [...] Read more.
Lipid transporters synergistically contribute to oil accumulation under normal conditions in microalgae; however, their effects on lipid metabolism under stress conditions are unknown. Here, we examined the effect of the co-expression of lipid transporters, fatty acid transporters, (FAX1 and FAX2) and ABC transporter (ABCA2) on lipid metabolism and physiological changes in the green microalga Chlamydomonas under nitrogen (N) starvation. The results showed that the TAG content in FAX1-FAX2-ABCA2 over-expressor (OE) was 2.4-fold greater than in the parental line. Notably, in FAX1-FAX2-ABCA2-OE, the major membrane lipids and the starch and cellular biomass content also significantly increased compared with the control lines. Moreover, the expression levels of genes directly involved in TAG, fatty acid, and starch biosynthesis were upregulated. FAX1-FAX2-ABCA2-OE showed altered photosynthesis activity and increased ROS levels during nitrogen (N) deprivation. Our results indicated that FAX1-FAX2-ABCA2 overexpression not only enhanced cellular lipids but also improved starch and biomass contents under N starvation through modulation of lipid and starch metabolism and changes in photosynthesis activity. The strategy developed here could also be applied to other microalgae to produce FA-derived energy-rich and value-added compounds. Full article
(This article belongs to the Special Issue Regulation of Plant Lipid Metabolism)
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21 pages, 2563 KiB  
Article
Heterologous Expression and Characterization of Plant Wax Ester Producing Enzymes
by Daolin Cheng, Ling Li, Ludmila Rizhsky, Priyanka Bhandary and Basil J. Nikolau
Metabolites 2022, 12(7), 577; https://doi.org/10.3390/metabo12070577 - 22 Jun 2022
Cited by 1 | Viewed by 2034
Abstract
Wax esters are widely distributed among microbes, plants, and mammals, and they serve protective and energy storage functions. Three classes of enzymes catalyze the reaction between a fatty acyl alcohol and a fatty acyl-CoA, generating wax esters. Multiple isozymes of two of these [...] Read more.
Wax esters are widely distributed among microbes, plants, and mammals, and they serve protective and energy storage functions. Three classes of enzymes catalyze the reaction between a fatty acyl alcohol and a fatty acyl-CoA, generating wax esters. Multiple isozymes of two of these enzyme classes, the membrane-bound O-acyltransferase class of wax synthase (WS) and the bifunctional wax synthase/diacylglycerol acyl transferase (WSD), co-exist in plants. Although WSD enzymes are known to produce the wax esters of the plant cuticle, the functionality of plant WS enzymes is less well characterized. In this study, we investigated the phylogenetic relationships among the 12 WS and 11 WSD isozymes that occur in Arabidopsis, and established two in vivo heterologous expression systems, in the yeast Saccharomyces cerevisiae and in Arabidopsis seeds to investigate the catalytic abilities of the WS enzymes. These two refactored wax assembly chassis were used to demonstrate that WS isozymes show distinct differences in the types of esters that can be assembled. We also determined the cellular and subcellular localization of two Arabidopsis WS isozymes. Additionally, using publicly available Arabidopsis transcriptomics data, we identified the co-expression modules of the 12 Arabidopsis WS coding genes. Collectively, these analyses suggest that WS genes may function in cuticle assembly and in supporting novel photosynthetic function(s). Full article
(This article belongs to the Special Issue Regulation of Plant Lipid Metabolism)
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30 pages, 4792 KiB  
Article
Specific Changes in Arabidopsis thaliana Rosette Lipids during Freezing Can Be Associated with Freezing Tolerance
by Hieu Sy Vu, Sunitha Shiva, Thilani Samarakoon, Maoyin Li, Sujon Sarowar, Mary R. Roth, Pamela Tamura, Samuel Honey, Kaleb Lowe, Hollie Porras, Neema Prakash, Charles A. Roach, Morgan Stuke, Xuemin Wang, Jyoti Shah, Gary Gadbury, Haiyan Wang and Ruth Welti
Metabolites 2022, 12(5), 385; https://doi.org/10.3390/metabo12050385 - 23 Apr 2022
Cited by 2 | Viewed by 2708 | Correction
Abstract
While the roles of a few specific lipids in plant freezing tolerance are understood, the effect of many plant lipids remains to be determined. Acclimation of plants to non-freezing cold before exposure to freezing temperatures improves the outcome of plants, compared to plants [...] Read more.
While the roles of a few specific lipids in plant freezing tolerance are understood, the effect of many plant lipids remains to be determined. Acclimation of plants to non-freezing cold before exposure to freezing temperatures improves the outcome of plants, compared to plants exposed to freezing without acclimation. Arabidopsis thaliana plants were subjected to one of three treatments: (1) “control”, i.e., growth at 21 °C, (2) “non-acclimated”, i.e., 3 days at 21 °C, 2 h at −8 °C, and 24 h recovery at 21 °C, and (3) “acclimated”, i.e., 3 days at 4 °C, 2 h at −8 °C, and 24 h recovery at 21 °C. Plants were harvested at seven time points during the treatments, and lipid levels were measured by direct-infusion electrospray ionization tandem mass spectrometry. Ion leakage was measured at the same time points. To examine the function of lipid species in relation to freezing tolerance, the lipid levels in plants immediately following the freezing treatment were correlated with the outcome, i.e., ion leakage 24-h post-freezing. Based on the correlations, hypotheses about the functions of specific lipids were generated. Additionally, analysis of the lipid levels in plants with mutations in genes encoding patatin-like phospholipases, lipoxygenases, and 12-oxophytodienoic acid reductase 3 (opr3), under the same treatments as the wild-type plants, identified only the opr3-2 mutant as having major lipid compositional differences compared to wild-type plants. Full article
(This article belongs to the Special Issue Regulation of Plant Lipid Metabolism)
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18 pages, 6366 KiB  
Article
Complex Changes in Membrane Lipids Associated with the Modification of Autophagy in Arabidopsis
by Yosia Mugume, Geng Ding, Maria Emilia Dueñas, Meiling Liu, Young-Jin Lee, Basil J. Nikolau and Diane C. Bassham
Metabolites 2022, 12(2), 190; https://doi.org/10.3390/metabo12020190 - 18 Feb 2022
Cited by 8 | Viewed by 2814 | Correction
Abstract
Autophagy is a conserved mechanism among eukaryotes that degrades and recycles cytoplasmic components. Autophagy is known to influence the plant metabolome, including lipid content; however, its impact on the plant lipidome is not fully understood, and most studies have analyzed a single or [...] Read more.
Autophagy is a conserved mechanism among eukaryotes that degrades and recycles cytoplasmic components. Autophagy is known to influence the plant metabolome, including lipid content; however, its impact on the plant lipidome is not fully understood, and most studies have analyzed a single or few mutants defective in autophagy. To gain more insight into the effect of autophagy on lipid concentrations and composition, we quantitatively profiled glycerolipids from multiple Arabidopsis thaliana mutants altered in autophagy and compared them with wild-type seedlings under nitrogen replete (+N; normal growth) and nitrogen starvation (−N; autophagy inducing) conditions. Mutants include those in genes of the core autophagy pathway, together with other genes that have been reported to affect autophagy. Using Matrix-Assisted Laser Desorption/Ionization—Mass Spectrometry (MALDI-MS), we imaged the cellular distribution of specific lipids in situ and demonstrated that autophagy and nitrogen treatment did not affect their spatial distribution within Arabidopsis seedling leaves. We observed changes, both increases and decreases, in the relative amounts of different lipid species in the mutants compared to WT both in +N and −N conditions, although more changes were seen in −N conditions. The relative amounts of polyunsaturated and very long chain lipids were significantly reduced in autophagy-disrupted mutants compared to WT plants. Collectively, our results provide additional evidence that autophagy affects plant lipid content and that autophagy likely affects lipid properties such as chain length and unsaturation. Full article
(This article belongs to the Special Issue Regulation of Plant Lipid Metabolism)
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21 pages, 2908 KiB  
Article
A Role for Inositol Pyrophosphates in the Metabolic Adaptations to Low Phosphate in Arabidopsis
by Eric S. Land, Caitlin A. Cridland, Branch Craige, Anna Dye, Sherry B. Hildreth, Rich F. Helm, Glenda E. Gillaspy and Imara Y. Perera
Metabolites 2021, 11(9), 601; https://doi.org/10.3390/metabo11090601 - 4 Sep 2021
Cited by 11 | Viewed by 3448
Abstract
Phosphate is a major plant macronutrient and low phosphate availability severely limits global crop productivity. In Arabidopsis, a key regulator of the transcriptional response to low phosphate, phosphate starvation response 1 (PHR1), is modulated by a class of signaling molecules called inositol [...] Read more.
Phosphate is a major plant macronutrient and low phosphate availability severely limits global crop productivity. In Arabidopsis, a key regulator of the transcriptional response to low phosphate, phosphate starvation response 1 (PHR1), is modulated by a class of signaling molecules called inositol pyrophosphates (PP-InsPs). Two closely related diphosphoinositol pentakisphosphate enzymes (AtVIP1 and AtVIP2) are responsible for the synthesis and turnover of InsP8, the most implicated molecule. This study is focused on characterizing Arabidopsis vip1/vip2 double mutants and their response to low phosphate. We present evidence that both local and systemic responses to phosphate limitation are dampened in the vip1/vip2 mutants as compared to wild-type plants. Specifically, we demonstrate that under Pi-limiting conditions, the vip1/vip2 mutants have shorter root hairs and lateral roots, less accumulation of anthocyanin and less accumulation of sulfolipids and galactolipids. However, phosphate starvation response (PSR) gene expression is unaffected. Interestingly, many of these phenotypes are opposite to those exhibited by other mutants with defects in the PP-InsP synthesis pathway. Our results provide insight on the nexus between inositol phosphates and pyrophosphates involved in complex regulatory mechanisms underpinning phosphate homeostasis in plants. Full article
(This article belongs to the Special Issue Regulation of Plant Lipid Metabolism)
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