Consequences of ω-6-Oleate Desaturase Deficiency on Lipid Dynamics and Functional Properties of Mitochondrial Membranes ofArabidopsis thaliana

Caiveau, Olivier; Fortune, David H.; Cantrel, Catherine; Zachowski, Alain; Moreau, F.

doi:10.1074/jbc.m006231200

Cited by 48 publications

(24 citation statements)

References 32 publications

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“…We took advantage of two mutant Arabidopsis cell lines, fad2 and Fad3 1 , which are affected in their fatty acid desaturases. The 18:1 desaturase is shut down in the fad2 mutant (Okuley et al, 1994), resulting in an accumulation of 18:1 fatty acids (Caiveau et al, 2001), whereas the Fad3 1 mutant accumulates 18:3 fatty acids (Shah et al, 1997). Given the important role played by lipids with saturated fatty acyl chains in regulating the physicochemical properties of biological membranes, it was particularly interesting to check DRM formation in these two cell lines, which exhibit significant differences in the mean fluidity (defined as temperaturedependent lipid movements in the membrane) of their PM, compared to the PM of wild-type cells (Vaultier et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

“…Because of their deficit in 18:1 desaturase (Okuley et al, 1994), fad2 cells accumulate fatty acyl chains enriched in 18:1 (Caiveau et al, 2001), whereas the Fad3 1 mutant accumulates 18:3 fatty acids (Shah et al, 1997).…”

Section: Impact Of the Fatty Acid Unsaturation Degree On Lipid Microdmentioning

confidence: 99%

“…Thus, the important changes in the fatty acid composition of fad2 and Fad3 1 membranes (Shah et al, 1997;Caiveau et al, 2001), and therefore their different and PM DRMs (small dots) represent the means 6 SD of four and seven replicates, respectively. B, Values for GA (black dots) and GA DRMs (white) represent the means 6 SD of three replicates.…”

Section: Impact Of the Fatty Acid Unsaturation Degree On Lipid Microdmentioning

confidence: 99%

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Insights into the Role of Specific Lipids in the Formation and Delivery of Lipid Microdomains to the Plasma Membrane of Plant Cells

et al. 2006

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The existence of sphingolipid-and sterol-enriched microdomains, known as lipid rafts, in the plasma membrane (PM) of eukaryotic cells is well documented. To obtain more insight into the lipid molecular species required for the formation of microdomains in plants, we have isolated detergent (Triton X-100)-resistant membranes (DRMs) from the PM of Arabidopsis (Arabidopsis thaliana) and leek (Allium porrum) seedlings as well as from Arabidopsis cell cultures. Here, we show that all DRM preparations are enriched in sterols, sterylglucosides, and glucosylceramides (GluCer) and depleted in glycerophospholipids. The GluCer of DRMs from leek seedlings contain hydroxypalmitic acid. We investigated the role of sterols in DRM formation along the secretory pathway in leek seedlings. We present evidence for the presence of DRMs in both the PM and the Golgi apparatus but not in the endoplasmic reticulum. In leek seedlings treated with fenpropimorph, a sterol biosynthesis inhibitor, the usual D 5 -sterols are replaced by 9b,19-cyclopropylsterols. In these plants, sterols and hydroxypalmitic acid-containing GluCer do not reach the PM, and most DRMs are recovered from the Golgi apparatus, indicating that D 5 -sterols and GluCer play a crucial role in lipid microdomain formation and delivery to the PM. In addition, DRM formation in Arabidopsis cells is shown to depend on the unsaturation degree of fatty acyl chains as evidenced by the dramatic decrease in the amount of DRMs prepared from the Arabidopsis mutants, fad2 and Fad31, affected in their fatty acid desaturases.Despite the ongoing debate on the size, lifespan, and dynamics of lipid microdomains (Munro, 2003;Pike, 2004;Nichols, 2005;Hancock, 2006), the existence of sterol-and sphingolipid-enriched membrane microdomains in the plasma membrane (PM) of eukaryotic cells is now well recognized (Simons and Ikonen, 1997;Brown and London, 2000;Simons and Toomre, 2000;Bagnat and Simons, 2002;Simons and Vaz, 2004;Hancock, 2006). Evidence for microdomains comes in part from examination of membrane constituents that are resistant to solubilization by nonionic detergents at low temperature, giving rise to the concept of lipid rafts (Simons and Ikonen, 1997;Brown and London, 1998;Rö per et al., 2000;Hancock, 2006). Such steroland sphingolipid-enriched microdomains can be isolated as detergent-resistant membranes (DRMs). In the following, the terms of DRMs and microdomains will be assigned to respectively indicate the isolated entities and the corresponding membrane entities. Lipid properties of microdomains are similar to liquid-ordered domains, which are characterized by tightly packed hydrocarbon tails but with a high degree of lateral mobility (Brown and London, 2000;Simons and Vaz, 2004). Cholesterol is thought to contribute to the tight packing of lipids in liquid-ordered domains by filling interstitial spaces between lipid molecules (Brown, 1998)

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Section: Discussionmentioning

confidence: 99%

Section: Impact Of the Fatty Acid Unsaturation Degree On Lipid Microdmentioning

confidence: 99%

Section: Impact Of the Fatty Acid Unsaturation Degree On Lipid Microdmentioning

confidence: 99%

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Insights into the Role of Specific Lipids in the Formation and Delivery of Lipid Microdomains to the Plasma Membrane of Plant Cells

et al. 2006

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“…Membrane Potential and Oxygen Consumption-Membrane potential was measured continuously and simultaneously to oxygen consumption using a tetraphenylphosphonium (TPP ϩ )-sensitive electrode in the presence of 4 M TPP ϩ and a Clark-type oxygen electrode at 20°C (14). The membrane potential values were calculated using the equation of Kamo et al (15) (16).…”

Section: Methodsmentioning

confidence: 99%

Alteration of Plant Mitochondrial Proton Conductance by Free Fatty Acids

Cabassa¹,

Mesneau²,

Miroux³

et al. 2002

Journal of Biological Chemistry

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We characterized the uncoupling activity of the plant uncoupling protein from Solanum tuberosum (StUCP) using mitochondria from intact potato tubers or from yeast (Saccharomyces cerevisiae) expressing the StUCP gene. Compared with mitochondria from transfected yeast, StUCP is present at very low levels in intact potato mitochondrial membranes (at least thirty times lower) as shown by immunodetection with anti-UCP1 antibodies. Under conditions that ruled out undesirable effects of nucleotides and free fatty acids on uncoupling activity measurement in plant mitochondria, the linoleic acid-induced depolarization in potato mitochondria was insensitive to the nucleotides ATP, GTP, or GDP. In addition, sensitivity to linoleic acid was similar in potato and in control yeast mitochondria, suggesting that uncoupling occurring in potato mitochondria was because of a UCP-independent proton diffusion process. By contrast, yeast mitochondria expressing StUCP exhibited a higher sensitivity to free fatty acids than those from the control yeast and especially a marked proton conductance in the presence of low amounts of linoleic acid. However, this fatty acid-induced uncoupling was also insensitive to nucleotides. Altogether, these results suggest that uncoupling of oxidative phosphorylation and heat production cannot be the dominant feature of StUCP expressed in native potato tissues. However, it could play a role in preventing reactive oxygen species production as proposed for mammalian UCP2 and UCP3.The discovery in plants of a mitochondrial uncoupling protein resembling uncoupling proteins from mammals raised the possibility of a new uncoupling mechanism involving a transport pathway for backflow of protons into the matrix of plant mitochondria (1, 2). Indeed, a protein fraction containing a purine nucleotide-sensitive, free fatty acid-activated uncoupling activity, called PUMP, has been isolated from potato tuber mitochondria and characterized after reconstitution in proteoliposomes (1). In addition, various cDNAs coding for putative UCPs were identified in plants such as potato, Arabidopsis thaliana, and skunk cabbage (Symplocarpus foetidus), a thermogenic plant from the Aracea family (3-6). Recently, the Arabidopsis thaliana AtUCP1 gene was expressed in Escherichia coli and the isolated protein reconstituted into liposomes (7). Like mammalian UCPs, the plant UCP 1 requires free fatty acids for its activity and is inhibited by purine nucleotides (GDP, ATP, GTP, or ADP) (7-10). At the mitochondrial level, it has been proposed that ATP, GTP, or GDP were absolutely required to get a fully coupled state in potato tuber mitochondria oxidizing succinate (1, 8). Similarly, it has been suggested that the fatty acid-induced uncoupling in wheat mitochondria was sensitive to purine nucleotides (11).In this paper, we sought to characterize better the properties of plant UCP-like protein by comparing the fatty acid-dependent uncoupling capacity of either native UCP present in intact potato mitochondria or StUCP expressed at a high lev...

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“…Mutations for FAD2 and FAD5 desaturases impair plant growth under low temperature, and fad2 mutant plants show a much more severe phenotype than the fad5 mutant under low temperature growth (Kunst et al, 1989;Hugly and Somerville, 1992;Miquel et al, 1993). The FAD2 mutation abolishes 18:1 desaturation in the ER pathway, thus reducing desaturation of ER-derived MGDG and DGDG in the plastid and desaturation of mitochondrial membrane lipids, including PC, PE, DPG, PI, and PG (Caiveau et al, 2001). In this study, we found that the ADS2 mutation resulted in higher 16:0 and 18:0 and lower 16:3 and 18:3 content under 6°C growth conditions, indicating that ads2 mutant plants lose their ability to increase FA desaturation in response to low temperature exposure (Table 1).…”

Section: Association Of Fa Desaturation With Cold and Freezing Tolerancementioning

confidence: 99%

ACYL-LIPID DESATURASE2Is Required for Chilling and Freezing Tolerance inArabidopsis

2013

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Fatty acid desaturation of membrane lipids is a strategy for plants to survive chilling or freezing temperature. To further characterize enzymes involved in this stress response pathway, ACYL-LIPID DESATURASE2 (ADS2; Enzyme Commission 1.14.99) was studied using genetic, cell, and biochemical approaches. ads2 mutant plants appear similar to the wild type under standard growth conditions but display a dwarf and sterile phenotype when grown at 6°C and also show increased sensitivity to freezing temperature. Fatty acid composition analysis demonstrated that ads2 mutant plants at 6°C have reduced levels of 16:1, 16:2, 16:3, and 18:3 and higher levels of 16:0 and 18:0 fatty acids compared with the wild type. Lipid profiling revealed that 34C species of phosphatidylglycerol (PG) and monogalactosyl diacylglycerol (MGDG) content in ads2 mutants were lower and phosphatidic acid, phosphatidylinositol, phosphatidylethanolamine, phosphatidylcholine, lyso-phosphatidylcholine, and phosphatidylserine were higher than the wild type. Subcellular localization of C-and N-terminal enhanced fluorescence fusion proteins indicated that ADS2 localized primarily to the endoplasmic reticulum, although signal was also confirmed in Golgi and plastids. A double mutation with a putative plastid ADS3 paralog exacerbates the growth defects of ads2 mutant plants under low temperature. These observations suggest that ADS2 encodes a 16:0 desaturase of MGDG and PG. We hypothesize that a low temperature-induced shift from the plastid to endoplasmic reticulum pathway for membrane lipid biosynthesis is required for the cold stress response in Arabidopsis thaliana, and ADS2 is essential to adjust the acyl composition of organelle membrane lipid composition in response to cold stress.

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Consequences of ω-6-Oleate Desaturase Deficiency on Lipid Dynamics and Functional Properties of Mitochondrial Membranes ofArabidopsis thaliana

Cited by 48 publications

References 32 publications

Insights into the Role of Specific Lipids in the Formation and Delivery of Lipid Microdomains to the Plasma Membrane of Plant Cells

Insights into the Role of Specific Lipids in the Formation and Delivery of Lipid Microdomains to the Plasma Membrane of Plant Cells

Alteration of Plant Mitochondrial Proton Conductance by Free Fatty Acids

ACYL-LIPID DESATURASE2Is Required for Chilling and Freezing Tolerance inArabidopsis

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