Linking Gene Expression and Membrane Lipid Composition of<i>Arabidopsis</i>

Szymański, Jędrzej; Brotman, Yariv; Willmitzer, Lothar; Cuadros-Inostroza, Álvaro

doi:10.1105/tpc.113.118919

Cited by 68 publications

(55 citation statements)

References 83 publications

(106 reference statements)

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“…Oleosins also appear to play an important role in determining LD size during seed development when these organelles are being formed (Miquel et al, 2014). However, beyond oleosins, only a relatively small number of other LD proteins have been identified in plants Gidda et al, 2013;Horn et al, 2013;Szymanski et al, 2014), and their roles in the biogenesis of LDs (including their growth, fusion, turnover, size, and quantity), especially outside of seed tissues, remain mostly unknown. On the other hand, some proteins in mammals and yeast that are involved in LD formation and turnover are conserved in plants (e.g., CGI-58; James et al, 2010;Park et al, 2013), and the heterologous expression of plant oleosins in yeast promotes the formation of LDs from the ER (Jacquier et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Arabidopsis SEIPIN Proteins Modulate Triacylglycerol Accumulation and Influence Lipid Droplet Proliferation

et al. 2015

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The lipodystrophy protein SEIPIN is important for lipid droplet (LD) biogenesis in human and yeast cells. In contrast with the single SEIPIN genes in humans and yeast, there are three SEIPIN homologs in Arabidopsis thaliana, designated SEIPIN1, SEIPIN2, and SEIPIN3. Essentially nothing is known about the functions of SEIPIN homologs in plants. Here, a yeast (Saccharomyces cerevisiae) SEIPIN deletion mutant strain and a plant (Nicotiana benthamiana) transient expression system were used to test the ability of Arabidopsis SEIPINs to influence LD morphology. In both species, expression of SEIPIN1 promoted accumulation of large-sized lipid droplets, while expression of SEIPIN2 and especially SEIPIN3 promoted small LDs. Arabidopsis SEIPINs increased triacylglycerol levels and altered composition. In tobacco, endoplasmic reticulum (ER)-localized SEIPINs reorganized the normal, reticulated ER structure into discrete ER domains that colocalized with LDs. N-terminal deletions and swapping experiments of SEIPIN1 and 3 revealed that this region of SEIPIN determines LD size. Ectopic overexpression of SEIPIN1 in Arabidopsis resulted in increased numbers of large LDs in leaves, as well as in seeds, and increased seed oil content by up to 10% over wild-type seeds. By contrast, RNAi suppression of SEIPIN1 resulted in smaller seeds and, as a consequence, a reduction in the amount of oil per seed compared with the wild type. Overall, our results indicate that Arabidopsis SEIPINs are part of a conserved LD biogenesis machinery in eukaryotes and that in plants these proteins may have evolved specialized roles in the storage of neutral lipids by differentially modulating the number and sizes of lipid droplets.

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Section: Introductionmentioning

confidence: 99%

Arabidopsis SEIPIN Proteins Modulate Triacylglycerol Accumulation and Influence Lipid Droplet Proliferation

et al. 2015

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“…Most recently, strictly coordinated gene expression at the biochemical pathway level in parallel with changes of specific glycerolipid pools was reported in Arabidopsis in response to light and temperature stimuli (Szymanski et al, 2014). Nonetheless, how glycerolipid composition is mechanistically modulated between the two glycerolipid pathways and precisely what factors are involved in this process remain largely unknown.…”

Section: Introductionmentioning

confidence: 99%

Understanding the Biochemical Basis of Temperature-Induced Lipid Pathway Adjustments in Plants

et al. 2015

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Glycerolipid biosynthesis in plants proceeds through two major pathways compartmentalized in the chloroplast and the endoplasmic reticulum (ER). The involvement of glycerolipid pathway interactions in modulating membrane desaturation under temperature stress has been suggested but not fully explored. We profiled glycerolipid changes as well as transcript dynamics under suboptimal temperature conditions in three plant species that are distinctively different in the mode of lipid pathway interactions. In Arabidopsis thaliana, a 16:3 plant, the chloroplast pathway is upregulated in response to low temperature, whereas high temperature promotes the eukaryotic pathway. Operating under a similar mechanistic framework, Atriplex lentiformis at high temperature drastically increases the contribution of the eukaryotic pathway and correspondingly suppresses the prokaryotic pathway, resulting in the switch of lipid profile from 16:3 to 18:3. In wheat (Triticum aestivum), an 18:3 plant, low temperature also influences the channeling of glycerolipids from the ER to chloroplast. Evidence of differential trafficking of diacylglycerol moieties from the ER to chloroplast was uncovered in three plant species as another layer of metabolic adaptation under temperature stress. We propose a model that highlights the predominance and prevalence of lipid pathway interactions in temperature-induced lipid compositional changes.

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“…We followed the approach of Collins et al (2016) to generate a target list that contains oxidized lipids from an established conventional lipid target list Szymanski et al, 2014;Pant et al, 2015) developed by Giavalisco et al (2011). Among others, this list of 2,009 entries contains storage and membrane lipids and FAs classified according to acyl/alkyl chain length and number of double bonds.…”

Section: Generation Of An Oxylipid Target Listmentioning

confidence: 99%

Structure Annotation and Quantification of Wheat Seed Oxidized Lipids by High-Resolution LC-MS/MS

2017

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Lipid oxidation is a process ubiquitous in life, but the direct and comprehensive analysis of oxidized lipids has been limited by available analytical methods. We applied high-resolution liquid chromatography-mass spectrometry (LC-MS) and tandem mass spectrometry (MS/MS) to quantify oxidized lipids (glycerides, fatty acids, phospholipids, lysophospholipids, and galactolipids) and implemented a platform-independent high-throughput-amenable analysis pipeline for the high-confidence annotation and acyl composition analysis of oxidized lipids. Lipid contents of 90 different naturally aged wheat (Triticum aestivum) seed stocks were quantified in an untargeted high-resolution LC-MS experiment, resulting in 18,556 quantitative mass-to-charge ratio features. In a posthoc liquid chromatography-tandem mass spectrometry experiment, high-resolution MS/MS spectra (5 mD accuracy) were recorded for 8,957 out of 12,080 putatively monoisotopic features of the LC-MS data set. A total of 353 nonoxidized and 559 oxidized lipids with up to four additional oxygen atoms were annotated based on the accurate mass recordings (1.5 ppm tolerance) of the LC-MS data set and filtering procedures. MS/MS spectra available for 828 of these annotations were analyzed by translating experimentally known fragmentation rules of lipids into the fragmentation of oxidized lipids. This led to the identification of 259 nonoxidized and 365 oxidized lipids by both accurate mass and MS/MS spectra and to the determination of acyl compositions for 221 nonoxidized and 295 oxidized lipids. Analysis of 15-year aged wheat seeds revealed increased lipid oxidation and hydrolysis in seeds stored in ambient versus cold conditions. Lipid oxidation is a process inevitably connected to life. Although essential for all respiring organisms, oxygen can form reactive species (ROS). The accumulation of these compounds leads to the phenomenon commonly referred to as oxidative stress in microbes and plant and animal tissues. ROS play a role in the attack against microbial pathogens by host cells (Imlay, 2013), time-dependent death of dormant seeds (Lee et al., 2010), human diseases (Coyle and Puttfarcken, 1993;Giugliano et al., 1996), in aging (Sohal and Weindruch, 1996;Sohal et al., 2002), and in signaling processes (Gilroy et al., 2016;Mignolet-Spruyt et al., 2016) Unlike oxidized fatty acids (FAs), oxidized lipids are hardly available commercially. Targeted liquid chromatography-mass spectrometry (LC-MS) analysis of oxidized lipids using authentic standards is not very common (Hui et al., 2010;Ravandi et al., 2014). Often, oxidized lipids are detected using tandem mass spectrometry (MS/MS), where the collision-induced products of precursor ions (PRs) are scanned for fragments or neutral losses (NLs) that correspond to oxidized acyl residues expected in oxidized lipids (Spickett and Pitt, 2015), and in some cases, higher resolution MS/MS spectra are provided to support the identification (Buseman et al., 2006;Vu et al., 2012).High-resolution mass spectrometry (MS) allows for ...

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Linking Gene Expression and Membrane Lipid Composition ofArabidopsis

Cited by 68 publications

References 83 publications

Arabidopsis SEIPIN Proteins Modulate Triacylglycerol Accumulation and Influence Lipid Droplet Proliferation

Arabidopsis SEIPIN Proteins Modulate Triacylglycerol Accumulation and Influence Lipid Droplet Proliferation

Understanding the Biochemical Basis of Temperature-Induced Lipid Pathway Adjustments in Plants

Structure Annotation and Quantification of Wheat Seed Oxidized Lipids by High-Resolution LC-MS/MS

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